Stress Fractures

Clin Sports Med 25 (2006) xiii

CLINICS IN SPORTS MEDICINE FOREWORD

Stress Fractures

Mark D. Miller, MD Consulting Editor

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nyone who routinely works in a training room is intimately familiar with the stress associated with treating stress fractures: it is not simply a matter of telling an athlete to rest, it is convincing them to join you on a difficult and complex journey that does not always have a definable endpoint. This issue of the Clinics in Sports Medicine offers an up-to-date roadmap for that journey. Dr. Kaeding has hired the best guides available for the trip—so strap on your backpack and join us. Dr. Kaeding has organized this well-conceived issue to cover the science of stress fractures and their classification, treatment, and epidemiology. Imaging is critical in the diagnosis of stress fractures because plain films are often negative. Although pharmacologic treatment is an exciting concept in the treatment of stress fractures, it is not well studied. Treatment, then, must focus on individual stress fractures using an anatomic approach. This issue is a helpful review that can be used to help manage even the most challenging stress fractures. It is hoped that it can be kept at hand as a personal stress reducer while managing these difficult problems in athletes. Mark D. Miller, MD Professor, Department of Orthopaedic Surgery University of Virginia Health System P.O. Box 800753 Charlottesville, VA 22903-0753, USA E-mail address: [email protected]

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Clin Sports Med 25 (2006) xv–xvi

CLINICS IN SPORTS MEDICINE PREFACE

Stress Fractures

Christopher C. Kaeding, MD Guest Editor

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n order for the field of sports medicine to continue to advance, a marriage of clinical observation and basic science is required. Clinical studies and observations help us to understand the clinical course and behavior of pathologic entities. These efforts provide us with evidence of causative factors as well as the efficacy of various interventions. Unfortunately, these clinical reports are often biased and skewed by the author’s opinion, hence the recent emphasis on evidence-based medicine and the strength of evidence in clinical studies. Unfortunately, stress fractures occur with varying grades and locations. The relatively low number of each combination of grade and location seen at one clinical site makes prospective controlled studies difficult. This emphasizes the importance of using a grading system that will allow multicenter observers to compare apples to apples. In every area of medicine, if one reviews the history of progress, a keen clinical observation has at times led to a major breakthrough. This encourages us all to be astute observers of our clinical practices. By being observant, we will see correlations and patterns. These patterns often lead to an increased understanding. An example of this is the classification of stress fractures into high or low risk categories. This contribution stems from observing patterns in the clinical history of stress fractures in different locations. If an observation does not make sense, ask why. Inquisitive observation will make your practice more stimulating and advance the field. This can be done regardless of whether one considers oneself an academic. As our basic science colleagues continue to unveil the secrets of biology, they will benefit from the input of observant clinicians. The clinician facilitates the

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PREFACE

scientist in determining what question to ask and where to look for the answer. Revelations made by research scientists will in turn aid the clinician in determining which interventions stand the best chance of clinical benefit. Recently, the intersection of basic science and clinical care with respect to stress fractures is more apparent. We have only recently started to open the black box of understanding the biologic explanation of why stress fractures occur. Advances continue in the descriptions of the process of bone repair and adaptation as well as the cellular signaling involved. I believe that many of the developing concepts of fatigue failure of in vivo bone will also apply to overuse injuries of other mesenchymal tissue such as tendon. It is with this introduction that I encourage our readers to stay abreast of basic science advances and be inquisitive observers of their clinical practices. Christopher C. Kaeding, MD Division of Sports Medicine Department of Orthopedics Ohio State University 2050 Kenny Road Columbus, OH 43221, USA E-mail address: [email protected]

Clin Sports Med 25 (2006) 1–16

CLINICS IN SPORTS MEDICINE The Pathophysiology of Stress Fractures Michelle Pepper, MDa, Venu Akuthota, MDb, Eric C. McCarty, MDc,* a

Medical College of Wisconsin, Milwaukee, WI, USA Department of Physical Medicine and Rehabilitation, University of Colorado School of Medicine, Denver, CO, USA c Sports Medicine and Shoulder Surgery, Department of Orthopaedic Surgery, University of Colorado School of Medicine, 311 Mapleton Avenue, Boulder, CO 80304, USA b

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s athletes continue to be more competitive in their desire to be the best, they will train exceptionally hard, sometimes to the point of injury. For society generally in the United States, there is a desire to have a better fitness level and the initial zeal of running or getting in shape will occur in such a rapid fashion that injuries will sometimes happen. A common type of injury seen in competitive as well as recreational athletes is the stress fracture. This type of fracture can arise when the stresses on the bone are greater than the capacity of the bone to withstand and heal from the stresses. An understanding of the science and adaptations that occur with human bones when they undergo stress activity is necessary when looking at the causes and pathophysiology of stress fractures. STRESS FRACTURES Bone Basic Science Injury to bone encompasses an array of defects of bone architecture, including bone strains, stress reactions, and nondisplaced and displaced stress fractures. These injuries occur essentially when bone fails to remodel adequately with the application of repetitive subthreshold stress. Because running and jogging involve ground reaction forces that are three to eight times greater than walking, distance runners and track athletes are particularly prone to developing stress fractures. An understanding of bone basic science is needed to illuminate the causes and treatment principles for stress fractures. Bone is a highly organized and dynamic living tissue, with both metabolic and structural components. These components are interdependent and responsive to each other. The metabolic component involves mineral homeostasis and bone remodeling, and the structural component involves maintaining skeletal integrity and bone remodeling.

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At the microscopic level, bone has two forms, woven and lamellar. Woven bone is an immature type found in the embryo and newborn; lamellar bone is a more mature bone and, through remodeling, replaces woven bone by 4 years of age [1]. Lamellar bone is more highly organized, containing stress-oriented collagen, which makes it anisotropic (mechanical properties differ depending on the direction of applied force) [2]. Normal lamellar bone is structurally organized into cortical (compact) bone or cancellous (trabecular) bone. Cortical bone makes up 80% of the skeleton and is composed of tightly packed osteons or a haversian system. Osteons usually are oriented in the long axis of the bone and are connected by haversian canals [3]. Cortical bone is found principally at the diaphysis of long bones and the “shell” of cuboid-like bones such as vertebral bodies and tarsal or carpal bones. Cortical bone is characterized by a metabolic turnover rate that is eight times slower than cancellous bone and four times greater in mass. The majority of stress fractures in runners occur in cortical bone. Cancellous (trabecular) bone is found principally at the metaphysis and epiphysis of long bones and in cuboid-like bones. It is less dense and undergoes more stress remodeling. Clinically, bone mineral density (BMD) studies measure areas containing mostly cancellous bone (vertebral bodies, femoral trochanter, and sacrum) because of its earlier and higher rate of bone turnover and its greater likelihood of demonstrating changes in BMD. There are three major types of bone cells: osteoblasts, osteocytes, and osteoclasts. Osteoblasts are derived from undifferentiated mesenchymal cells. They line the surface of bones and function primarily to produce bone matrix (type I collagen and osteocalcin). Osteoblasts have receptors for parathyroid hormone (PTH) and 1,25-dihydroxyvitamin D [1,4]. Generally, these hormones function systemically through an osteoblastic mediator. PTH directly inhibits osteoblastic formation of osteocalcin, whereas 1,25-dihydroxyvitamin D stimulates osteocalcin formation. Locally, an osteoblast is stimulated by several growth factors, including transforming growth factor β-1, -2, and -3; bone morphogenic proteins 1 through 7; insulin-like growth factors I and II; and acidic and basic fibroblast growth factor [1,4]. Osteocytes are former osteoblasts that have become surrounded with bone mineral matrix (calcified bone). Osteocytes function to maintain bone and control extracellular concentrations of calcium and phosphorus. The final cell type, osteoclasts, is derived from hematopoietic precursors and functions to resorb bone. Osteoclasts bind to the bone surface and resorb an isolated area of bone by dissolving the hydroxyapatite crystals and digesting the collagen. Osteoclasts have specific receptors for calcitonin and, when bound, calcitonin directly inhibits bone resorption. Osteoclasts do not have receptors for PTH or 1,25-dihydroxyvitamin D and are therefore stimulated indirectly by these hormones through an osteoblast-mediated mechanism to increase bone resorption [1]. The macroscopic composition of bone differs depending on anatomic site, age, diet, and disease. Generally, the mineral, or inorganic, phase accounts for 60% of the tissue, the organic phase accounts for 35%, and water accounts for the

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remaining 5%. The mineral or inorganic phase consists of crystalline calcium hydroxyapatite (Ca10 [PO4]6 [OH]2). It is responsible for the compressive strength of bone. The organic phase consists of 90% type I collagen and is responsible for the tensile strength of bone. The remainder of the organic phase consists of proteoglycans, matrix proteins, growth factors, and cytokines. Generally, the expected age range of peak bone mass accrual is between 25 and 30 years [4]. After this age period, both men and women gradually lose bone mass. Women appear to acquire most of their bone mass at an earlier age than boys do (age 11–14 years compared with 13–17 years) [4,5]. Women who are postmenopausal or are hypoestrogenic for other reasons experience accelerated bone loss caused by increased bone resorption compared with formation. Therefore, female athletes who are hypoestrogenic during adolescence initially may accrue a lower peak bone mass, which may be an irreversible problem after a certain age [4,6,7]. In studies that used bone turnover markers, it has been observed that amenorrheic runners have a reduced bone turnover, especially in bone formation, than eumenorrheic runners do. This reduced turnover is believed to be linked to various endocrine abnormalities (including hypoestrogenemia), low body mass index, and low energy intake relative to expenditure [8]. Recent studies suggest that it may be the altered energy balance that ultimately causes this imbalance in bone homeostasis. Both chronic undernutrition and acute dietary energy restrictions have been found to be accompanied by reduced bone formation. The latter also has been associated with depressed levels of IGF-I, a hormone that has been shown to stimulate the production of type I collagen [9–11]. The uncoupling of bone formation and resorption can be seen with restricted energy availability of as little as 30 kcal/kg of lean body mass/d [12]. Bone Remodeling According to Wolff’s law, bone has a cellular and molecular remodeling response to applied mechanical stress. The bony adaptation is a function of the number of loading cycles, cycle frequency, and the amount of strain, strain rate, and strain duration per cycle [13]. Both cortical and cancellous bone remodel continuously by osteoclastic and osteoblastic activity. This remodeling occurs throughout life and is affected by multiple factors including metabolic state, nutritional status, menstrual patterns, age, gender, level of fitness, and ethnicity. Bone also responds to piezoelectric changes, such that tensile forces create electropositivity and thereby stimulate osteoclastic activity [13], whereas compressive forces create electronegativity and thereby stimulate osteoblastic activity. Most cortical stresses in nature are tensional. Torsion or twisting provides tension circumferentially, whereas bending produces tension on the convex side and compression on the concave side. Tensional forces have been shown to result in microfracture and debonding at cement lines [14]. Stress Injury A stress injury occurs on a continuum from normal bone remodeling and repair to frank cortical fracture. Overall bone health depends on mechanical, hor-

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BOX 1: INITIATION OF STRESS FRACTURE 1. Accumulation of microtrauma from repetitive loading of bone (fatigue failure) 2. Fatigue failure persists, leading to crack initiation 3. If initial failure is inadequately repaired, it can lead to more loading and crack propagation

monal, nutritional, and genetic factors. The susceptibility of bone to fracture under fluctuating stresses is related to the crystalline structure and collagen orientation of the osteon. Fatigue load under certain strain rates can cause a progressive accumulation of microdamage (crack initiation) (Box 1) (Fig. 1) [15]. When such a process is prolonged, bone eventually may fail through crack propagation. Bone simultaneously repairs these cracks by new bone formation at their tips, thereby decreasing the chance for propagation. A stress injury of bone is the result of either excessive bone strain with the accumulation of microdamage and the inability to keep up with appropriate skeletal repair (fatigue reaction or fracture) or depressed bony remodeling in response to normal strain (insufficiency reaction or fracture). The former situation most likely occurs in athletes and military recruits. The latter most likely occurs with the female athlete triad, metabolic bone disease, and osteoporosis. Sacral insufficiency stress fractures have been found to occur in female runners and often mimic the presentation of sacroiliitis. There may also be a component of reperfusion injury following prolonged strenuous exercise that results in bone tissue ischemia. This may help explain how some stress fractures occur in cortical bone areas of lower strain and when intracortical osteopenia precedes evidence of microscopic cracks [16]. An additional consideration in the athletic population is the relationship between training regimens and stress injury. Muscles exert a protective effect

Fig. 1. Example of crack initiation in bone. (From Nalla RK, Kinney JH, Ritchie RO. Letters: mechanistic fracture criteria for the failure of human cortical bone. Nat Mater 2003;2:164–8; with permission.)

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on cortical bone by acting as the major shock absorbers. With muscle contraction, cortical bone surface bending strains are reduced [17,18]. In most weightbearing bones, it is believed that, with muscle fatigue, the shock-absorbing effect is lessened and more force is transmitted directly to bone, thereby increasing the likelihood of microdamage accumulation. In nonweight-bearing and some weight-bearing bones, repetitive contraction of muscle at its insertion may generate enough force to cause stress-induced injury [19]. EXTRINSIC AND INTRINSIC FACTORS LEADING TO STRESS FRACTURES There are numerous factors contributing to the risk of stress fractures. However, many of these proposed factors remain unproven. Additionally, many risk factors for stress fractures are interrelated and are methodologically difficult to analyze independently. The cause of stress fractures is multifactorial, and individual athletes vary in their susceptibility to stress injury. These factors are divided into extrinsic factors (characteristics of the environment in which the athlete trains or competes) and intrinsic factors (characteristics of the athlete him- or herself). Extrinsic Factors Training regimen A high training volume is a major risk factor in stress fracture development. Multiple studies in runners have demonstrated that higher weekly running mileage correlates with an increased incidence of stress fractures [20] and overall running injuries [21–23]. Ballet dancers who train for more than 5 hours per day have a significantly higher risk for stress fractures than those who train for less than 5 hours daily [24]. Abrupt or rapid changes in duration, frequency, or intensity of training programs also increase an athlete’s risk of stress fracture. Reducing the intensity or frequency of the training program leads to fewer stress fractures in female and male military recruits [25–27]. However, this intervention has not been studied in athletes. Footwear Athletic footwear is designed to reduce the impact on ground contact and to provide stability by controlling foot and ankle motion [28]. Shoe age has been shown to be a better indicator of shock-absorbing quality than shoe cost. Gardner and colleagues [29] have shown that training in shoes older than 6 months increases the risk for stress fracture. However, there has been no association between shoe cost and stress fracture risk [29]. A woman’s foot has a wider forefoot-to-hindfoot ratio, which can result in poor shoe fit, leaving the hindfoot relatively unsupported. Custom-made biomechanical shoe orthoses that place the foot in a neutral subtalar position as well as absorb shock have been shown to lower the overall incidence of stress fractures in infantry recruits [30,31]. However, this may not be applicable to running athletes [32].

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Training surface The surface on which an athlete trains may also contribute to the risk of stress fracture. Theoretically, training on uneven surfaces could increase the risk of stress fracture by causing increased muscle fatigue and redistributing the load to bone. Hard or less compliant surfaces, such as cement, could also increase stress fracture risk through higher mechanical forces being transmitted to bone during impact. It is difficult to control for and quantify training surface in observational or prospective studies; however, a correlation has been demonstrated in some studies [21,33], whereas other studies have shown no effect [20,23]. One small study found that treadmill runners were at a lower risk for developing tibial stress fracture but were also less likely to achieve tibial bone strengthening than overground runners [33]. Type of sport An Australian study by Goldberg and Pecora [34] in 1994 quantified the rate of stress fracture in men and women in different sports. In this study, the percentage of athletes per season who had stress fractures were: softball 6.3%, track 3.7%, basketball 2.9%, tennis 2.8%, gymnastics 2.8%, lacrosse 2.7%, baseball 2.6%, volleyball 2.4%, crew 2.2%, and field hockey 2.2%. Sprinters, hurdlers, and jumpers tend to have more foot fractures, whereas middle and long-distance runners have more long bone and pelvic fractures [35]. Rowers and golfers have been found to have increased rates of rib stress fractures [36,37]. INTRINSIC FACTORS Demographic Factors Gender Most studies have found that women have a higher incidence of stress fractures compared with men. This higher incidence probably is multifactorial, secondary at least in part to gender-associated risk factors such as dietary deficiencies, menstrual irregularities, lower BMD, and narrower bone width. Gender differences in muscle physiology, especially neuromuscular control, also may be to blame because several studies have shown that women have a slower rate of force development in the muscle than men do [38–40]. In the United States military, the risk of stress fractures in female recruits undergoing the same training program as men is up to 10 times higher [4]. This increased risk also has been observed in athletic populations [34,41,42]. Bennell and colleagues [35] have reported no overall difference between stress fracture incidence in male and female athletes. However, the data appeared to show a trend for a higher risk of stress fractures in females when the amount of training hours were taken into account. Women, however, appear to have more femoral neck, metatarsal, and pelvic stress fractures than men do [43]. Further research is needed to determine whether the apparently higher incidence of stress fractures in women is independent of other known risk factors.

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Age The role of age as a risk for stress fractures in female athletes is not established. Studies in military recruits have been inconsistent, with some studies finding an increased risk of stress fractures with increasing age [44,45] and others finding a decreased risk [29,46–48] or no effect [49,50]. This lack of agreement is most likely caused by confounding factors such as previous physical activity level, hormonal status, BMD, and training level. Most studies in athletic populations have not found a correlation between age and stress fracture risk, although rigorous studies controlling for other possibly confounding variables are presently lacking. Race The incidence of stress fractures is significantly higher in white and Asian women than in African American women [29,44–46]. This is believed to be related to differences in bone turnover and peak bone density and not to race independently. It also appears that both ethnic differences in bone mineralization and bone integrity in athletes are mediated by heritable differences in titratable acid, sodium, and calcium excretion [51]. Aerobic fitness, muscle strength, and flexibility Previously inactive or less active military recruits have a higher incidence of stress fractures compared with those who are active before beginning basic training [29,48,49]. There are several possible factors contributing to this, including decreased aerobic fitness, decreased muscle strength, lower endurance, and poor flexibility. A study of military recruits found no association between aerobic fitness (predicted VO2max) and stress fracture risk [52]. It is unlikely that aerobic fitness alone accounts for the difference [53,54]. The role of flexibility on stress fractures has yet to be well defined [35,47,55]. BIOMECHANICAL FACTORS Bone Mineral Density Lower BMD, especially of the femoral neck, has been shown to be associated with an increased risk of stress fractures in the female athlete [56]. Although there are case-control studies that both support [57] and refute [49] this finding, Bennell and colleagues [53] were the first to examine this condition prospectively. They found that lower BMD in the lumbar spine and foot were significant predictors of later stress fracture development in female track and field athletes. Of note, an athlete with an apparently normal BMD (caused by the increased bone loading of sport) may be at an increased risk of stress fracture if she falls below the mean among female athletes. Also, as observed by dual x-ray absorptiometry scanning in athletic females, cancellous bone stress fractures correlate with early onset osteopenia much more than cortical bone stress fractures do [58]. This indicates the necessity of bone density evaluation in any young female with cancellous stress fracture. Menstrual disturbance and lower BMD most likely are not risk factors independent of each other but are interrelated, with amenorrheic athletes having both lower BMD and higher stress fracture incidence [59].

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Bone Geometry The amount of force a bone can withstand is proportional to its cross-sectional area and moment of inertia (a measure of bone resistance to bending). Studies of military personnel have found these parameters to be significantly lower among those who develop stress fractures [60–62]. These studies also have found that of those who sustained femoral, tibial, or foot stress fractures, 31% had narrowed tibial width compared with those without fracture [63]. This narrowed tibial width may be an indicator of a biomechanically weaker skeletal structure. It is hypothesized that women are likely to have overall narrower bones than men [64], and this is a possible factor contributing to a higher incidence of stress fractures in female athletes. ANATOMIC FACTORS Foot Morphology The structure of the foot helps to determine how much ground contact force is absorbed in the foot and how much is transferred to the bones of the leg and thigh. A rigid, high-arched foot (pes cavus) absorbs less stress and transmits greater force to the tibia and femur. A flexible, low-arched foot (pes planus) absorbs more force in the foot itself and transmits less to the tibia, fibula, and femur. One military study evaluating foot morphology found persons with the highest arches sustained 3.9 times as many stress fractures as those with the lowest arches [65]. Other studies [65,66] suggest that individuals with pes cavus seem to be at an increased risk of tibial and femoral stress fractures, whereas those with pes planus may sustain more metatarsal stress fractures. However, other studies have not found a significant correlation between foot structure and stress fracture risk [20,53]. It is possible that both pes planus and pes cavus foot structures may increase the risk of stress fracture at various sites, but this has not yet been adequately evaluated or proven. Leg Length Discrepancy Leg length discrepancy also has been associated with an increased risk of stress fractures in female athletes [20,53]. The degree of leg length difference may correlate with increasing stress fracture risk [67]. However, one study of male military recruits did not confirm this relationship [68]. It is reasonable to evaluate and correct significant leg length discrepancy in runners, especially those with other stress fracture risks. Knee Alignment Valgus knee alignment and a quadriceps angle greater than 15° may also increase the risk for tibial stress fracture [68,69]. HORMONAL FACTORS Delayed Menarche Female athletes generally reach menarche at a later age than female nonathletes do, particularly those in certain sports such as ballet, running, and gymnastics [70,71]. Delayed menarche may cause lower peak bone mass attainment or may

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be a marker for other possible influences on stress fracture risk, such as low body fat, low body weight, future menstrual disturbance, or excessive training. The effect of this delay on bone health and the risk of stress fractures have not been well studied; however, some studies suggest osteopenia, stress fracture, and scoliosis may be potential complications of delayed menarche [53,71]. Scoliosis, in particular, has been observed in female ballet dancers with delayed menarche [71]. This may also lead to pelvic obliquity and relative leg length discrepancies and the potential for increasing the risk for stress fracture. Menstrual Disturbance Multiple studies have demonstrated that stress fractures occur more commonly in women with amenorrhea or oligomenorrhea than in eumenorrheic women [17,46,48,53,57,71]. Athletes with menstrual disturbances have low basal estrogen concentrations [72] and a lower BMD than eumenorrheic athletes do [73]. It has been hypothesized that estrogen deprivation increases the physiologic set point for bone modeling and remodeling, making it more difficult to activate the cellular response necessary to induce bone adaptation to stress [4,74] and increasing the risk of stress fractures. Health care providers, athletes, coaches, and parents need to be aware that menstrual disturbance is not simply a normal product of training and that such disturbances can have devastating consequences. Menstrual disturbances also are seen in association with disordered eating and endothelial cell dysfunction (as in the female athlete triad, discussed later). Therefore, athletes with menstrual irregularity should be further evaluated accordingly. Contraception Some studies have shown that oral contraceptive pills (OCP) seem to have a protective effect in preventing stress fractures in female athletes [17,75]. It appears that exogenous estrogen may help curb further bone loss in the hypoestrogenic amenorrheic athlete; however, it may not be sufficient to stimulate bone growth [71,76–79]. Several small studies of amenorrheic women or those with anorexia have found BMD at the lumbar spine or hip to be higher for women taking OCP compared with those who were not [76,77,80], whereas other studies show no significant change [71,78]. It has also been theorized that OCP may act through another mechanism, such as improving bone microarchitecture and quality without significantly affecting BMD [4]. However, to add to the controversy, a recent study by Hartard and colleagues [81] has shown that OCP use is associated with decreased BMD of the spine (7.9%) and the femoral neck (8.8%) in female endurance athletes compared with non-OCP users. The authors [81] also found that early age at initiation of OCP was an important risk factor for low peak bone mass in young women. Based on the conflicting results from research and the lack of well-controlled studies, it is difficult to assess the effects of OCP on skeletal health in normally menstruating women. In women who have menstrual disturbances, the use of OCP or another hormonal replacement therapy may be effective in preventing further bone loss; however, the resumption of menses may mask an underlying nutritional

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disorder and provide a false sense of security. Recent evidence also suggests that depo-medroxyprogesterone may contribute to impaired bone accretion and low bone mineral density, and it should be avoided in young women [82]. NUTRITIONAL FACTORS Low Calcium and Vitamin D Intake Low calcium intake is associated with low BMD [83] and therefore may contribute to the development of stress fractures. Myburgh and colleagues [57] observed an association between decreased calcium intake and increased stress fracture risk. However, other studies found no association between calcium intake and stress fracture risk, with both stress fracture and nonstress fracture groups having normal calcium intake [13,84,85]. Athletes whose calcium intake is below the daily recommended value are likely to be at risk for stress fractures, but for those with normal dietary calcium intake, other factors play a larger role. Vitamin D is also essential to bone health, and its functions include stimulating calcium transport, osteoblastic stimulation, and decreasing parathyroid hormone. Recent studies have focused on the role of the vitamin D receptor allele in predicting bone density. More research is necessary to determine the clinical applications of its use in screening [86–88]. Disordered Eating Inadequate caloric intake relative to the energy expenditure required for exercise appears to be the primary mechanism by which female athletes are predisposed to menstrual dysfunction and detrimental effects on bone. Anorexia nervosa has been associated with a significantly decreased BMD [7,89]. Nearly 75% of adolescent girls with anorexia have a BMD more than two standard deviations below the normal value [90]. Not surprisingly, women with anorexia nervosa are at an increased risk for stress fracture development [91,92]. Interestingly, disordered eating is associated with low BMD in the absence of menstrual irregularities [59]. The Female Athlete Triad The female athlete triad refers to an interrelated problem consisting of disordered eating, amenorrhea, and osteoporosis. Hoch and colleagues [93] have also found that amenorrheic athletes have reduced brachial artery endotheliumdependent flow-mediated vasodilation compared with oligomenorrheic and eumenorrheic athletes. Furthermore, in a 2-year follow-up study, the original amenorrheic athletes were found to have a significant improvement in BMD with different combinations of estrogen and progesterone or the return of menses naturally. The female athlete triad is a potentially lethal combination of medical disorders reported in some female athletes [4,42]. The athletes at greatest risk appear to be those who feel significant pressure to excel in sports for which leanness and a low body weight are considered advantageous, such

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as gymnastics, figure skating, ballet, and distance running [94]. Also, athletes participating in individual sports are at higher risk than those in team sports. The problem usually begins with disordered eating, which includes a spectrum of abnormal and harmful eating patterns such as binging and purging, restrictive eating, fasting, and the use of diet pills or laxatives. The preoccupation with food, a distorted body image, and intense fear of becoming fat are often present as well. Some athletes will meet the Diagnostic and Statistical Manual of Mental Disorders, revised edition IV [95], criteria for anorexia nervosa or bulimia, whereas other athletes may display similar behaviors without meeting full diagnostic criteria. A new classification of eating disorder not otherwise specified (ie, ED-NOS) allows for the identification of women who do not meet other classification criteria. This classification has been helpful in this population because the athlete’s weight may seem adequate as a result of increased lean tissue mass; however they are not consuming enough calories to meet their energy needs. Abnormal eating patterns may lead to athletic-associated amenorrhea. Athletic amenorrhea is a complex multifactorial condition with serious associated comorbidities. Extreme caloric restriction, excessive exercise, physical and emotional stress associated with exercise and competition, percentage of body fat, and genetics contribute to the condition. There is, however, increasing evidence that suggests nutritional restrictions and the resulting endocrine and metabolic changes are a critical initiator of hypothalamic-induced athletic amenorrhea and osteoporosis [96]. Disordered eating, estrogen deficiency, and menstrual dysfunction predispose women to the third component of the triad, osteoporosis [89]. Reduced BMD in premenopausal women appears to be irreversible, despite weight gain, resumption of menses, or estrogen replacement [6,7]. One study found that, with the resumption of menses, there was a significant increase in vertebral BMD. However after 2 years of normal menses, BMD remained below the agenormative level. Slemenda and colleagues [97] have shown that the low estrogenic state associated with amenorrhea has a more profound effect on cancellous bone than on cortical bone. Cancellous bone is found in a higher percentage in the pelvis, sacrum, and femoral neck areas where female athletes tend to have a higher occurrence of stress fractures. These factors put the female athlete who is experiencing the triad complex at a significant risk for stress fractures. Although some investigators have found that weight-bearing exercise has a skeletally protective effect and may attenuate the bone loss usually seen in anorexics [89], the use of excessive training to control weight could also contribute to the increased risk of stress fractures associated with the female athlete triad. Several other factors are known to increase the risk for osteoporosis, but these factors have not been thoroughly investigated as possible risks for stress fractures in female athletes. These other factors include smoking, caffeine consumption, and certain medications such as thyroid hormone and corticosteroids. In a study of female army recruits, it was found that current or past smoking, alcoholic consumption of ≥ 10 drinks per week, corticosteroid use, use of

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depo-medroxyprogesterone acetate, lower adult weight, and no history of regular exercise increased the likelihood of stress fracture [45,82]. SUMMARY Stress fractures can occur in any active individual, from the weekend warrior to the elite athlete. As these injuries occur, it is important to understand how bones respond to the stresses placed on them. The understanding of potential intrinsic and extrinsic causes is important in treatment of these injuries. The proper identification and prevention of these stress injuries allows for athletes to return to activity expeditiously. References [1] Kaplan FS, Hayes WC, Keaveny TM, et al. Form and function of bone. In: Simon SR, editor. Orthopaedic basic science. Rosemont (IL): American Academy of Orthopaedic Surgeons; 1994. p. 127–94. [2] Monteleone Jr GP. Stress fractures in the athlete. Orthop Clin North Am 1995;26(3): 423–32. [3] Markey KL. Stress fractures. Clin Sports Med 1987;6(2):405–25. [4] Nattiv A, Armsey Jr TD. Stress injury to bone in the female athlete. Clin Sports Med 1997;16(2):197–224. [5] Theintz G, Buchs B, Rizzoli R, et al. Longitudinal monitoring of bone mass accumulation in healthy adolescents: evidence for a marked reduction after 16 years of age at the levels of lumbar spine and femoral neck in female subjects. J Clin Endocrinol Metab 1992; 75(4):1060–5. [6] Drinkwater BL, Nilson K, Ott S, et al. Bone mineral density after resumption of menses in amenorrheic athletes. JAMA 1986;256(3):380–2. [7] Rigotti NA, Neer RM, Skates SJ, et al. The clinical course of osteoporosis in anorexia nervosa: a longitudinal study of cortical bone mass. JAMA 1991;265(9):1133–8. [8] Zanker CL, Swaine IL. Relation between bone turnover, estradiol, and energy balance in women distance runners. Br J Sports Med 1998;32(2):167–71. [9] Zanker CL, Swaine IL. Responses of bone turnover markers to repeated endurance running in humans under conditions of energy balance or energy restriction. Eur J Appl Physiol 2000;83:434–40. [10] Ammann P, Rizzoli R, Muller K, et al. IGF-I and pamidronate increase bone mineral density in ovariectomized adult rats. Am J Physiol 1993;265(5 Pt 1):E770–6. [11] Chevalley T, Rizzoli R, Manen D, et al. Arginine increases insulin-like growth factor-I production and collagen synthesis in osteoblast-like cells. Bone 1998;23(2):103–9. [12] Ihle R, Loucks AB. Dose-response relationships between energy availability and bone turnover in young exercising women. J Bone Miner Res 2004;19(8):1231–40. [13] Carter DR, Caler WE. A cumulative damage model for bone fracture. J Orthop Res 1985; 3(1):84–90. [14] Carter DR, Hayes WC. Compact bone fatigue damage: a microscopic examination. Clin Orthop 1977;127:265–74. [15] Fyhrie DP, Milgrom C, Hoshaw SJ, et al. Effect of fatiguing exercise on longitudinal bone strain as related to stress fracture in humans. Ann Biomed Eng 1998;26(4):660–5. [16] Otter MW, Qin YX, Rubin CT, et al. Does bone perfusion/reperfusion initiate bone remodeling and the stress fracture syndrome? Med Hypotheses 1999;53(5):363–8. [17] Barrow GW, Saha S. Menstrual irregularity and stress fractures in collegiate female distance runners. Am J Sports Med 1988;16(3):209–16. [18] Egol KA, Koval KJ, Kummer F, et al. Stress fractures of the femoral neck. Clin Orthop 1998;348:72–8.

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[19] Stanitski CL, McMaster JH, Scranton PE. On the nature of stress fractures. Am J Sports Med 1978;6(6):391–6. [20] Brunet ME, Cook SD, Brinker MR, et al. A survey of running injuries in 1505 competitive and recreational runners. J Sports Med Phys Fitness 1990;30(3):307–15. [21] Macera CA, Pate RR, Powell KE, et al. Predicting lower-extremity injuries among habitual runners. Arch Intern Med 1989;149(11):2565–8. [22] Marti B, Vader JP, Minder CE, et al. On the epidemiology of running injuries: the 1984 Bern Grand-Prix study. Am J Sports Med 1988;16(3):285–94. [23] Walter SD, Hart LE, McIntosh JM, et al. The Ontario cohort study of running-related injuries. Arch Intern Med 1989;149(11):2561–4. [24] Kadel NJ, Teitz CC, Kronmal RA. Stress fractures in ballet dancers. Am J Sports Med 1992; 20(4):445–9. [25] Scully TJ, Besterman G. Stress fracture–a preventable training injury. Mil Med 1982; 147(4):285–7. [26] Rudzki SJ. Injuries in Australian Army recruits: part I: decreased incidence and severity of injury seen with reduced running distance. Mil Med 1997;162(7):472–6. [27] Popovich RM, Gardner JW, Potter R, et al. Effect of rest from running on overuse injuries in army basic training. Am J Prev Med 2000;18(Suppl 3):S147–55. [28] Frey C. Footwear and stress fractures. Clin Sports Med 1997;16(2):249–57. [29] Gardner Jr LI, Dziados JE, Jones BH, et al. Prevention of lower extremity stress fractures: a controlled trial of a shock absorbent insole. Am J Public Health 1988;78(12):1563–7. [30] Finestone A, Giladi M, Elad H, et al. Prevention of stress fractures using custom biomechanical shoe orthoses. Clin Orthop 1999;360:182–90. [31] Gillespie WJ, Grant I. Interventions for preventing and treating stress fractures and stress reactions of bone of the lower limbs in young adults. In: Cochrane review. 4th edition. Cochrane Database Sys Rev 2000;2:CD000450. [32] Ekenman I, Milgrom C, Finestone A, et al. The role of biomechanical shoe orthoses in tibial stress fracture prevention. Am J Sports Med 2002;30(6):866–70. [33] Milgrom C, Finestone A, Segev S, et al. Are overground or treadmill runners more likely to sustain tibial stress fracture? Br J Sports Med 2003;37(2):160–3. [34] Goldberg B, Pecora C. Stress fractures: a risk of increased training in freshman. Phys Sportsmed 1994;22:68–78. [35] Bennell KL, Malcolm SA, Thomas SA, et al. The incidence and distribution of stress fractures in competitive track and field athletes: a twelve-month prospective study. Am J Sports Med 1996;24(2):211–7. [36] Lord MJ, Ha KI, Song KS. Stress fractures of the ribs in golfers. Am J Sports Med 1996; 24(1):118–22. [37] Hickey GJ, Fricker PA, McDonald WA. Injuries to elite rowers over a 10-yr period. Med Sci Sports Exerc 1997;29(12):1567–72. [38] Bell DG, Jacobs I. Electro-mechanical response times and rate of force development in males and females. Med Sci Sports Exerc 1986;18(1):31–6. [39] Hakkinen K. Force production characteristics of leg extensor, trunk flexor and extensor muscles in male and female basketball players. J Sports Med Phys Fitness 1991;31(3): 325–31. [40] Winter EM, Brookes FB. Electromechanical response times and muscle elasticity in men and women. Eur J Appl Physiol 1991;63(2):124–8. [41] Johnson AW, Weiss Jr CB, Wheeler DL. Stress fractures of the femoral shaft in athletes: more common than expected: a new clinical test. Am J Sports Med 1994;22(2):248–56. [42] Zernicke RF, McNitt-Gray J, Otis C, et al. Stress fracture risk assessment among elite collegiate women runners. J Biomech 1994;27:854. [43] Lombardo SJ, Benson DW. Stress fractures of the femur in runners. Am J Sports Med 1982; 10(4):219–27. [44] Brudvig TJ, Gudger TD, Obermeyer L. Stress fractures in 295 trainees: a one-year study of incidence as related to age, sex, and race. Mil Med 1983;148(8):666–7.

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[45] Lappe JM, Stegman MR, Recker RR. The impact of lifestyle factors on stress fractures in female Army recruits. Osteoporos Int 2001;12(1):35–42. [46] Friedl KE, Nuovo JA, Patience TH, et al. Factors associated with stress fracture in young army women: indications for further research. Mil Med 1992;157(7):334–8. [47] Milgrom C, Finestone A, Shlamkovitch N, et al. Youth is a risk factor for stress fracture: a study of 783 infantry recruits. J Bone Joint Surg Br 1994;76B(1):20–2. [48] Winfield AC, Moore J, Bracker M, et al. Risk factors associated with stress reactions in female Marines. Mil Med 1997;162(10):698–702. [49] Cline AD, Jansen GR, Melby CL. Stress fractures in female army recruits: implications of bone density, calcium intake, and exercise. J Am Coll Nutr 1998;17(2):128–35. [50] Reinker KA, Ozburne S. A comparison of male and female orthopaedic pathology in basic training. Mil Med 1979;144(8):532–6. [51] Vaitkevicius H, Witt R, Maasdam M, et al. Ethnic differences in titratable acid excretion and bone mineralization. Med Sci Sports Exerc 2002;34(2):295–302. [52] Swissa A, Milgrom C, Giladi M, et al. The effect of pretraining sports activity on the incidence of stress fractures among military recruits: a prospective study. Clin Orthop 1989;245:256–60. [53] Bennell KL, Malcolm SA, Thomas SA, et al. Risk factors for stress fractures in track and field athletes: a twelve-month prospective study. Am J Sports Med 1996;24(6):810–8. [54] Beck TJ, Ruff CB, Shaffer RA, et al. Stress fracture in military recruits: gender differences in muscle and bone susceptibility factors. Bone 2000;27(3):437–44. [55] Giladi M, Milgrom C, Stein M, et al. External rotation of the hip: a predictor of risk for stress fractures. Clin Orthop 1987;216:131–4. [56] Lauder TD, Dixit S, Pezzin LE, et al. The relation between stress fractures and bone mineral density: evidence from active-duty Army women. Arch Phys Med Rehabil 2000; 81(1):73–9. [57] Myburgh KH, Hutchins J, Fataar AB, et al. Low bone density is an etiologic factor for stress fractures in athletes. Ann Intern Med 1990;113(10):754–9. [58] Marx RG, Saint-Phard D, Callahan LR, et al. Stress fracture sites related to underlying bone health in athletic females. Clin J Sport Med 2001;11(2):73–6. [59] Cobb KL, Bachrach LK, Greendale G, et al. Disordered eating, menstrual irregularity, and bone mineral density in female runners. Med Sci Sports Exerc 2003;35(5):711–9. [60] Beck TJ, Ruff CB, Mourtada FA, et al. Dual-energy X-ray absorptiometry derived structural geometry for stress fracture prediction in male US Marine Corps recruits. J Bone Miner Res 1996;11(5):645–53. [61] Milgrom C, Giladi M, Simkin A, et al. An analysis of the biomechanical mechanism of tibial stress fractures among Israeli infantry recruits: a prospective study. Clin Orthop 1988;231:216–21. [62] Milgrom C, Giladi M, Simkin A, et al. The area moment of inertia of the tibia: a risk factor for stress fractures. J Biomech 1989;22(11–12):1243–8. [63] Giladi M, Milgrom C, Simkin A, et al. Stress fractures and tibial bone width: a risk factor. J Bone Joint Surg Br 1987;69B(2):326–9. [64] Miller GJ, Purkey Jr WW. The geometric properties of paired human tibiae. J Biomech 1980;13(1):1–8. [65] Giladi M, Milgrom C, Stein M. The low arch, a protective factor in stress fractures: a prospective study of 295 military recruits. Orthop Rev 1985;14:709–12. [66] Simkin A, Leichter I, Giladi M, et al. Combined effect of foot arch structure and an orthotic device on stress fractures. Foot Ankle 1989;10(1):25–9. [67] Friberg O. Leg length asymmetry in stress fractures: a clinical and radiological study. J Sports Med Phys Fitness 1982;22(4):485–8. [68] Cowan DN, Jones BH, Frykman PN, et al. Lower limb morphology and risk of overuse injury among male infantry trainees. Med Sci Sports Exerc 1996;28(8):945–52. [69] Finestone A, Shlamkovitch N, Eldad A, et al. Risk factors for stress fractures among Israeli infantry recruits. Mil Med 1991;156(10):528–30.

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[70] Stager JM, Hatler LK. Menarche in athletes: the influence of genetics and prepubertal training. Med Sci Sports Exerc 1988;20(4):369–73. [71] Warren MP, Brooks-Gunn J, Hamilton LH, et al. Scoliosis and fractures in young ballet dancers: relation to delayed menarche and secondary amenorrhea. N Engl J Med 1986; 314(21):1348–53. [72] Loucks AB, Horvath SM. Athletic amenorrhea: a review. Med Sci Sports Exerc 1985; 17(1):56–72. [73] Drinkwater BL, Nilson K, Chesnut CH, et al. Bone mineral content of amenorrheic and eumenorrheic athletes. N Engl J Med 1984;311(5):277–81. [74] Frost HM. A new direction for osteoporosis research: a review and proposal. Bone 1991; 12(6):429–37. [75] Bennell KL, Malcolm SA, Thomas SA, et al. Risk factors for stress fractures in female trackand-field athletes: a retrospective analysis. Clin J Sport Med 1995;5(4):229–35. [76] Hergenroeder AC. Bone mineralization, hypothalamic amenorrhea, and sex steroid therapy in female adolescents and young adults. J Pediatr 1995;126(5 Pt 1):683–9. [77] Cumming DC, Wall SR, Galbraith MA, et al. Reproductive hormone responses to resistance exercise. Med Sci Sports Exerc 1987;19(3):234–8. [78] Klibanski A, Biller BM, Schoenfeld DA, et al. The effects of estrogen administration on trabecular bone loss in young women with anorexia nervosa. J Clin Endocrinol Metab 1995;80(3):898–904. [79] Warren MP, Perlroth NE. The effects of intense exercise on the female reproductive system. J Endocrinol 2001;170(1):3–11. [80] Seeman E, Szmukler GI, Formica C, et al. Osteoporosis in anorexia nervosa: the influence of peak bone density, bone loss, oral contraceptive use, and exercise. J Bone Miner Res 1992;7(12):1467–74. [81] Hartard M, Kleinmond C, Kirchbichler A, et al. Age at first oral contraceptive use as a major determinant of vertebral bone mass in female endurance athletes. Bone 2004; 35(4):836–41. [82] Berenson AB, Radecki CM, Grady JJ, et al. A prospective, controlled study of the effects of hormonal contraception on bone mineral density. Obstet Gynecol 2001;98(4):576–82. [83] Specker BL. Evidence for an interaction between calcium intake and physical activity on changes in bone mineral density. J Bone Miner Res 1996;11(10):1539–44. [84] Bennell K, Matheson G, Meeuwisse W, et al. Risk factors for stress fractures. Sports Med 1999;28(2):91–122. [85] Cooper KL, Beabout JW, Swee RG. Insufficiency fractures of the sacrum. Radiology 1985; 156(1):15–20. [86] Eisman JA. Vitamin D receptor gene alleles and osteoporosis: an affirmative view. J Bone Miner Res 1995;10(9):1289–93. [87] Fleet JC, Harris SS, Wood RJ, et al. The BsmI vitamin D receptor restriction fragment length polymorphism (BB) predicts low bone density in premenopausal black and white women. J Bone Miner Res 1995;10(6):985–90. [88] Morrison NA, Qi JC, Tokita A, et al. Prediction of bone density from vitamin D receptor alleles. Nature 1994;367(6460):284–7. [89] Rigotti NA, Nussbaum SR, Herzog DB, et al. Osteoporosis in women with anorexia nervosa. N Engl J Med 1984;311(25):1601–6. [90] Bachrach LK, Guido D, Katzman D, et al. Decreased bone density in adolescent girls with anorexia nervosa. Pediatrics 1990;86(3):440–7. [91] Frusztajer NT, Dhuper S, Warren MP, et al. Nutrition and the incidence of stress fractures in ballet dancers. Am J Clin Nutr 1990;51(5):779–83. [92] Nattiv A, Puffer JC, Green GA. Lifestyles and health risks of collegiate athletes: a multicenter study. Clin J Sport Med 1997;7(4):262–72. [93] Hoch AZ, Dempsey RL, Carrera GF, et al. Is there an association between athletic amenorrhea and endothelial cell dysfunction? Med Sci Sports Exerc 2003;35(3):377–83. [94] Nattiv A, Agostini R, Drinkwater B, et al. The female athlete triad: the inter-relatedness

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of disordered eating, amenorrhea, and osteoporosis. Clin Sports Med 1994;13(2): 405–18. [95] American Psychiatric Association. In: Diagnostic and statistical manual of mental disorders. 4th edition. Washington, DC: American Psychiatric Association Press; 1994. [96] Loucks AB. Energy availability, not body fatness, regulates reproductive function in women. Exerc Sport Sci Rev 2003;31(3):144–8. [97] Slemenda CW, Reister TK, Hui SL, et al. Influences on skeletal mineralization in children and adolescents: evidence for varying effects of sexual maturation and physical activity. J Pediatr 1994;125(2):201–7.

Clin Sports Med 25 (2006) 17–28

CLINICS IN SPORTS MEDICINE Classification and Return-to-Play Considerations for Stress Fractures Jason J. Diehl, MDa, Thomas M. Best, MD, PhDa, Christopher C. Kaeding, MDb,* a Division of Sports Medicine, Department of Family Medicine, The Ohio State University Sports Medicine Center, 2050 Kenny Road, Columbus, OH 43221, USA b Division of Sports Medicine, Department of Orthopedics, The Ohio State University Sports Medicine Center, 2050 Kenny Road, Columbus, OH 43221, USA

“S

tress reactions” and “stress fractures” are fatigue-failure injuries of bone that are commonly diagnosed in competitive, occupational, and recreational athletes. These overuse injuries result in a mechanical failure of bone due to the accumulation of microdamage secondary to repetitive strain episodes. A stress reaction precedes a stress fracture in the bone fatiguefailure continuum and is hallmarked by bony microfailure without cortical disruption. These injuries are most common in the lower extremities of endurance and repetitive-motion athletes such as runners, jumpers, skaters, and soldiers [1,2]. Despite a female predilection in military recruits, in athletes, there seems to be no difference in incidence between men and women [3]. Next to prompt and proper diagnosis and treatment, return-to-play decision making can have the greatest impact on an athlete’s recovery. It is therefore important that athletes be given the best evidence available to guide their time frame for return to sport and physical activity. Bone stress-injury treatment and return-to-play decision making is based on the site of the injury and its corresponding potential for healing and risk of significant complication. Most stress fractures heal uneventfully with relative rest and activity modification. These fractures have recently been termed lowrisk stress fractures [4]. Overtreatment of low-risk stress fractures can lead to deconditioning and unnecessary loss of training and competition. Conversely, there are anatomic sites that have a predilection for slow or incomplete healing, a high tendency for recurrence, or a significant risk of complication with progression of the fracture. Fractures at these locations are termed high-risk stress fractures [5]. To avoid prolonged or inadequate healing and potentially serious complications, it is important to be cognizant of these high-risk sites. Prompt diagnosis and treatment is key to minimize the impact of high-risk stress fractures on the athlete’s career. * Corresponding author. E-mail address: [email protected] (C.C. Kaeding).

0278-5919/06/$ – see front matter doi:10.1016/j.csm.2005.08.012

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Successful treatment of stress fractures should not only focus on bony healing but also address reasons why the injury occurred in the first place. These reasons can be divided into intrinsic and extrinsic risk factors. Intrinsic risk factors include biomechanical, hormonal, and nutritional status. Common biomechanical factors leading to recurrent stress fractures include muscle weakness, low bone density, high longitudinal arches, leg-length discrepancies, and likely forefoot and knee varus [6–9]. Menstrual irregularities have also been linked to increased stress fracture incidence in general [10]. The most common extrinsic risk factor appears to be training errors. For example, training errors have been shown to increase the risk of stress fractures in military recruits who begin training in poor physical condition and have high volumes of training [11,12]. Individuals with a history of a previous stress fracture also are at higher risk of future injuries [13]. Return-to-play decision making is an integral part of the treatment of stress fractures in athletes. The development of the treatment plan should include consideration of intrinsic and extrinsic predisposing factors, classification and grade of the stress fracture, and the point in the athlete’s career or competitive season at which he or she presents. The authors stress that each treatment is individualized for best recovery and prevention of future injuries. In this article, the authors briefly discuss the pathophysiology and diagnostic process of stress fractures and expand on the classification of stress fractures and its impact on return-to-play decision making based on the relative risk of the fracture. PATHOPHYSIOLOGY Stress fractures were first described in military recruits exposed to new cyclic loading activities. Repetitive loading alters a bone’s microstructure through remodeling according to Wolff’s law. The result is a stronger bone able to withstand greater loads [14]. When an athlete begins a new or increases a current exercise program, an increase in the number and size of microfractures within the bone occurs. The body responds by increasing oseteoclastic and osteoblastic activity. Initially, osteoblastic activity lags behind the resorptive properties of the osteoclasts. This process leaves the bone susceptible to fatigue failure if the area is continually stressed without adequate time for repair [15,16]. An alternative hypothesis is that muscle dysfunction from overuse results in focal bending stresses that exceed the structural and physiologic tolerance of bone. With continual strain episodes, fatigue failure proceeds through a progression of microfracture initiation, propagation, and eventual macrofracture. If the body does not repair the microscopic crack before additional loads are applied, then the fracture progresses across the bone. This process is termed crack propagation. Continued propagation and coalescence of the microcracks can result in macroscopic failure of the bone. The balance between the creation/propagation of microcracks and the body’s ability to repair them may be influenced by multiple factors. These

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factors may include the athlete’s hormonal, menstrual, and nutritional status; muscle function; and genetic predisposition. These factors continue to be studied and elucidated. There is a continuum of fatigue failure of bone. Early accumulation of microdamage is often referred to as a stress reaction of bone. When a clear fracture line is visible on imaging (CT, MRI, or radiograph), a stress fracture has developed. Some consider a stress reaction as an early, low-grade stress fracture. How far the athlete’s injury has progressed on this continuum of early microcrack formation to complete fracture has bearing on treatment, prognosis, and return-to-play considerations. DIAGNOSIS Most athletes who have stress fractures present with an insidious onset of progressive pain in a focal area [17]. Initially, pain is present only with activity and may be associated with localized muscular soreness. As the fracture continues to develop, the pain usually begins to affect performance, and with continued training, pain persists into activities of daily living. In more severe cases, pain becomes continual. Physical examination usually demonstrates tenderness within a localized area. There may also be painful loss of joint motion or muscular tightness surrounding the injury. With more severe cases, there may be swelling or palpable irregularities at the fracture site. Many imaging modalities are helpful in the diagnosis of stress fractures. Plain radiographs are useful when positive, but the findings may be subtle and may not accurately depict the severity of the injury. This is especially true if the radiograph is taken within the first few weeks of the injury. Bone scans have traditionally been used in the diagnosis of stress fractures because of their high sensitivity [18]. The sensitivity has been shown to be 84% to 100% within 3 days of symptoms [19]. Bone scans, however, are not as specific as other modalities. Bone scans are also time-consuming for the patient. Because the uptake can persist for months after clinical healing, bone scans are not as useful in follow-up care. The two other imaging techniques that have become more useful in the diagnosis and management of stress fractures are CT and MRI. CT is less expensive and offers eloquent bony detail including fracture location, orientation, and extent and signs of healing. It is particularly helpful in areas such as the tarsal navicular to determine whether the fracture is complete or incomplete [20]. MRI has become the method of choice for many physicians because of its availability, speed, and the amount of information that is provided [21–23]. Its sensitivity is similar to that found with bone scan, but MRI is capable of showing more precise location and extent of fracture [24]. For tibial stress injuries, one study demonstrated the specificity and the positive predictive values to approach 100% [22]. T2-weighted images not only show the fracture site but also accurately confirm the degree of marrow edema [25].

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CLASSIFICATION The classification of stress fractures into high risk or low risk has been suggested by multiple authors [4,5,26]. This distinction allows the medical staff to quickly determine whether they can be aggressive or conservative with their decision to return an athlete to participation. Low-risk stress fractures include the femoral shaft, medial tibia, ribs, ulna shaft, and first through fourth metatarsals—all of which have a favorable natural history. These sites tend to be on the compressive side of the bone and respond well to activity modification. Low-risk stress fractures are less likely to recur, become a nonunion, or have a significant complication should it progress to complete fracture. Management of these injuries is discussed later and is guided primarily by the individuals’ symptoms. In comparison to low-risk stress fractures, high-risk stress fractures do not have an overall favorable natural history. With delay in diagnosis or with less aggressive treatment, high-risk stress fractures tend to progress to nonunion or complete fracture, require operative management, or recur in the same location [27]. High-risk stress fracture locations include the femoral neck, the patella, the anterior tibial diaphysis, the medial malleolus, the talus, the tarsal navicular, the proximal fifth metatarsal, and the first metatarsal phalengeal seasmoids. It is clear that location determines whether a stress fracture is low risk or high risk. In addition to knowing the classification of a stress fracture as high versus low risk as determined by its anatomic site, the extent of the fatigue failure or the grade of the stress fracture is also needed to completely describe the injury. As mentioned earlier, stress injuries to bone create a continuum, from mild microfailure to cortical disruption to complete fracture. There have been two previously published grading scales for the stress reaction/fracture continuum. The scale published by Arendt and Griffiths [21] has been used for the femur, tibia, fibula, navicular, calcaneus, and forefoot, whereas the scale published by Fredericson and colleagues [28] was developed using data for the tibia alone. Both scales consider grade 4 to be a complete stress fracture and grades 1 to 3 to be increasing levels of periosteal changes and marrow edema. One large study by Arendt and Griffiths [21] demonstrated that grade 3 and 4 injuries took longer to heal than grade 1 and 2 injuries. This study demonstrated that the grade of injury has prognostic implications regarding the time of healing. The management of bony stress injuries should be based on the location and grade of the injury. These two details give the amount of microdamage that has accumulated and whether it is a high- or low-risk injury. The following discussion focuses on treatment and return-to-play strategies for stress fractures depending on their anatomic location and associated classification as high or low risk. MANAGEMENT OF AND RETURN-TO-PLAY STRATEGIES FOR LOW-RISK FRACTURES Return-to-play decisions continue to challenge sports medicine practitioners. In the modern era of evidence-based decision making, practitioners continue to be faced with scenarios in which the best available evidence is expert opinion. Many factors need to be discussed with the athlete, and none of these is more

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important than the risks of continued participation, particularly in the setting of an ongoing injury. Low-risk does not equate to no risk for any athlete with a stress fracture. A treatment plan should always be tailored to the individual’s athletic and personal goals, with an honest discussion of the risks and benefits of continued participation versus relative or absolute rest. In the treatment of low-risk stress fractures, a major consideration is often where the athlete is in his or her competitive season. Athletes at the end of a competitive season or in their off season often desire to be healed from their stress fracture before resumption of preseason training or competition. For these athletes, treatment includes relative rest and activity modification to a pain-free level. The acceptable level of activity differs for each athlete and may include discontinuation of only the aggravating activity alone, discontinuing all training activities, or placing the patient on non–weightbearing status (Table 1). To maintain fitness, athletes should be allowed to cross-train if it is pain-free. Frequent cross-training activities include cycling, swimming, and aqua-running. Low-risk stress fractures usually heal when the athlete is limited to pain-free activity for 4 to 8 weeks [26]. This period of healing is an ideal time to assess the modifiable risk factors that may decrease the chance for recurrent injury. Gradual increase in activity (activities of daily living) should begin after the athlete is pain-free and the site is nontender [26].

Table 1 Low-risk stress fracture treatment guide Symptoms

Goal

Treatment suggestions

Any level of pain

Heal injury

Pain with no functional limitations

Continue participation

Pain with functional limitation

Continue participation

Limiting pain intensifies despite functional activity modification (ie, unable to continue to perform at any reasonable functional level despite activity modification)

Heal injury

Titrate activity to a pain-free level for 4–8 w depending on the grade of injury Braces/crutches Modify risk factors Titrate activity to a stable or decreasing level of pain Closely follow Modify risk factors Decrease activity level to point at which pain level is decreasing and until a functional level of pain has been achieved, then titrate activity to stable or continued decrease level of pain Modify risk factors Complete rest Immobilization Surgery Modify risk factors

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Although there are no supporting data, a common recommendation is that no more than a 10% increase in activity should be added per week of training. In contrast, athletes in the midst of their competitive season with low-risk stress fractures often desire to finish the season and treat for a cure later. A treatment plan for these individuals should be based on their ability to function at the time of diagnosis. Those athletes who present with pain without functional limitation should be able to continue participation, using pain to guide their activities (see Table 1). They may continue to train and compete at a level that does not cause the pain to intensify. Hence, relative rest and activity modification are titrated to the level of discomfort. When athletes who have low-risk stress fractures have pain that limits their function, they should be treated with activity modification for training and activities of daily living until the pain decreases to a functional level. The goal is to decrease the repetitive stress at the fracture site enough to allow the body to restore the dynamic balance between damage and repair. This strategy may include decreasing volume and intensity of activity, equipment changes, technique changes, or cross-training. One benefit to such a strategy is that the athlete typically does not suffer a substantial loss of conditioning or competition while allowing their body to repair the bone injury. If their pain intensifies and activity modification alone is inadequate for recovery, then treatment should be intensified to include complete rest, immobilization, or surgical intervention. Athletes diagnosed with a stress reaction or low-grade injury at a low-risk site should follow treatment guidelines similar to those of a higher-grade injury. The major difference is the expected time of treatment and the degree of relative rest required. It has been shown that grade 1 and 2 stress reactions can heal with no changes in activity level [29]. In Arendt and Griffith’s [21] study, return to full activity for early stress injuries (grade 1, 3.3 weeks; grade 2, 5.5 weeks) was significantly faster than for more severe injuries (grade 3, 11.4 weeks; grade 4, 14.3 weeks). This finding stresses the importance of temporarily modifying activity to the level at which symptoms and injuries do not progress. This study also demonstrated the value of grading the severity of the fatigue failure. A low-grade stress fracture at a low-risk site has a better prognosis for time to recovery than a higher-grade injury at the same low-risk site. In addition to modification of activities, there are treatment modalities that have been shown to increase the healing rate and decrease the time to return to play. For example, in the treatment of tibial stress fractures, the use of pneumatic leg braces has been effective in reducing healing time [30]. It is also important to evaluate the nutritional history, menstrual history, training schedule, and equipment use of any athlete with a bone stress injury before returning the athlete to play. MANAGEMENT OF AND RETURN-TO-PLAY STRATEGIES FOR HIGH-RISK FRACTURES Return-to-play considerations for athletes who have high-risk stress fractures are more difficult than for low-risk stress fractures (Table 2). In general, return

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should be recommended only after proper treatment and complete healing of the injury. As previously mentioned, high-risk stress fractures have more frequent complications such as delayed union, nonunion, and refracture. High-risk stress fractures also have a significantly poorer prognosis should they progress to complete fracture. The treatment for high-risk stress fractures should be based on the immediate goal of preventing any progression of the fracture and avoiding delayed healing, nonunion, or refracture. Depending on the exact site and grade of the high-risk stress fracture, this treatment often requires absolute rest or internal fixation. Avoiding delay in diagnosis of a high-risk stress fracture is key to minimizing the risk of potential complications. If radiographs do not demonstrate a stress fracture but the history and examination are concerning for a stress fracture in a high-risk area, then further imaging should be pursued to exclude a stress fracture before returning the athlete to play [5]. Because of the significant complications associated with injury progression, it is suggested that individuals who have evidence of a high-risk stress fracture do not continue to participate in their activity. Depending on the site of the high-risk stress fracture, prolonged immobilization with non–weight-bearing restrictions or operative management are often the treatments of choice. The low-grade injury at a high-risk location should be managed with the goal of healing based on the individuals risk for reinjury and desired speed of recovery. Most early stress reactions at high-risk sites (grades 1 and 2) heal with nonoperative management [5]. A period of rest to eliminate the individuals’ symptoms and a return to training with activity modification is suggested for early stress reactions at high-risk sites. The key difference between a low-grade stress fracture at a high-risk versus a low-risk location is that an individual who has a low-grade fracture at a low-risk site can be allowed to continue to compete but an individual who has a low-grade fracture at a high-risk site needs to heal before full return to activity. This difference is due to the marked increased risk of significant complication with fracture progression at the high-risk site. This risk is unacceptable in the vast majority of cases. For example, a runner may be allowed to continue to run with stable and tolerable pain with a second metatarsal stress fracture but not a superior femoral neck stress fracture. The risk associated with progression of the second metatarsal fracture is minor compared with the risk of progression of the femoral neck stress fracture. Regardless of grade and location, the risk of continued participation should be discussed with each athlete. The management of each fracture should be individualized. For example, a recreational runner with a low-grade stress reaction of the fifth metatarsal can be treated with an ankle-foot orthosis boot and cross-training until symptoms resolve and healing is noted radiographically. Cross-training can maintain fitness at high levels [31,32]. Highly competitive athletes who place a greater amount of stress at these high-risk locations are at increased risk for fracture progression and reinjury and, in the opinion of the authors, should be managed aggressively. For example, a competitive runner with a grade 3 stress reaction of the fifth meta-

Complications

Displacement Nonunion Avascular necrosis

Nonunion Delayed union Fracture progression

Fracture progression Nonunion

Nonunion Delayed union Displacement

Anatomic site

Femoral neck

Anterior tibia

Medial malleolus

Tarsal navicular

Tension: Strict NWB or bed rest Surgical fixation RTP when healed Compression: NWB until pain-free with radiographic evidence of healing, then slow activity progression RTP after no pain on examination or with any activities Surgical fixation (optional) Nonoperative: NWB until pain-free with ADL; pneumatic leg splints RTP with slow progression after nontender and pain-free with ADL (9 mo) Operative: Intramedullary nailing RTP is usually faster (2–4 mo) Nonoperative: (No fracture line) 4–6 wk pneumatic casting Avoid impact; rehabilitation RTP when nontender, no pain with ADL Operative: (Fracture line, nonunion, or progression) ORIF with bone graft Nonoperative: NWB cast 6–8 wk, then WB cast 6–8 wk RTP is gradual after pain-free with ADL Orthotics and rehabilitation suggested Operative: (Complete, nonunion) RTP only when healed

Suggested treatment

Table 2 Management of and return-to-play strategies for high-risk stress fractures

Levels C and D

Levels C and D

Level A (RCT) Level B (nonrandomized) Levels C and D

Level C (expert opinion) Level D (case series)

Level of data

24 DIEHL, BEST, KAEDING

Displacement Fracture completion

Nonunion Delayed union Refracture Nonunion Delayed union Refracture

Patella

Seasmoids

Nonoperative: NWB cast 6–8 wk RTP is Gradual after pain-free with ADL Orthotics and rehabilitation suggested Operative: Reserved for nonunion Nonoperative: (Nondisplaced) Long-leg NWB cast 4–6 wk Rehabilitation following RTP is gradual after pain-free with ADL Operative: Horizontal—ORIF Vertical—lateral fragment excision RTP when healed Nonoperative: NWB 6–8 wk RTP is gradual after pain-free with ADL Operative: Excision if fail nonoperative Nonoperative: (No fracture line) NWB cast 4–6 wk followed by WB cast until healed RTP after nontender and pain-free Operative: (Fracture line, nonunion, or individual at high risk for refracture) Intramedullary screw fixation RTP 6–8 wk, early ROM/rehabilitation Levels C and D

Level C

Level C

Level C

Abbreviations: ADL, activities of daily living; NWB, non–weight bearing; ORIF, open reduction with internal fixation; RCT, randomized controlled trial; ROM, range of motion; RTP, return to play; WB, weight bearing.

Fifth metatarsal

Nonunion Delayed union

Talus

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tarsal should consider operative management because of the reported high incidence of recurrence at the same site after healing with nonoperative methods. This aggressive treatment may prevent the athlete from having a repeat injury in a subsequent season. Similarly, running athletes with anterior cortex stress fractures of the tibia may return to activity faster with surgical management compared with conservative treatment. In summary, surgical intervention may be considered for high-risk stress fractures for several reasons. Surgical intervention may speed healing of the fracture and allow earlier return to play (the tibial shaft dreaded black line is often nailed to achieve this goal). Another indication for surgical intervention may be to prevent refracture (eg, the internal fixation of a proximal fifth metatarsal stress fracture). A third indication for surgery is to prevent a catastrophic fracture progression (eg, the internal fixation of a femoral neck stress fracture). UPPER EXTREMITY Upper-extremity stress fractures account for less than 10% of all stress fractures and are commonly found in throwing athletes and rowers. There has been increased attention focused on upper-extremity stress fractures in recent years. Upper-extremity stress fracture sites are primarily considered low risk and heal with activity modification alone. The one exception may be an olecranon stress fracture in a competitive thrower. This stress fracture heals well before a fracture line forms with conservative management [33]; however, if a true stress fracture line is found in a throwing athlete’s olecranon, then the individual may be better served with internal fixation (level C and D) [34]. SUMMARY Stress fractures are common injuries, particularly in endurance athletes. Stress fracture management should take into consideration the injury site (low versus high risk), the grade (extent of microdamage accumulation), and the individual’s competitive situation. Low-risk stress fractures usually respond well to nonoperative management, and treatment is largely guided by the patient’s symptoms. High-risk stress fractures should be treated more aggressively with absolute rest or surgical fixation, with the goal of fracture healing and minimizing risk of complete fracture or refracture. The overall goal of treatment is to allow activity and avoid deconditioning when appropriate, while minimizing the risk of significant complication to the athlete. Overtreatment of low-risk stress fractures can result in unnecessary deconditioning and loss of playing time. Undertreatment of a high-risk stress fracture may place the athlete at risk of a significant complication, putting the athlete’s career at risk. Understanding the classification and grade of stress fractures and their implications on returnto-play decisions is key to optimal care of the athlete. References [1] Matherson GO, Clement DB, McKenzie DC, et al. Stress fractures in athletics: a study of 320 cases. Am J Sports Med 1987;15:46–58.

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[2] Kadel NJ, Teitz CC, Kronmal RA. Stress fractures in ballet dancers. Am J Sports Med 1992; 20:445–9. [3] Bennell KL, Malcolm SA, Thomas SA, et al. The incidence and distribution of stress fracture in the competitive track and field athletes. Am J Sports Med 1996;24:211–7. [4] Boden BP, Osbahr DC, Jimenez C. Low-risk stress fractures. Am J Sports Med 2001;29: 100–11. [5] Boden BP, Osbahr DC. High-risk stress fractures: evaluation and treatment. Am Acad Orthop Surg 2000;8(6):344–53. [6] Korpelainen R, Orava S, Karpakka J, et al. Risk factors for recurrent stress fractures in athletes. Am J Sports Med 2001;29:304–10. [7] Cowan DN, Jones BH, et al. Lower limb morphology and risk of overuse injury among male infantry trainees. Med Sci Sports Exerc 1996;28:945–52. [8] Hoffman JR, Chapnik L, Shamis A, et al. The effect of leg strength on the incidence of lower extremity overuse injuries during military training. Mil Med 1999;164:153–6. [9] Bennell KL, Matherson G, Meeuwisse W, et al. Risk factors for stress fractures. Sports Med 1999;28:91–122. [10] Barrow GW, Saha S. Menstral irregularity and stress feactures in collegiate female distance runners. Am J Sports Med 1988;16:209–16. [11] Almeda SA, Williams KM, Shaffer RA, et al. Epidemiological patterns of musculoskeletal injuries and physical training. Med Sci Sports Exerc 1999;30:1176–82. [12] Gardner LI, Dziados JE, Jones BH, et al. Prevention of lower extremity stress fractures: a controlled trial of shock absorbent insole. Am J Public Health 1988;78:1563–7. [13] Giladi M, Milgrom C, Kashtan H, et al. Recurrent stress fractures in military recruits. One-year follow-up of 66 recruits. J Bone Joint Surg Br 1986;68:429–41. [14] Beck BR. Tibial stress injuries: an aetiological review for the purposes of guiding management. Sports Med 1998;26:265–79. [15] Bennell KL, Malcolm SA, Wark JD, et al. Models for the pathogenesis of stress fractures in athletes. Br J Sports Med 1996;30:200–4. [16] Johnell O, Rausing A, Wendeberg B, et al. Morphological bone changes in shin splints. Clin Orthop 1982;167:180–4. [17] Jones BH, Thacker SB, Gilchrist J, et al. Prevention of lower extremity stress fractures in athletes and soldiers: a systematic review. Epidemiol Rev 2002;24:228–47. [18] Wilcox JR, Moniot AL, Green JP. Bone scanning in the evaluation of exercise-related stress injuries. Radiology 1977;117:699–703. [19] Couture CJ, Karlson KA. Tibial stress injuries. Physician Sports Med 2002;30:29–37. [20] Torg JS, Pavlov H, Freiberger RH. Stress fractures of the tarsal navicular. A retrospective review of twenty-one cases. J Bone Joint Surg Am 1982;4:700–12. [21] Arendt EA, Griffiths HJ. The use of MR imaging in the assessment and clinical management of stress reactions of bone in high-performance athletes. Clin Sports Med 1997;16: 291–306. [22] Gaeta M, Minutoli F, Seribano E, et al. CT and MR imaging findings in athletes with early tibial stress injuries. Radiology 2005;235:553–61. [23] Lee JK, Yao L. Stress fractures: MR imaging. Radiology 1988;169:217–20. [24] Stafford SA, Rosenthal DI, Gebhardt MC, et al. MRI in stress fracture. AJR Am J Roentgenol 1986;147:553–6. [25] Amendola A. MRI of foot and ankle: the orthapedic surgeon’s perspective in ractical MR imaging of the foot and ankle. Boca Raton (FL): CRC Press LLC; 2000. [26] Brukner P, Bradshaw C, Bennell K. Managing common stress fractures: let risk level guide treatment. Physician Sports Med 1998;26(8):39–47. [27] Orava S, Hulkko A. Delayed unions and nonunions of stress fractures in athletes. Am J Sports Med 1988;16:378–82. [28] Fredericson M, Bergman AG, Hoffman KL, et al. Tibial stress reactions in runners; correlation of clinical symptoms and scintigraphy with a new magnetic resonance imaging grading system. Am J Sports Med 1995;23:472–81.

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[29] Chisin R, Milgrom C, Giladi M, et al. Clinical significance of nonfocal scintigraphic findings in suspected tibial stress fractures. Clin Orthop 1987;220:200–5. [30] Swenson EI, DeHaven KE, Sebastianelli WJ, et al. The effect of a pneumatic leg brace on return to play in athletes with tibial stress fractures. Am J Sports Med 1997;25(3):322–8. [31] Eyestone ED, Fellingham G, George J, et al. Effect of water running and cycling on maximum oxygen consumption and 2-mile run performance. Am J Sports Med 1993;21: 41–4. [32] Frangolias DD, Taunton JE, Rhodes EC, et al. Maintenance of aerobic capacity during recovery from right Jones’ fracture. Clin J Sports Med 1997;7:54–8. [33] Schickendantz MS, Ho CP, Koh J. Stress injuries of the proximal ulna in professional baseball players. Am J Sports Med 2002;30:737–41. [34] El Attrache NS, Ahmad CS. Valgus extension overload syndrome and olecranon stress fractures. Sports Med Arthroscopy Rev 2003;11:25–9.

Clin Sports Med 25 (2006) 29–36

CLINICS IN SPORTS MEDICINE Treatment of Stress Fractures: The Fundamentals William Glenn Raasch, MD*, David J. Hergan, MD Department of Orthopaedic Surgery, Medical College of Wisconsin, 9200 W. Wisconsin Ave., Milwaukee, WI 53226, USA

I

n 1855, Breithraupt [1] first described the overuse injury to the fifth metatarsal in marching Prussian soldiers. The injury, commonly known as “march fracture,” was not confirmed until 40 years later with the advent of radiography. It was not until 1958 that Devas [2] first reported this injury in athletes. The stress fracture is now recognized as a common source of pain and dysfunction in an active population. It is this important first step of recognition that allows for an accurate diagnosis and subsequent treatment plan. Because of the often-insidious onset of symptoms, a high index of suspicion is required. By being familiar with a sport and its associated injuries, the clinician is better positioned for a more timely diagnosis. In other words, you cannot treat what you are not looking for. Several studies have addressed the epidemiology of stress fractures, highlighting the sports in which injury is more common. For example, Johnson and colleagues [3], in a 2-year prospective study on the incidence of stress fractures in the collegiate athletes, the stress fracture rate in males was highest in trackand-field (9.7%), followed by lacrosse (4.3%), crew (2.4%), and football (1.1%). In the female population, the stress fracture rate was also highest in trackand-field (31.1%), followed by crew (8.2%), basketball (3.6%), lacrosse (3.1%), and soccer (2.6%). Several studies have also reported on the anatomic distribution of stress fractures, with the most common sites being the tibia, metatarsals, and fibula [4,5]. Bennell and colleagues [4] followed 111 competitive track-and-field athletes over 12 months and reported 26 stress fractures, with 46% of injuries involving the tibia, 15% the navicular, and 12% the fibula. Smrcina [6] also reported that 95% of all stress fractures occur in the lower extremity. The predominance of lower-extremity involvement reflects the high repetitive loads typically experienced by a weight-bearing bone compared with the non–weight-bearing upper extremity. That is not to say that the upper extremity is free from destructive force. Racquet and overhead throwing sports create high levels of stress in * Corresponding author. E-mail address: [email protected] (W.G. Raasch).

0278-5919/06/$ – see front matter doi:10.1016/j.csm.2005.08.013

© 2005 Elsevier Inc. All rights reserved. sportsmed.theclinics.com

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a repetitious fashion, the ingredients necessary for a stress fracture. Motion analysis of the baseball player has confirmed the significant forces that occur at the shoulder and elbow during the overhead throwing motion. Subsequently, humeral shaft, olecranon, and clavicle stress fractures have been reported in the throwing athlete [7–9]. In the tennis player, stress fractures have been reported in the humerus [10], distal radius [11], and ulna [12,13]. With ulnar fractures, the injury involved the nondominant arm in players using a twohanded backhand. Again, knowing the sport and location in which a stress fracture is likely is the first step in making the diagnosis, allowing for an appropriate treatment plan. TREATMENT PRINCIPLES When considering treatment plans for a stress injury, one must understand why the injury occurs in the first place. Stress injuries occur when a physiologic load is placed on a bone in a repetitive fashion at a rate at which the body does not have time to recover. The load is considered insufficient to cause acute injury but, when combined with a cyclic pattern, can result in chronic injury. It is the “right” (or better stated, “wrong”) combination of load, repetition, and inadequate recovery that eventually results in injury. Extrinsic and intrinsic factors may contribute to the occurrence of a stress fracture and, alternatively, provide an avenue of treatment. Extrinsic factures that have been suggested as leading to injury include training regimens, playing equipment (footwear, playing surface), and nutritional habits. Intrinsic factors include anatomic variation, muscle endurance, and hormonal effects. EXTRINSIC TREATMENT Training Regimen An increase in activity is often the triggering event for a stress injury. Numerous military studies have shown the high rate of stress injury during basic training for which a progressive and demanding exercise regimen is required [14–20]. These military studies provide a relatively uniform patient population that, by order of the commanding officer, is highly compliant. When an increase in activity is noted in the patient’s history, activity modification is often the starting point for treatment. With activity modification, the athlete is simply unloading the injured bone, allowing the natural repair process to catch up while doing no further harm. In addition, when taking a history of the athlete’s training, it is often helpful to further define the increase in activity with regard to duration, intensity, or frequency of training. This information may allow the clinician to recommend a more acceptable level of activity modification, such as restricting a runner’s distance to a preinjury level while allowing the athlete to satisfy his or her subjective need to run three times per week. It is also important for the athlete to understand that the initial activity modification is only a starting point and that it may require adjustment if symptoms persist. Often, the most important part of modifying an athlete’s activity is providing a formal plan to guide the recovery. Rarely is the recommendation, “Don’t play your

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sport for 6 weeks” acceptable to the competitive athlete. A more practical approach for the runner who “needs to run” is to instruct the athlete to half the distance and then increase by 10% per week. If discomfort arises at any time, the athlete must return to the previous level for an additional week. Although not always successful, the plan provides the athlete with reasonable guidelines and allows for continued running. Equipment An athlete’s equipment not only includes what they wear but also the surface on which they play. The most common equipment modification deals with footwear. Several studies have looked at the effect of increased cushioning on the incidence of stress fractures [21–23]. These studies tend to support the use of cushioning in the prevention of injuries to the foot, with a variable effect on tibial injuries. For instance, a randomized prospective study by Milgrom and colleagues [21] of 390 military recruits showed a lower incidence of metatarsal stress fractures during military training with modified basketball shoes compared with standard-issue boots. The study did not show the same reduction in tibial stress fractures. Another military study by Stacy and Hungerford [23] also showed a reduction in training injuries when soldiers of the New Zealand Army switched to running shoes during basic training. Although these studies do not directly address the use of a well-cushioned shoe or orthotic in the treatment of existing stress fractures, any modification that reduces impact would appear to be a reasonable treatment in shifting the balance from breakdown to repair. The surface on which an athlete participates may also have an effect on stress fractures. It has been implied that the more rigid the surface, the greater the risk for stress injury. In turn, a change in the running surface may have a significant effect on symptoms. For instance, a change from asphalt to a wellcushioned treadmill may allow the runner to maintain his or her mileage while reducing symptoms. Several studies however, have reported that hard surfaces are not associated with an increased risk of overuse injury [24–27]. In addition, Voloshin [28] studied the ability of different surfaces to absorb shock. He reported the opposite of what one might expect, noting that a grass surface absorbed less shock than an asphalt surface. From this evidence, one can extrapolate that the stress delivered to the bone is not just a product of ground reaction forces but a result of combined forces including those generated through muscle contraction. At present, the literature does not provide a definitive answer; the clinician must resort to a trial-and-error approach when recommending a change in running surfaces. Nutritional Habits Proper nutrition is necessary for optimal bone health in the young athlete. In a retrospective study, Myburgh and colleagues [29] reported a lower intake of calcium in athletes who had stress fractures. Disordered eating patterns must always be considered and corrected whenever a stress fracture is diagnosed. This is especially true in the female athlete who has multiple stress fractures. In such

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circumstances, the athlete must be evaluated for the female athletic triad [30], consisting of disordered eating, amenorrhea, and osteoporosis. Severe eating disorders are considered medical emergencies and often require a multidisciplinary approach including nutritional and psychologic counseling. INTRINSIC TREATMENT Anatomic Variation Variations in anatomy have been implicated as a cause for lower-extremity stress fractures. An example of this is Morton’s foot with a short, hypermobile first ray and a long second ray. In a study of second metatarsal fractures in ballet dancers by Khan and colleagues [31], six of the eight case reports were noted to have Morton’s foot. Giladi and coworkers [32] reported the higher incidence of tibial stress fractures in male recruits who had greater passive external rotation of the hip ( >60° ). Finally, Bennell and coleagues [33] reported that 70% of athletes diagnosed with a stress fracture had a limb-length discrepancy. With the recognition of these anatomic variations, treatment is simply limited to the correction of limb-length discrepancies and to educating the athlete on the increased risk of injury. Muscle Endurance Markey [34] proposed that muscle mass may disperse impact loads to bone and when muscles fatigue, the protective function is lost, resulting in an increased risk of stress fracture. Several military and athletic studies have suggested that the out-of-shape athlete is at greater risk for injury [35–37]. Winfield and colleagues [37] studied the incidence of stress reactions in 101 female US Marine Corps trainees for 10 weeks during physical training. They noted a higher rate of injury in trainees who ran fewer miles (< 2.8 miles per session) before commencement of training. It can be concluded that the least physically fit individuals would have the lowest muscle mass and endurance and tend to have the lowest bone density, making the bone more susceptible to injury. Strengthening the muscle groups around a stress fracture may provide controlled loading for bone remodeling and, subsequently, reduce the risk for recurrence. Hormonal Factors Low estrogen environments in the female athlete are associated with loss of bone-mineral density, predisposing the athlete to stress fracture. Myburgh and colleagues [29] found that runners who had decreased bone-mineral density were at greater risk for stress fracture. Several studies have shown that amenorrheic and oligomenorrheic athletes are especially at high risk of bone loss [34,37]. A complete menstrual history is required whenever a diagnosis of stress fracture is made in the young female athlete. Hormonal replacement therapy may provide some benefit in the maintenance of bone-mineral density in the amenorrheic athlete but must be in conjunction with nutritional and lifestyle counseling.

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OTHER TREATMENT MODALITIES Ultrasound A number of studies have shown that ultrasound is effective in reducing the healing time of acute fractures. In a prospective double-blind randomized study of 67 tibial shaft fractures, Heckman and colleagues [38] reported a significant decrease in healing time with the addition of ultrasound (86 ± 5.8 days versus 114 ± 10.4 days). Kristiansen and coworkers [39], in a prospective double-blind study of distal radius fractures, also noted a significant decrease in healing time (61 ± 3 days versus 98 ± 5 days). The literature is less supportive when directly addressing stress fractures. Rue and colleagues [40] performed a randomized double-blinded study of 26 midshipmen who had 43 tibial stress fractures. Pulsed ultrasound was applied daily for 20 minutes, but no significant reduction in healing time was found. The investigators recommended additional study using a higher dose and possibly longer period of treatment. At present, there is no definitive evidence that ultrasound may improve or accelerate the healing of stress fractures. Electrical and Electromagnetic Fields The clinical effect of electrical and electromagnetic fields on enhancing stress fracture healing is not clearly defined by the literature. Most studies deal with their effect on delayed unions or nonunions and are not specifically designed to evaluate the efficacy on stress fractures. Two studies [41,42] often sited in support of electromagnetic field treatment were unblinded without controls. Compounding the confusion is the various options in which a current may be directed to the fracture site. The modalities of bone-growth stimulation available include direct-current stimulation with percutaneous or implanted electrodes, electromagnetic stimulation by inductive coupling using time-varying magnetic fields, and capacitive-coupling stimulation using electrodes placed on the skin. Borsalino and colleagues [43], in 1988, published a double-blinded placebocontrolled prospective study on the healing effects of femoral intertrochanteric osteotomies. Significant increased bone healing was identified by greater bone density and trabecular bridging in the treatment group. The study supported the use of bone stimulators as an adjunct to treating acute fractures, but because stress fracture behavior is often very different from acute traumatic fracture behavior, the study provides little support for their use on stress fractures. Sharrard [44], in 1990, published a study on pulsed electromagnetic fields on delayed tibial unions. The trial took place over a 12-week period and had a successful union rate of 45% in the treated group compared with 14% in the placebo group. Scott and King [45] reported on the effect of capacitive-coupled electrical fields on 23 long-bone nonunions. Sixty percent of the nonunions treated with the coupled electromagnetic field healed in a mean of 21 weeks, whereas none of the placebo-controlled group went on to union. Although these two studies suggest a positive effect on bone healing in a nonunion, one must again take a mild leap of faith when applying these results to stress fractures.

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Intravenous Pamidronate Stewart and colleagues [46] reported on the use of intravenous pamidronate on five symptomatic collegiate athletes who had tibial stress fractures. Pamidronate is a second-generation bisphosphonate that is currently used in the treatment of osteoporosis, hypercalcemia, and metastatic bone disease. It is thought to affect osteoclastic activity by binding to calcium phosphate crystals. With decreased osteoclastic activity, the osteoblasts may catch up, allowing the bone to heal. A 30-mg test dose was given intravenously over 2 hours, followed by four additional treatments at weekly intervals in 60-mg or 90-mg amounts. With the initial treatment, four of five subjects were able to continue training without symptoms within 72 hours. The fifth patient missed 3 weeks of training. At a minimum of 49 months of follow-up, all athletes remained asymptomatic. These investigators believe that the treatment is promising and plan to do a prospective study. HIGH-RISK STRESS FRACTURES Any treatment plan for stress fractures must also take into consideration the inherent and specific risk for further injury. It is helpful when devising a treatment plan to understand the difference between the “safe” and “high-risk” stress injury. A stress fracture may be considered higher risk if it has a high propensity to progress to a complete fracture. In addition, the morbidity associated with the completed or possibly displaced fracture must also be considered. Essentially, the higher the risk, the greater the benefit of early surgical intervention to prevent further morbidity. Ultimately, the final grouping of a stress fracture into a high- or low-risk category is somewhat arbitrary; the clinician must be aware of the relative risk associated with each fracture. The stress fracture most commonly associated with a high level of morbidity after completion is the femoral neck fracture occurring on the lateral or tension side. Delayed diagnosis of such an injury could result in a displaced fracture, with the possibility of avascular necrosis. In one study by Johansson and colleagues [47], 60% of athletes who had an appropriately treated displaced femoral neck fracture were unable to return to their preinjury activity level. The anterior cortex of the middle third of the tibia is another fracture that, if ignored, may progress to catastrophic failure and be prone to delayed union and nonunion. Although less likely to progress than the femoral neck stress fracture, the morbidity associated with a midshaft tibial fracture must be considered when weighing the risks and benefits of early surgical intervention. Stress fractures at higher risk for complete fracture but with less associated morbidity include the base of the fifth metatarsal and the tarsal navicular. In the elite-level athlete, early surgical intervention is considered for both of these fractures, although nonsurgical intervention is often the first treatment option. References [1] Breithaupt MD. Zur pathologie des menschlichen fusses [To the pathology of the human foot]. Med Zeitung 1855;24:169.

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[2] Devas MB. Stress fractures of the tibia in athletes of ‘shin soreness.’ J Bone Joint Surg [Br] 1958;40:227–39. [3] Johnson AW, Weiss CB, Wheeler DL. Stress fractures of the femoral shaft in athletes— more common than expected: a new clinical test. Am J Sports Med 1994;22:248–56. [4] Bennell KL, Malcolm SA, Thomas SA, et al. The incidence and distribution of stress fractures in competitive track and field athletes. Am J Sports Med 1996;24:211–7. [5] Brukner PD, Bradshaw C, Khan KM, et al. Stress fractures: a review of 180 cases. Clin Sports Med 1996;6:85–9. [6] Smrcina C. Stress fractures in athletes. Nurs Clin North Am 1991;26:159–66. [7] Branch T, Partin C, Chamberland P, et al. Spontaneous fractures of the humerus during pitching: a series of 12 cases. Am J Sports Med 1992;20:468–70. [8] Nuber GW, Diment MT. Olecranon stress fractures in throwers: a report of two cases and a review of the literature. Clin Orthop 1992;278:58–61. [9] Adolfsson L, Lysholm J. Case report: clavicular stress fracture in a javelin thrower. Clin Sports Med 1990;2:41–5. [10] Rettig AC. Stress fracture in the humerus in an adolescent tennis tournament player. Am J Sports Med 1985;13:55–8. [11] Loosli AR, Leslie M. Stress fractures of the distal radius: a case report. Am J Sports Med 1991;19:523–4. [12] Bell RH, Hawkins RJ. Stress fracture of the distal ulna: a case report. Clin Orthop 1986; 209:169–71. [13] Bollen SR, Robinson DG, Crichton KJ, et al. Stress fractures of the ulna in tennis players using a double-handed backhand stroke. Am J Sports Med 1993;21:751–2. [14] Berstein A, Childers MA, Fox KW, et al. March fractures of the foot: care and management of 692 patients. Am J Surg 1946;71:355–62. [15] Berstein A, Stone JR. March fracture: a report of 307 cases and a new method of treatment. J Bone Joint Surg [Am] 1944;26:743–50. [16] Freaney RB, Gerber FH, Laughlin RL, et al. Distribution and natural history of stress fractures in US Marine recruits. Radiology 1983;146:339–46. [17] Giladi M, Ahronson Z, Stein M, et al. Unusual distribution and onset of stress fractures in soldiers. Clin Orthop Rel Res 1985;192:142–6. [18] Kreipe RE, Thompson JR. March fracture: an analysis of two hundred cases. AJR Am J Roentgenol 1944;52:282–90. [19] Leveton AL. March fractures of the long bones of the lower extremities and pelvis. Am J Surg 1936;71:222–32. [20] Scully TJ, Besterman G. Stress fractures: a preventable training injury. Mil Med 1982; 147:285. [21] Milgrom C, Giladi M, Stien M, et al. A prospective study of the effect of a shock absorbing orthotic device on the incidence of stress fractures in military recruits. Foot Ankle 1985; 6:101–4. [22] Schwellnus MP, Jordan G, Noakes TD. Prevention of common overuse injuries by the use of shock absorbing insoles. Am J Sports Med 1990;18:636–41. [23] Stacy RJ, Hungerford RL. A method to reduce work related injures during basic training in the New Zealand Army. Mil Med 1984;149:318. [24] Hoeberigs JH. Factors related to the incidence of running injuries: a review. Sports Med 1992;13:408–22. [25] Macera CA. Lower extremity injuries in runners: advances in prediction. Sports Med 1992;13:50–7. [26] Marti B. Health effects of recreational running in women: some epidemiological and preventive aspects. Sports Med 1991;11:20–51. [27] Van Mechelen W. Running injuries: a review of the epidemiological literature. Sports Med 1992;14:320–5. [28] Voloshin KW. Dynamic loading during running on various surfaces. Human Mov Sci 1992;11:675–89.

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[29] Myburgh KH, Hutchins J, Fataar AB, et al. Low bone mineral density is an etiologic factor for stress fractures in athletes. Ann Intern Med 1990;113:754–9. [30] Nattiv A, Agostini R, Drinkwater BL, et al. the female athlete triad: the interrelatedness of disordered eating, amenorrhea and osteoporosis. Clin Sports Med 1994;13:405–18. [31] Khan K, Brown J, Way S, et al. Overuse injuries in classical ballet. Sports Med 1995;19: 341–57. [32] Giladi M, Milgrom C, Simkin A, et al. Stress fractures: identifiable risk factors. Am J Sports Med 1991;19:647–52. [33] Bennell KL, Malcolm SA, Thomas SA, et al. Risk factors for stress fractures in track and field athletes: a twelve-month prospective study. Am J Sports Med 1996;24:810–8. [34] Markey KL. Stress fractures. Clin Sports Med 1987;6:405–25. [35] Jones BH, Bovee MW, Harris JM, et al. Intrinsic risk factors for exercise-related injuries among male and female army trainees. Am J Sports Med 1993;21:705–10. [36] Valimaki VV, Alfthan H, Lehmuskallio E, et al. Risk factors for clinical stress fractures in male military recruits: a prospective cohort study. Bone 2005;37(2):267–73. [37] Winfield AC, Moore J, Bracker M, et al. Risk factors associated with stress reactions in female Marines. Mil Med 1997;162:698–702. [38] Heckman JD, Ryaby JP, McCabe J, et al. Acceleration of tibial fracture healing by noninvasive low-intensity pulsed ultrasound. J Bone Joint Surg [Am] 1994;76:26–34. [39] Kristiansen TK, Ryaby JP, McCabe J, et al. Accelerated healing of distal radial fractures with the use of specific, low-intensity ultrasound. A multicenter, prospective, randomized, double-blind, placebo-controlled study. J Bone Joint Surg [Am] 1997;79:961–73. [40] Rue JH, Armstrong DW, Frassica FJ, et al. The effect of pulsed ultrasound in the treatment of tibial stress fractures. Orthopedics 2004;27:1192–5. [41] Benazzo F, Mosconi M, Beccarisi G, et al. Use of capacitive coupled electric fields in stress fractures in athletes. Clin Orthop Rel Res 1995;310:145–9. [42] Rettig AC, Shelbourne KD, McCarroll JR, et al. The natural history and treatment of delayed union stress fractures of the anterior cortex of the tibia. Am J Sports Med 1988;16:250–5. [43] Borsalino G, Bagnacani M, Bettati E, et al. Electrical stimulation of human femoral intertrochanteric osteotomies: double blind study. Clin Orthop 1988;237:256–63. [44] Sharrard WJW. A double-blind trial of pulsed electromagnetic fields for delayed union of tibial fractures. J Bone Joint Surg Br 1990;72:347–55. [45] Scott G, King JB. A prospective double blind trial of electrical capacitive coupling in the treatment of non-union of long bones. J Bone Joint Surg Am 1994;76:820–6. [46] Stewart GW, Brunet ME, Manning MR, et al. Treatment of stress fractures in athletes with intravenous pamidronate. Clin J Sport Med 2005;15:92–4. [47] Johansson C, Ekenman I, Tornkvist H, et al. Stress fractures of the femoral neck in athletes: the consequence of a delay in diagnosis. Am J Sports Med 1990;18:524–8.

Clin Sports Med 25 (2006) 37–52

CLINICS IN SPORTS MEDICINE Epidemiology of Stress Fractures Rebecca A. Snyder, BAa, Michael C. Koester, MD, ATCa,*, Warren R. Dunn, MD, MPHb a b

Vanderbilt Sports Medicine, Medical Center East, South Tower, Suite 3200, Nashville, TN 37232, USA Heath Services Research Center, 6000 Medical Center East, North Tower, Nashville, TN 37232-8300, USA

S

tress fractures are a frequent cause of injury in competitive and recreational athletes. The pathophysiology of stress fracture has been well described in the literature. Data regarding the epidemiology of stress fractures in athletes, including injury patterns and risk factors, are lacking. Clinical experience suggests that stress fractures occur more frequently in sports involving repetitive weight-bearing activity; however, little else is known. This article briefly discusses the intricacies of sports injury epidemiology and reviews the current literature regarding stress fracture incidence, characteristics, and morbidity. Because the focus is on competitive and recreational athletes, the discussion does not include a review of the large body of literature pertaining to stress fractures in military recruits. METHODS To ensure a comprehensive review of available studies, a literature search was conducted using the MEDLINE database. The terms “stress fracture,” “athletes,” “epidemiology,” and “incidence” were searched from 1966 through May 2005. The references of all retrieved articles also were reviewed. Prospective studies were searched for initially, but the inclusion criteria were expanded after only three such studies were identified [1–3]. Retrospective medical record reviews were then included. Studies using patient surveys to determine stress fracture prevalence were excluded from the review because of the potential for recall bias. Overall, a total of 25 studies were identified and thoroughly reviewed. EPIDEMIOLOGY OF SPORTS INJURIES Injury Exposure Epidemiology is the study of diseases in populations, including the relationship between exposures and outcomes. For the purpose of this discussion, the term “exposure” is defined as athletic activity, and the occurrence of a stress

* Corresponding author. E-mail address: [email protected] (M.C. Koester). 0278-5919/06/$ – see front matter doi:10.1016/j.csm.2005.08.005

© 2005 Elsevier Inc. All rights reserved. sportsmed.theclinics.com

38

SNYDER, KOESTER, DUNN

fracture is the outcome of interest. One of the major challenges in sports injury epidemiology is the process of defining and collecting meaningful exposure data [4]. A quantitative measure of injury exposure is often not accounted for in studies, and data are expressed as the number of injuries per athlete over a given time period (eg, a calendar year or a season). Although this calculation makes data collection easier, it does not always allow for the expression of injury risk because neither the number of at-risk athletes nor the quality and quantity of the exposure are expressed. Knowing the characteristics of the exposure in the at-risk population allows for a greater potential to generalize the findings of a particular study. Properly quantifying exposure can be difficult, and the methods depend on the sport being studied. Incidence rates are often measured by athlete-years, athlete- seasons, or athlete exposures. An athlete-year or athlete-season allows the researcher to account for the total number of participants over a stated period of time. An athlete exposure may consist of a single player participating in a single game or practice, or, for example, in football, it may be defined as an individual athlete participating in a single drill per practice or a single play per game. For sports such as cross-country and track and field, injuries per hour of activity may be more appropriate to consider. However, even this measure of risk does not account for all characteristics of the exposure, such as the intensity of the exposure. Assessing Injury Incidence and Risk Identifying the population at risk is one of the most important tasks in properly designing a sports injury study [4]. The population at risk is defined in the denominator as the total number of active participants. The rate is often misused but is considered an instantaneous measure of how fast a disease is occurring in the population (eg, fractures per week). A proportion describes what fraction of the population is affected and is expressed as a percentage or probability. Incidence is equal to the total number of new injuries occurring during a specified period of time divided by the population at risk. Injury incidence may be reported as a measure of cumulative incidence or as an incidence rate. Because cumulative incidence is a measure of events, it is also a measure of risk [5]. An incidence calculated over a specified time period during which all of the individuals are considered at risk for the outcome is called the “cumulative incidence” [5]. The cumulative incidence of a stress fracture, therefore, is estimated by dividing the number of stress fractures by the number of subjects in the study at the beginning of the observation period. Cumulative incidence is time-dependent; therefore, longer observation periods will likely yield a greater measured incidence because the population has a longer total exposure time. In the case of an observation period of several years, this can be adjusted for by calculating a cumulative annual incidence, which gives a proportion expressed as injuries per year. An incidence rate may be calculated when everyone in the population does not have an equal exposure or everyone has been observed for varying lengths of time. It is estimated by

EPIDEMIOLOGY OF STRESS FRACTURES

39

dividing the number of events by the number of subjects per time period (athleteseasons or athlete-year). Incidence rates allow for an easier comparison and contrast of multiple studies but do not account for differences in the population at risk or the variation in exposure. The majority of studies reviewed report a proportion of individuals who developed a stress fracture of the total number of individuals who were evaluated at some point during the observation period. Because the studies did not use the number of subjects per time period in the denominator, the measurements cannot be considered incidence rates. Proportions were typically reported as either a participant proportion or case proportion, depending on the numerator. A participant proportion uses the number of athletes with stress fractures as the numerator, whereas a case proportion assesses the total number of stress fractures, accounting for athletes with multiple stress fractures during the study period. The denominator for both equations is the total number of athletes at risk at some point over the study population. Of the studies evaluated for the present review, most report the participant proportion or both the participant proportion and the case proportion. Also, several of the studies do not clarify whether they are providing the number of athletes with stress fractures or the number of stress fractures. In these situations, a conservative assumption was made that the authors were providing the number of athletes with stress fractures and, thus, considered the measure to be a “participant proportion.” Study Design Three separate study designs predominate in the stress fracture literature: case series, prospective cohorts, and retrospective cohorts. A case series consists of a population of individuals who have experienced the exposure and have developed the outcome of interest. Risk factors cannot be determined, nor can anything of interest be learned regarding the population at risk. Injury data reported without a denominator can describe only injury frequency [6]. Few conclusions can be drawn about the outcome because a variety of factors may result in an unrepresentative sample of injuries presenting to a given clinic. A cohort design can be conducted prospectively or retrospectively. Each design allows for comparing athletes with and those without the outcome. Because the entire population at risk is defined at the beginning of the study, potential risk factors can be evaluated more easily. There are many differences between prospective and retrospective study designs. Most important, the retrospective cohort has already experienced the exposure; thus, data collection is subject to selection factors, inaccurate or incomplete record keeping, and, in the case of survey studies, to recall bias. The prospective cohort is the preferred design because it permits the ongoing collection of predetermined data sets over a specific period of time. Method of Diagnosis The validity of sports injury data depends on the definition of injury in the study population. Although all of the studies in this review used stress fracture

Retrospective

Prospective

Retrospective

Retrospective

Retrospective

Retrospective

USA

Australia

USA

Canada

Australia

USA

Arendt et al [8] 2003 Bennell et al [1] 1996 Brubaker and James [15] 1974 Clement et al [11] 1981 Dixon and Fricker [26] 1993 Goldberg and Pecora [9] 1994

Study design

Country

Study

Table 1 Proportion of athletes with stress fractures

NCAA

Gymnasts

All

T-F

T-F

NCAA

Sport

3000

42/74

987/663

109

49/46

3610/2248

Number (M/F)

Review of medical records

Review of medical records Review of medical records

Review of medical records

Review of medical records Monitoring

Data collection

3

10

2

17

1

10

Observation period (y)

XR/BS

XR/BS

NR

NR

BS/CT

MRI/BS/XR

Diagnosis

1.9/NR/NR

26.7/21.4/ 29.7

5.3/4.9/5.9

21.1/20.4/ 21.7 15.6/NR/NR

1.0/0.8/1.9

Participant proportion (T/M/F)

NR

NR

NR

27.4/24.5/ 30.4 NR

NR

Case proportion (T/M/F)

40 SNYDER, KOESTER, DUNN

Retrospective

Retrospective

Retrospective

Prospective

Retrospective

Retrospective

Prospective

Retrospective

USA

Australia

Japan

USA

USA

Canada

USA

USA

All

T-F

All

NCAA

NCAA

All

Basketball

NCAA

680/309

275

867/540

0/199

593/321

6415/3861

0/49

5900

Review of medical records

Review of medical records Review of medical records Monitoring

Monitoring

Review of medical records Review of medical records Review of medical records

4.5

3

5

1

2

10

5

14

NR

XR/MRI

NR

XR

XR/BS

MRI/BS/XR

NR

NR

0.5/NR/NR

7.8/5.5/ 11.5 8.7/NR/NR

NR/NR/6.5

2.6/NR/NR

1.9/2.0/1.9

NR/NR/40.8

1.4/NR/NR

NR

NR

NR

NR

3.7/2.0/6.9

NR

NR

NR

Abbreviations: BS, bone scan; F, female; M, male; NCAA, National Collegiate Athletic Association; NR, not recorded; T, total; T-F, track and field; XR, radiography.

Hame et al [10] 2004 Hickey et al [32] 1997 Iwamoto and Takeda [12] 2003 Johnson et al [2] 1994 Lloyd et al [7] 1986 Matheson et al [13] 1989 Nattiv et al [3] 2000 Witman et al [14] 1981

EPIDEMIOLOGY OF STRESS FRACTURES 41

42

SNYDER, KOESTER, DUNN

as the outcome, the methods of diagnosis varied. When comparing injury data among studies, the diagnostic tool must be considered because it may greatly affect the number of stress fractures reported. For example, Lloyd and colleagues [7] defined cases using only plain radiographs, although there may be a 2- to 4-week delay in stress fracture diagnosis using this method. Thus, stress fracture incidence may be under-reported in studies using only plain radiographs to diagnose stress fracture. Also, tarsal stress fractures are notoriously difficult to diagnose by radiography, potentially resulting in a delayed or missed diagnosis. Conversely, both MRI and bone scans are sensitive and will detect stress fractures at an early stage. MRI scanning, particularly, is quite sensitive and detects bone “stress injury,” a precursor to an actual stress fracture. Studies using MRI scans will likely detect a higher incidence of stress fractures and stress reactions compared with other diagnostic tests. Unfortunately, many of the studies did not identify the method of diagnosis. These studies must be interpreted with caution because the validity of the results cannot be determined. RESULTS Fourteen cohort studies were identified that provided a measure of either the proportion or cumulative incidence of stress fractures among athletic populations (Table 1). Each study that was reviewed observed different athlete populations, including recreational and competitive athletes, collegiate athletes, track and field athletes, gymnasts, and basketball players. Because of the variety in sport, frequency, and intensity of activity, caution should be exercised in comparing results across studies. Furthermore, because the study observation periods varied from 1 to 17 years and the subject population was often variable during the duration of the study, it is difficult to compare the proportions of athletes with stress fractures across groups. Subject populations in the 14 studies consisted of either all of the athletes participating in a sport at an institution or all of the athletes who presented to a sports medicine or orthopedic clinic. It is important to make several important distinctions between these two study designs. First, the medical records reviewed from a sports medicine or orthopedic clinic include records from only those patients who were referred to the clinic. Therefore, because some participants who develop stress fractures may not seek treatment or may see only their primary care physician, the potential for referral bias was introduced into these studies. Second, studies that include all athletes participating in a sport in the denominator are more accurate than studies limited to the “injured athletes” (individuals who present to a clinic) or in the denominator. Three of the 14 studies were prospective studies [1–3]. Bennell and colleagues [1] and Nattiv and colleagues [3] evaluated stress fractures in track and field athletes in Australia and the United States, respectively. Johnson and colleagues [2] prospectively studied collegiate athletes. In addition to these three prospective studies, 11 retrospective studies were identified that evaluated the occurrence of

EPIDEMIOLOGY OF STRESS FRACTURES

43

stress fracture in an athletic population by a review of medical records. Of the five studies that evaluated collegiate athletes, the proportion of athletes with stress fractures range from 1.0% to 2.6% [2,7–10]. Four studies assessed what proportion of recreational or competitive athletes who visit a sports medicine or orthopedic clinic present with stress fractures, and their findings range from 0.5% to 7.8% [11–14]. Of the studies that focus on track and field athletes, Nattiv and colleagues and Bennell and colleagues report cumulative annual incidences of 8.7% and 21.1%, respectively [1,3]. Brubaker and colleagues [15] have reported that 15.6% of individuals who visited an orthopedics clinic with a running-related injury presented with stress fractures. A great deal of variation exists among studies reporting stress fractures as a proportion of total athletic injuries, likely because of differences in the populations studied and variations in the definition of all injuries reported (Table 2). In track and field athletes, James and colleagues [16] have reported that stress fractures accounted for 6.0% of all reported injuries, whereas Bennell and colleagues [1] have reported a proportion of 20%. Other studies assessing athletes from multiple sports have found that stress fractures account for 0.5% to 4.8% of all injuries [11,14]. Although methodologies differ, these contrasting results provide evidence of the increased occurrence of stress fractures in track and field athletes.

Table 2 Stress fractures as a proportion of total injuries Study

Sport

Stress fractures/ total injuries (%)

Stress fractures/ total injuries (M) (%)

Stress fractures/ total injuries (F) (%)

Bennell et al [1] 1996a Clement et al [11] 1981 Hickey et al [32] 1997 James et al [16] 1978 Witman et al [14] 1981 Dixon and Fricker [26] 1993b Hame et al [10] 2004b Lloyd et al [7] 1986b

T-F

20.0 (N = 26/130)

16.4 (N = 12/73)

24.6 (N = 14/57)

All

4.8 (N = 87/1819)

4.4 (N = 48/1081)

5.3 (N = 39/738)

Basketball

NR

NR

9.0 (N = 20/223)

T-F

6.0 (14/232)

NR

NR

All

0.5 (N = 5/951)

NR

NR

Gymnastics

51.7 (N = 31/60)

47.4 (N = 9/19)

53.7 (N = 22/41)

NCAA

22.9 (N = 80/349)

NR

NR

NCAA

NR

NR

52 (N = 13/25)

Abbreviations: F, female; M, male; NCAA, National Collegiate Athletic Association; NR, not recorded; T-F, track and field. a Percentage of musculoskeletal injuries. b Percentage of total fractures.

44

SNYDER, KOESTER, DUNN

STRATIFIED DATA Age The role of age as an independent risk factor for developing a stress fracture cannot be determined from the available literature. No study has controlled for activity level; thus, the distribution of fractures among age groups is more likely to be associated with training volume and intensity rather than the ages of the participants. There are no studies in athletes that suggest an independent effect of age on the occurrence of stress fractures. Studies in military recruits have had conflicting results as to whether recruits in their late 20s and early 30s are at an increased risk for stress fractures compared with their younger counterparts [17–19]. Only a handful of studies report stress fracture frequency by age group. Courtenay and Bowers [20] have reported that a higher proportion of stress fractures occurred among younger subjects. Goldberg and Pecora [9] have found that college freshman suffer far more stress fractures than upperclassmen; however, it is likely that this increased injury frequency reflects the sudden increase in training volume and intensity on initiation to college athletics. Following a retrospective chart review at a large sports medicine clinic, Matheson and colleagues [13] have reported a stress fracture incidence of 4.2% among older subjects (≥ 50 years old) and 11.2% among younger subjects (≤ 50 years old). Over 50% of athletes with stress fractures were younger than 20 years of age in one series, with 8% of the stress fractures occurring in 10- to 14-year-old athletes [12]. Ohta-Fukushima and colleagues [21] have reported five stress fractures in children under the age of 10, including a tibial stress fracture in a 6-year-old boy. Race There are few comparative data regarding stress fractures among different racial groups. The majority of studies come from Europe and North America, and few report race or ethnicity of the participants. Two studies from the United States have attempted to examine differences in stress fracture rates between African Americans and whites [3,22]. Barrow and Saha [22] have found no differences, but their data were compiled from a questionnaire and included a sample of only 12 African American athletes. Nattiv and colleagues [3] also have reported no significant differences in stress fracture incidence between African American and white collegiate track athletes (P ≤ .35). Studies from Japan and Korea show slight differences in fracture patterns compared with the more heavily studied white populations, but the differences are more likely related to the variation in activity rather than race [12,21,23]. Gender The female athlete triad (menstrual irregularity, disordered eating, and osteopenia) emphasizes the susceptibility of young female athletes to stress fracture and contributes to the clinical impression that females are at an increased risk for such injuries compared with young men. Two authors have reported significant findings in subpopulations of female athletes. Lloyd and colleagues [7] have found a difference in cumulative stress fracture incidence of 4% in girls with a

EPIDEMIOLOGY OF STRESS FRACTURES

45

regular menstrual history versus 15% in girls with irregular or absent menses (P ≤ .025). In a separate report, female athletes with a history of disordered eating suffered significantly more stress fractures (P ≤ .001) [3]. Clearly, more research is needed in this population, which may be at particular risk. Several descriptive studies have reported stress fracture rates in athletes stratified by gender, but few studies have been appropriately designed to assess true differences in risk. Hame and colleagues [10] have found that women experienced a higher proportion of stress fractures than men did (P = .001) in a population of college athletes, but the report did not provide specific details. Nattiv and colleagues [3] have reported no significant difference in stress fracture incidence between men and women (P ≤ .39), and neither did Iwamoto and Takeda [12]. The limitation of these studies is that all failed to account for total injury exposure (training volume) when comparing injuries between men and women. For example, Bennell and colleagues [1] have found a stress fracture incidence of 20.4% in men and 21.7% in women in a prospective study of track and field athletes. However, when stress fractures rates were adjusted for total training hours, a difference emerged. Men experienced 0.54 stress fractures per 1000 training hours versus 0.86 stress fractures per 1000 training hours for women [1]. This difference was not statistically significant (P = .82), but the study was not sufficiently powered to detect a statistically significant difference in stress fracture incidence rates [1]. Hence, although this difference was not statistically significant, it may be of clinical significance. Only a large prospective study, accounting for differences in volume and intensity of training, will definitively answer the question of gender differences in stress fracture risk. STRESS FRACTURE CHARACTERISTICS Fifteen studies provided sufficient details to allow a review of anatomic fracture sites, but the studies are of limited value in assessing fracture occurrence by sport. Few inferences can be made regarding specific injury patterns because of the heterogeneity of the study populations and inconsistent methodology. Variations in exposure will affect fracture patterns. In addition to the volume of activity, other potentially confounding variables include sports or activities, climate, and male-to-female participation ratios. For example, athletes in colder climates may run on frozen ground or use indoor surfaces, resulting in higher impact. On the other hand, some athletes may discontinue running for the winter and, thus, have no injury exposure. Factors such as these deserve consideration when interpreting limited epidemiologic data. Regional and national variations in sporting activities also may greatly affect the association between particular sports and stress fractures. A large study [12] of Japanese athletes found a majority of stress fractures occurring among basketball and baseball players, followed by track and field athletes and rowers. The injury exposure in these populations differed with the majority of reviewed studies from Europe and North America and resulted in a high proportion of rib (15.8%) and ulnar (8.2%) stress fractures [12]. Differences in injury exposure

46

SNYDER, KOESTER, DUNN

within a clinic population are highlighted by one study that details a large number of injuries in dancers, contrasting with few dancing injuries reported in the other studies [24]. A handful of authors have investigated the occurrence of stress fractures among intercollegiate athletes in the United States [2,7–10]. Compared with specialty clinic populations, these studies offer a more homogeneous population in regard to age and sporting activities. Unfortunately, few associations can be made between particular sports and fracture patterns in collegiate athletes (Table 3). The relatively small number of stress fractures sustained makes analysis difficult because even a slight variation in training practices may greatly influence stress fracture rates in a given population. Arendt and colleagues [8] detail an aggressive land training program initiated over one summer by the men’s hockey team, which resulted in five athletes with tibial stress fractures. These were the only stress fractures of the tibia suffered by male athletes over the 10-year observation period and comprised 14% of all stress fractures sustained by men in the study [8]. Stress fractures of the tibia, metatarsals, and fibula are the most frequently reported anatomic sites in the majority of studies (Table 4). Stress fractures of the femur, first metatarsal sesamoid, and pelvis were encountered far less commonly but had relatively similar rates of occurrence among studies. The occurrence of tarsal navicular fractures was variable, but overall, such fractures were Table 3 Sport-specific proportion of athletes with stress fractures Proportion of athletes with stress fracture Sport

Arendt et al [8] 2003

Goldberg and Pecora [9] 1994

Johnson et al [2] 1994

Basketball (T/M/F) Baseball (M) Crew (T/M/F) Cross-country (M/F) Fencing (T/M/F) Field hockey (F) Football (M) Golf (M/F) Gymnastics (T/M/F) Ice hockey (M/F) Lacrosse (T/M/F) Soccer (T/M/F) Softball (F) Swimming (T/M/F) Tennis (T/M/F) Track and field (T/M/F) Volleyball (T/M/F) Wrestling (M)

NR/2.9/3.6 0.3 NR 3.9/6.4 NR NR 0.3 0/0 NR/3.0/4.3 2.1/0 NR NR/NR/2.3 1.1 NR/0/0 NR/0/0.8 NR/0.8/1.6 NR 0

2.9/NR/NR 2.6 2.2/NR/NR NR 1.9/NR/NR 2.2 0.8 NR 2.8/NR/NR NR 2.7/NR/NR 2.0/NR/NR 6.3 1.3/NR/NR 2.8/NR/NR 3.7/NR/NR 2.4/NR/NR NR

NR/0/3.6 0 NR/2.4/8.2 NR NR/0/0 0 1.1 0/0 NR NR NR/4.3/3.1 NR/0/2.6 0 NR/0/0 NR/0/0 NR/9.7/31.1 NR/NR/0 NR

Abbreviations: F, female; M, male; NR, not recorded; T, total.

USA

Italy

Australia

Australia Australia USA Korea Finland

Japan USA

Canada

USA Japan

USA Canada

Arendt et al [8]

Benazzo et al [25]

Bennell et al [1]

Brukner et al [24] Courtenay and Bowers [20] Goldberg and Pecora [9] Ha et al [23] Hulkko et al [28]

Iwamoto and Takeda [12] Johnson et al [2]

Matheson et al [13]

Nattiv et al [3]a Ohta-Fukushima et al [21]

Sullivan et al [27] Taunton et al [30]

Running Running

T-F All

All

All NCAA

All All NCAA All All

T-F

T-F

NCAA

Sport

57 62

33/37 222

145/175

125/71 12/22

102/78 108 26/32 169 217/97

12/14

22/23

28/43

Number (M/F)

XR/BS XR/BS

XR/MRI XR/BS

BS/XR

XR/MR/BS XR/BS

CT/BS/XR XR/BS BS/XR BS/XR XR/BS

BS/CT

CT/BS/XR

MRI/BS/XR

Diagnosis M F M F M F — — — — M F — M F M F — M F — —

Gender 28.6 41.9 33.3 28 41.7 50 20.6 38 19 32 64.1 44.3 44.4 33.3 41 46.2 51.4 45 21.1 47.2 43.9 54

Tib 10.7 10.3 12.5 12 25 0 16.7 29.6 12.1 10.7 18.4 4.1 4.6 0 0 5.5 7.4 12.1 3.5 7.4 21.1 11

Fib 35.7 16.5 12.5 16 0 14.3 23.3 18.5 25.9 7.2 20.7 28.9 11.2 25 18.2 6.9 10.3 24.2 29.8 26.9 14 16

MT

Anatomic site (%)

17.9 18.6 29.2 28 25 7.1 14.4 4.6 NR 4.7 2.8 3.1 NR 0 18.2 NR NR NR NR NR 0 3

Nav 0 2.3 8.3 12 8.3 0 5.6 0.9 3.4b 1.2 0.9 0 NR 0 0 32.4b 19.4b NR 1.8b 3.7b 7 8

Tars 7.8 11.6 0 0 0 14.3 3.3 2.8 10.3 12.4 8.3 5.2 NR 33.3 18.2 6.9 7.4 12.1 7 0 3.5 6

Fem

NR NR 0 0 0 7.1 1.7 0.9 3.4 4.1 0.9 5.2 6.6 0 0 0 1.7 NR 1.8 2.8 10.5 NR

Pelvis

NR NR 0 4 0 0 1.1 0 3.4 1.8 3.7 7.2 3.6 0 0 1.4 1.7 NR 0.9 0 0 NR

Ses

Abbreviations: BS, bone scan; F, female; Fem, femur; Fib, fibula; M, male; MT, metatarsal; Nav, Navicular; NCAA, National Collegiate Athletic Association; NR, not recorded; Ses, sesamoid; Tars, tarsal; T-F, track and field; Tib, tibia; XR, radiography. a Did not separately report tarsal navicular injuries. b Published as abstract only.

Country

Study

Table 4 Stress fracture distribution by most frequent anatomic sites

EPIDEMIOLOGY OF STRESS FRACTURES 47

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SNYDER, KOESTER, DUNN

encountered more commonly in track and field athletes. The overall frequency could not be ascertained because several studies did not differentiate navicular fractures from other tarsal bone fractures. Few conclusions can be drawn from analyzing specific fracture sites by sport, given the small number of reported injuries (Table 5). In a prospective study of elite Australian track and field athletes, Bennell and colleagues [1] did report a Table 5 Stress fracture occurrence according to sport and bone (by percentage) Sport Basketball Arendt et al [8] Brukner et al [24] Hickey et al [32]a Iwamoto and Takeda [12] Distance Running Arendt et al [8]

Number Gender Tib

Fib

MT

Nav

Tars

Fem

Pelvis Ses

0 0 0

100c 0 25

0 0 25

0 0 0

0 0 0

NR NR 0

0 0 0

4 5 4

M F —

0 100 25

20

F

40

20

15

10

5

5

NR

NR

44

—

63.6

NR

18.2

NR

NR

NR

0

9.1

7 16 10 6 35

M F M F —

14.3 43.8 40 33.3 42.9

0 0 20 33.3 22.9

28.6c 18.8c 20 16.7 14.3

28.6 18.8 20 0 2.9

0 0 0 16.7 5.7

28.6 18.8 0 0 5.7

NR NR 0 0 2.9

0 0 0 0 0

—

61.8b NR

27c

0

1

6.9

2.5

NR

—

43.9

21

29.6

0

7

3.5

10.5 0

—

54

11

16

3

8

6

NR

NR

M F M F —

50 11.1 28.6 26.3 25.9

0 0 7.1 5.2 9.3

50c 33.3c 17.1 15.8 16.7

0 44.4 35.7 36.8 35.2

0 0 14.3 10.5 3.7

0 11.1 0 0 1.9

0 0 0 0 1.9

0 0 0 5.2 1.9

—

71.8b NR

25.6c 2.6

0

0

0

NR

F —

25 36.4

25 9.1

0 NR

0 NR

0 0 18.2 9.1

Benazzo et al [25] Brukner et al [24] Hulkko et al 204 [28] Sullivan et al 57 [27] Taunton et al 62 [30] Track Arendt et al [8] 4 9 Benazzo et al 14 [25] 19 Brukner et al 54 [24] Hulkko et al 39 [28] Soccer Arendt et al [8] 4 Iwamoto and 11 Takeda [12]

50 NR

0 NR

Abbreviations: F, female; Fem, femur; Fib, fibula; M, male; MT, metatarsal; Nav, Navicular; NR, not recorded; Ses, sesamoid; Tars, tarsal; Tib, tibia. a Method of diagnosis not described. b Listed only as “lower leg” and includes tibia and fibula. c Listed as “forefoot” and includes sesamoids of great toe and phalanges.

EPIDEMIOLOGY OF STRESS FRACTURES

49

statistically significant (P ≤ .01) association between specific events and the fracture site. Distance runners were more likely to suffer a long bone (tibia, femur, and fibula) or pelvic stress fracture, whereas foot fractures occurred more frequently in jumpers, sprinters, hurdlers, and multi-event athletes [1]. Although the number of total participants was not given, the findings by Benazzo and colleagues [25] also suggest an association between the “power” running events (jumping and sprinting) in track and the occurrence of tarsal navicular stress fractures. Overall, fractures of the upper extremities were found to be relatively rare, although most studies focused only on lower-extremity injuries. The ulna was the upper-extremity bone injured most frequently. Because many of the reviewed studies focused on track and field athletes in general and runners in particular, the overall frequency of upper extremity stress fractures could not be discerned. Stress fractures of the axial skeleton also were relatively infrequent, consisting mainly of injuries to the ribs, pars interarticularis, and pelvis. Rib stress fractures were associated with rowing, whereas the majority of athletes with ulnar stress fractures played baseball [12,21]. Dixon and Fricker [26] have found that 45% of all stress fractures in the female gymnasts involved the pars. MORBIDITY AND OUTCOMES The available literature offers few data in regard to outcomes and recurrence rates following a stress fracture. Sullivan and colleagues [27] have reported that seven of 51 athletes who had a stress fracture had suffered a radiologically proven fracture before study enrollment. Bennell and colleagues [1] have found that 60% of athletes with a stress fracture over their prospective 12-month observation period had experienced a previous stress fracture. There was a strong recruitment bias in this sample because nearly 40% of all athletes who volunteered to participate in the study had a history of at least one previous stress fracture [1]. Several studies provided varying details regarding concurrent and subsequent stress fractures. Six studies reported more than one stress fracture occurring in 4% to 11% of athletes [1,8,21,23,25,27]. None of the authors commented on whether concurrent fractures were symptomatic or diagnosed only through imaging. Courtenay and colleagues [20] found bilateral stress fractures in 16 athletes (7 tibias, 7 fibulas, and 2 metatarsals), whereas Ha and colleagues [23] reported 7 bilateral stress fractures of the tibia and 2 bilateral fibular stress fractures. Only Sullivan and colleagues [27] reported a reoccurrence of a fracture at the same site as a previous fracture (fibula). Hulkko and Orava [28] found that 9% of total fractures occurred in athletes with a previous fracture, reported during their study period, whereas Bennell and colleagues [1] and Ha and colleagues [23] found rates of 7% and 3%, respectively. The time period from diagnosis to return to full sports participation varied greatly when reported. Johnson and colleagues [2] found a range of 8 to 17 weeks to return to full activity in eight collegiate athletes with femoral stress fractures. Two studies reported cumulative data regarding the timing of return to sports

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Table 6 Time elapsed from treatment to full recovery Study

Tib

Fib

MT

Nav

Tars

Fem

Benazzo et al [25] Johnson et al [2] Matheson et al [13] Taunton et al [30]

4.8 mo NR 11.7 wk 4.5 wk

NR NR 7.7 wk 2.4 wk

NR NR 7.9 wk 3.5 wk

5.96 mo NR NR NR

NR NR 17.3 wk 10 wk

NR 10.8 wk 7.5 wk 3.5 wk

Abbreviations: Fem, femur; Fib, fibula; MT, metatarsal; Nav, Navicular; NR, not recorded; Ses, sesamoid; Tars, tarsal; Tib, tibia.

[21,23]. Athletes returned to play at 1.5 months in the series by Ha and colleagues [23], whereas Ohta-Fukushima and colleagues reported that 65% of cases were healed within 12 weeks. Matheson and colleagues [29] and Taunton and colleagues [30] both reported resumption of activity by injury site (Table 6). Matheson and colleagues [29] found an average time to recovery of 12.8 weeks (range, 2–96 weeks) for all fractures, whereas Taunton and colleagues reported a mean time of only 4.8 weeks to “full recovery” [29,30]. Benazzo and colleagues [25] reported a return to activity time far in excess of other studies, likely because of their requirements for study subjects to be asymptomatic and have radiographic evidence of complete fracture healing. Overall, the published data on time missed because of injury have limited clinical application because of the differences in sports, symptoms at the time of presentation, methods of diagnosis, severity of injuries, and return to competition criteria. Arendt and colleagues [8] have classified stress fractures into four grades based on MRI findings. They found significant differences in time elapsed from diagnosis to return to play, depending on fracture grade [8]. The mean time to resumed play for all athletes was 8.4 weeks; however, recovery time varied from an average of 3.3 weeks for grade 1 injuries to 14.3 weeks for grade 4 injuries [8]. They also found that 20 of 22 foot stress fractures were grade 3 or 4 at the time of diagnosis, suggesting a possible delay in diagnosis [8]. A longer duration of symptoms before diagnosis of tarsal stress fractures was also reported in two additional studies [29,30]. The evidence conflicts as to whether a delay in diagnosis adversely affects recovery time [21,29,30].

Table 7 Fractures requiring surgical fixation Study

Surgery/total SF (%)

Tib

Fib

MT

Nav

Tars

Fem

Ses

Ulna

Benazzo et al [25] Ha et al [23] Hulkko et al [28] Ohta et al [21]

2/49 (4.1) 11/169 (6.5) 26/314 (8.3) 4/222 (1.8)

1 0 7 1

0 0 0 0

0 0 4 0

0 5 3 0

1 0 1 0

0 4 3 0

0 1 4 0

0 1 3 3

Abbreviations: Fem, femur; Fib, fibula; MT, metatarsal; Nav, Navicular; Ses, sesamoid; SF, surgical fixation; Tars, tarsal; Tib, tibia.

EPIDEMIOLOGY OF STRESS FRACTURES

51

Several stress fractures have been described as “high risk” for delayed union or progression to nonunion [31,32]. Although the cumulative data clearly indicate that the majority of stress fractures heal with conservative treatment, 43 patients were reported to have required surgical fixation (Table 7). In this review, tarsal navicular and tibial fractures were the most ominous injuries encountered, because nearly 40% (17/43) of surgeries were performed for fixation of these two types of fractures. Tibial stress fractures were not classified by anterior or posterior location. The only three career-ending injuries documented resulted from navicular stress fractures. The available evidence suggests that early diagnosis of a tarsal navicular stress fracture requires a high index of suspicion. Navicular stress injuries should not go unheeded, because this type of injury may portend a worse outcome than other stress fractures. Future research is needed to explore preventative strategies of these potentially devastating injuries. SUMMARY The pathophysiology of stress fractures is well understood, but a lack of quality epidemiologic data remains. Injuries to the tibia and metatarsals are the most frequent stress fractures reported in the literature. There is a clear association between increasing training volumes and increased risk of stress fracture, but little is known beyond this association. There is a pressing need for large prospective studies to better establish the risks of stress fracture by sport, age, and gender. Such studies would allow a better delineation of specific fracture sites and estimates of injury risk and lay the foundation for future prevention strategies. References [1] Bennell KL, Malcolm SA, Thomas SA, et al. The incidence and distribution of stress fractures in competitive track and field athletes: a twelve-month prospective study. Am J Sports Med 1996;24(2):211–7. [2] Johnson AW, Weiss Jr CB, Wheeler DL. Stress fractures of the femoral shaft in athletes– more common than expected: a new clinical test. Am J Sports Med 1994;22(2):248–56. [3] Nattiv A, Puffer JC, Casper J, et al. Stress fracture risk factors, incidence, and distribution: a 3 year prospective study in collegiate runners. Med Sci Sports Exerc 2000;32(Suppl 5):S347. [4] Finch CF. An overview of some definitional issues for sports injury surveillance. Sports Med 1997;24(3):157–63. [5] Gordis L. Epidemiology. Measuring the occurrence of a disease. 2nd edition. Philadelphia: WB Saunders; 2000. p. 31–62. [6] de Loes M. Exposure data: why are they needed? Sports Med 1997;24(3):172–5. [7] Lloyd T, Triantafyllou SJ, Baker ER, et al. Women athletes with menstrual irregularity have increased musculoskeletal injuries. Med Sci Sports Exerc 1986;18(4):374–9. [8] Arendt E, Agel J, Heikes C, et al. Stress injuries to bone in college athletes: a retrospective review of experience at a single institution. Am J Sports Med 2003;31(6):959–68. [9] Goldberg B, Pecora C. Stress fractures: a risk of increased training in freshmen. Phys Sportsmed 1994;22(3):68–78. [10] Hame SL, LaFemina JM, McAllister DR, et al. Fractures in the collegiate athlete. Am J Sports Med 2004;32(2):446–51. [11] Clement DB, Taunton JE, Smart GW, et al. A survey of overuse running injuries. Phys Sportsmed 1981;9(5):47–58.

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[12] Iwamoto J, Takeda T. Stress fractures in athletes: review of 196 cases. J Orthop Sci 2003; 8(3):273–8. [13] Matheson GO, MacIntyre JG, Taunton JE, et al. Musculoskeletal injuries associated with physical activity in older adults. Med Sci Sports Exerc 1989;21(4):379–85. [14] Witman P, Melvin M, Nicholas JA. Common problems seen in a metropolitan sports injury clinic. Phys Sportsmed 1981;9(3):105–8. [15] Brubaker CE, James SL. Injuries to runners. J Sports Med 1974;2(4):189–98. [16] James SL, Bates BT, Osternig LR. Injuries to runners. Am J Sports Med 1978;6(2):40–50. [17] Brudvig TJ, Gudger TD, Obermeyer L. Stress fractures in 295 trainees: a one-year study of incidence as related to age, sex, and race. Mil Med 1983;148(8):666–7. [18] Gardner Jr LI, Dziados JE, Jones BH, et al. Prevention of lower extremity stress fractures: a controlled trial of a shock absorbent insole. Am J Public Health 1988;78(12):1563–7. [19] Milgrom C, Finestone A, Shlamkovitch N, et al. Youth is a risk factor for stress fracture: a study of 783 infantry recruits. J Bone Joint Surg Br 1994;76B(1):20–2. [20] Courtenay BG, Bowers DM. Stress fractures: clinical features and investigation. Med J Aust 1990;153(3):155–6. [21] Ohta-Fukushima M, Mutoh Y, Takasugi S, et al. Characteristics of stress fractures in young athletes under 20 years. J Sports Med Phys Fitness 2002;42(2):198–206. [22] Barrow GW, Saha S. Menstrual irregularity and stress fractures in collegiate female distance runners. Am J Sports Med 1988;16(3):209–16. [23] Ha KI, Hahn SH, Chung MY, Yang BK, Yi SR. A clinical study of stress fractures in sports activities. Orthopedics 1991;14(10):1089–95. [24] Brukner P, Bradshaw C, Khan KM, et al. Stress fractures: a review of 180 cases. Clin J Sport Med 1996;6(2):85–9. [25] Benazzo F, Barnabei G, Ferrario A, et al. Le fratture da durata in atletica leggera [Stress fractures in track and field athlectics]. I J Sports Traumatol Rel Res 1992;14(1):51–65. [26] Dixon M, Fricker P. Injuries to elite gymnasts over 10 yr. Med Sci Sports Exerc 1993; 25(12):1322–9. [27] Sullivan D, Warren RF, Pavlov H, et al. Stress fractures in 51 runners. Clin Orthop 1984; 187:188–92. [28] Hulkko A, Orava S. Stress fractures in athletes. Int J Sports Med 1987;8(3):221–6. [29] Matheson GO, Clement DB, McKenzie DC, et al. Stress fractures in athletes: a study of 320 cases. Am J Sports Med 1987;15(1):46–58. [30] Taunton JE, Clement DB, Webber D. Lower extremity stress fractures in athletes. Phys Sportsmed 1981;9(1):77–86. [31] Kaeding CC, Spindler KP, Amendola A. Management of troublesome stress fractures. Instr Course Lect 2004;53:455–69. [32] Hickey GJ, Fricker PA, McDonald WA. Injuries of young elite female basketball players over a six-year period. Clin J Sport Med 1997;7(4):252–6.

Clin Sports Med 25 (2006) 53–62

CLINICS IN SPORTS MEDICINE Imaging of Stress Fractures Carolyn M. Sof ka, MD Department of Radiology and Imaging, Hospital for Special Surgery, 535 East 70th Street, New York, NY 10021, USA

S

tress injuries are a common cause of pain and morbidity in both professional and recreational athletes. The early diagnosis of such injuries is imperative to halt the progression of disease, which may result in a complete fracture. Stress fractures occur when unusual stresses are applied to normal bones that have not remodeled themselves enough to handle increased stress. This condition usually occurs in the setting of newly undertaken, vigorous athletic activity to which the patient—and the skeleton—has not accommodated. Clinically, the diagnosis of stress injuries may be difficult because the condition may mimic other musculoskeletal complaints such as tendon or muscle injuries, and therefore, imaging of these injuries is central to obtaining a rapid diagnosis. Conventional radiographs are the mainstay of imaging patients with musculoskeletal complaints; however, radiographic findings can sometimes lag behind the clinical presentation and therefore may compound a delay in diagnosis. Advanced cross-sectional imaging techniques, including MRI, CT, ultrasonography, and nuclear scintigraphy, can confirm the diagnosis of stress injuries earlier and, therefore, contribute to initiating appropriate treatment sooner. CONVENTIONAL RADIOGRAPHS The conventional radiographic diagnosis of stress injuries or stress fractures relies on the ability of the bone to remodel from the insult. High-resolution radiographs are important for diagnosing subtle osseous changes, especially in the small bones of the feet. Early radiographic changes of a stress fracture in the long bones can include the visualization of a faint fracture radiolucency in the cortical bone, although this can be subtle [1]. As the bone remodels in response to the insult and repetitive stress, the endosteum can become ill defined, thickened, and sclerotic (Fig. 1). As the fracture heals and remodels, periosteal reaction follows both on

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SOFKA

Fig. 1. (A) Lateral view radiograph of the proximal calf demonstrating endosteal remodeling and cortical thickening (arrow) consistent with a stress fracture. A faint radiolucent fracture plane is present. (B) Sagittal high-resolution fast spin echo MRI of the leg in the same patient demonstrating moderate cortical thickening and a faint cortical fracture line (arrow).

the cortical as well as involving the endosteal surface [1]. Periosteal new bone formation can be seen approximately 10 days after the initial injury pattern commences. Stress fractures in cancellous bone (eg, the calcaneus) usually follow a predictable pattern, following the band of stress, with a linear band of sclerosis appearing perpendicular to the trabeculae (Fig. 2) [1]. Stress fractures can occur anywhere in the skeleton, and stress fractures in certain bones are associated with various activities. For example, stress fractures of the metatarsals and tarsal bones are often associated with running or marching; fractures of the sacrum with running; fractures of the pelvis with bowling or gymnastics; fractures of the lumbar spine with ballet, running, and gymnastics; and fractures of the humerus and ulnar shafts with baseball [1–6]. The repetitive throwing athlete can sustain fractures of the upper extremity in both the distal humerus as well as the proximal forearm. Fractures of the distal humerus are often seen in pitchers, and proper development and conditioning of the biceps and triceps muscles have been advocated to prevent stresses on the humerus from the torsional loading that is often sustained during such activities [7]. Stress fractures of the posteromedial olecranon occur from repetitive valgus stress, which is often encountered in the throwing athlete; interestingly, these patients often have competent ulnar collateral ligaments [8]. Last, stress fractures of the ribs have been seen in pitching as well as in golfing [9,10]. The radiographic diagnosis of stress fractures occasionally may be difficult. Radiographic findings can lag behind the clinical symptoms, often yielding subtle or no obvious signs (Fig. 3). In situations in which the clinical suspicion

IMAGING OF STRESS FRACTURES

55

Fig. 2. (A) Sagittal fast inversion recovery MRI of the ankle demonstrating bone marrow edema pattern in the calcaneus. (B) Coronal fast spin echo MRI in the same patient demonstrating an incomplete insufficiency fracture line through the inferomedial margin of the calcaneus (arrow). (C) Axial fast spin echo MRI of the same patient demonstrating the incomplete hypointense fracture line (arrow) seen medially.

is high but the radiographic findings are noncontributory, further imaging with MRI or nuclear scintigraphy is suggested to evaluate for bone marrow edema and remodeling (see Fig. 3). Stress fractures in the long bones can occasionally be confused with other pathologies such as an osteoid osteoma; however, the clinical presentation often will suggest a stress fracture. In addition,

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SOFKA

Fig. 3. (A) Anteroposterior radiograph of the foot in a patient who had second toe pain, demonstrating no focal abnormality in the second toe. (B) Coronal fast inversion recovery MRI of the foot in the same patient demonstrates an intraosseous bone marrow edema pattern in the second metatarsal and surrounding soft tissue hyperintensity consistent with stress reaction. (C) Coronal fast spin echo proton density MRI in the same patient demonstrates mild cortical thickening (arrow) and endosteal remodeling consistent with stress reaction. No definite cortical break is seen.

high-resolution, thin-slice CT or MRI can demonstrate a nidus in the setting of an osteoid osteoma. The evaluation of a clinically suspected osseous stress injury should begin with conventional radiographic evaluation; with problematic or inconclusive cases directed to one of the advanced imaging modalities.

IMAGING OF STRESS FRACTURES

57

CT CT can demonstrate the regional osseous anatomy in multiple orthogonal planes. Visualizing the long bones in cross-section can increase the sensitivity of detecting subtle periosteal reaction or endosteal changes. One particularly useful application of CT is for the evaluation of stress injuries of the spine (pars interarticularis stress fractures), which often can be radiographically occult. Additionally, CT is useful in distinguishing between an osteoid osteoma and a stress fracture. Thin-cut CT scanning can demonstrate the central radiolucent nidus in the setting of an osteoid osteoma or a linear fracture line in the case of stress fractures. Although CT can clearly demonstrate osseous changes such as the periosteal reaction, endosteal remodeling, or a frank fracture line, this imaging modality is limited in demonstrating the activity of the lesion. A quiescent or chronic stress reaction may appear similar to a more active lesion on CT because the status of bone turnover, as demonstrated by “activity” on a nuclear medicine bone scan or bone marrow edema pattern on MRI , cannot be determined. Nevertheless, CT should be considered in patients in whom a stress reaction is the clinical concern, especially in the axial skeleton, and in whom MRI is not an option, because of either a relative or an absolute contraindication. ULTRASONOGRAPHY The use of ultrasonography in evaluating the musculoskeletal system is increasing in frequency. The superficial margins of cortical bone can be evaluated with ultrasonography, in which the cortex appears linear and echogenic (or bright). Given the acoustic impedance properties of cortical bone, the deeper margins of bone are not able to be visualized, resulting from the posterior acoustic shadowing from the more superficial layer of bone (Fig. 4). Because ultrasonography can be used to evaluate the superficial cortices of bone, it can be used to diagnose stress reactions or stress fractures in the more

Fig. 4. Longitudinal ultrasonographic image of the second metatarsal in a patient who had second toe pain and negative radiographs. Focal buckling of the dorsal cortical surface of the metatarsal is seen just proximal to the neck, with hypoechoic callus formation (arrow) consistent with a stress fracture. Mild power Doppler activity is present, consistent with inflammation.

58

SOFKA

superficial structures such as the feet and the calves (distal tibia). Ultrasonography can demonstrate focal buckling in the bone cortex as well as a surrounding hypoechoic callus (see Fig. 4). In addition, power Doppler ultrasonography can be applied, providing a semiquantitative evaluation of bone turnover activity, suggesting acuity. NUCLEAR MEDICINE Nuclear medicine scintigraphy is sensitive for diagnosing early stress remodeling and stress fractures. A radioactive tracer targeted for bone is injected intravenously and then, after the tracer is allowed to localize to areas of bone remodeling, the patient undergoes imaging. In the setting of stress fractures or stress reaction, areas of increased radiotracer activity correlate with areas of bone remodeling, trabecular microfractures, and periosteal reaction or callus formation [11]. Although nuclear medicine scintigraphy is quite sensitive for the evaluation of bone turnover and therefore can detect very early development of stress reactions or stress fractures, this method is not specific for fractures. The morphology of the bone and surrounding tissues cannot be evaluated. Any area of bone turnover can result in areas of increased radiotracer uptake, such as tumors, infection, inflammation, or trauma. Given this limitation, nuclear medicine examinations must be interpreted with close correlation of conventional radiographs as well as the patient's clinical history. MRI MRI, like nuclear medicine, is sensitive to detecting early marrow changes and early stress reactions. MRI also provides a detailed anatomic evaluation of the regional soft tissues and can be used to quantify the quality of the endosteal and cortical bone. MRI can be used to evaluate both the appendicular as well as the axial skeleton. MRI provides a comprehensive evaluation of the area in question, providing morphologic as well as functional information. MRI can demonstrate the status of the intramedullary bone, areas of bone edema or turnover, periosteal reaction, and frank fracture lines (Figs. 5 and 6). The addition of at least one water-sensitive pulse sequence (fat suppression or inversion recovery) should be included in all MRI examinations to evaluate for bone marrow edema (see Figs. 2, 3, 5, and 6). Endosteal marrow edema is one of the earliest signs of stress remodeling and can be seen with MRI [12]. The cross-sectional imaging capabilities and the ability to diagnose subtle marrow changes of MRI can help identify osseous abnormalities in areas not readily visualized with conventional radiography, such as the sacrum and pelvis. Specifically, stress fractures of the sacrum, which often are encountered when a long-distance runner changes the level of activity, can be difficult to discern on routine plain film radiographs. The importance of diagnosing stress fractures of the sacrum is that they can potentially mimic intervertebral disc pathology, which dictates a different course of clinical management [13]. A single large-field-

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Fig. 5. (A) Sagittal fast inversion recovery MRI of the lateral margin of the ankle demonstrating a striking bone marrow edema pattern in the fibula with periosteal reaction consistent with a stress fracture. (B) Sagittal fast spin echo MRI in the same patient demonstrates mild ill-defined endosteum and periosteal new bone formation (arrow ).

of-view water-sensitive pulse sequence can be used to provide a global overview of the lower lumbar spine, pelvis, and hips in patients presenting with nonspecific hip, lower- back, or groin pain, and in those in whom a stress fracture is a clinical concern. This “survey image” of the pelvis is especially useful to evaluate patients who have nonlocalizing clinical symptoms. Another important application of MRI is in diagnosing femoral neck stress fractures. Femoral neck stress fractures can present with symptoms of pain in the groin, hip, or anterior thigh, often mimicking other potential sources of pain such as a labral tear or iliopsoas tendon pathology [14]. Radiographic findings can lag behind clinical symptoms by a period of weeks to months, thus potentially resulting in a delayed diagnosis and completion of the fracture [15]. In addition, if the patient is moderately to severely osteoporotic, the diagnosis of an early, nondisplaced femoral neck fracture on routine anteroposterior and lateral radiographs can be limited. The advantage of MRI in contrast to nuclear medicine scintigraphy is that it can identify bone marrow edema and also can demonstrate the location of the fracture, classifying the fracture as a compression (on the inferior aspect of the neck) or a tension (on the superior aspect of the neck) type, of which the latter is considered to be more unstable [16]. Because MRI is sensitive for diagnosing bone marrow edema, the imaging findings should be interpreted in conjunction with the patient's symptoms. The presence of bone marrow edema can remain long after the initial diagnosis and treatment of a fracture, whereas the cortical bone matures and remodels. It has been demonstrated that the bone marrow edema pattern on MRI may be present for up to approximately 6 months after an initial diagnosis of a femoral neck

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Fig. 6. (A) Sagittal fast inversion recovery MRI of the knee demonstrating bone marrow edema pattern concentrated in the proximal posterior margin of the tibia, where there is a frank fracture line posteriorly and periosteal reaction. Sagittal (B) and coronal (C ) fast spin echo MRIs in the same patient demonstrate the morphology and detailed anatomy of the area to better advantage; the fracture line and periosteal new bone formation are evident (B and C, arrows).

fracture [17]. In addition, asymptomatic bone marrow edema patterns or stress reactions may be present in relatively asymptomatic subjects, such as marathon runners, who are exposed to osseous stresses. The clinical relevance of this finding has been debated. In one study of asymptomatic runners, tibial stress reactions were noted in the mid diaphysis of the tibiae; of note, these areas of activity did not correlate with the incidence of future frank stress fractures [18]. Similarly, bone marrow edema has been demonstrated in the bones of the feet

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and ankle in runners [19]. The activity of the intramedullary bone as well as the morphology of the bones (endosteal remodeling and cortical thickening) should thus be evaluated in conjunction with the patient’s presenting clinical symptoms. In summary, MRI can provide detailed information regarding the presence of a stress fracture or stress reaction, especially in cases in which the radiographic findings are inconclusive. MRI can provide information regarding the acuity of the abnormality as well as morphologic information about the bone, including periosteal new bone formation, endosteal remodeling, as well as subtle frank cortical fracture lines. SUMMARY The imaging evaluation of a patient in whom a stress reaction or fracture is clinically suspected should begin with high-resolution radiographs of the area in question. In inconclusive or indeterminate cases, additional imaging should be obtained. CT provides exquisitely fine osseous detail, in multiple planes, often demonstrating the endosteal remodeling or fracture line that is not apparent on conventional radiographs. The sensitivity of nuclear scintigraphy depicts areas of even subtle osseous turnover and stress remodeling. Ultrasonography, which is being used increasingly in the evaluation of the musculoskeletal system, can provide a limited evaluation of the superficial osseous structures, providing an imaging alternative, especially in those patients who are MRI -incompatible. MRI, however, provides the most comprehensive evaluation of stress injuries, revealing both functional as well as morphologic information about the bone. References [1] Daffner RH, Pavlov H. Stress fractures: current concepts. AJR Am J Roentgenol 1992;159: 245–52. [2] Pavlov H, Torg JS, Freiberger RH. Tarsal navicular stress fractures: radiographic evaluation. Radiology 1983;148:641–5. [3] Matheson GO, Clement DB, McKenzie DC, et al. Stress fractures in athletes: a study of 320 cases. Am J Sports Med 1987;15:46–58. [4] Czarnecki DJ, Till EW, Minikel JL. Unique sacral stress fracture in a runner [letter]. AJR Am J Roentgenol 1988;151:1255. [5] Schneider HJ, King AY, Bronson JL, et al. Stress injury and developmental change of the lower extremities in ballet dancers. Radiology 1974;113:627–32. [6] Tanabe S, Nakahira J, Bando E, et al. Fatigue fracture of the ulna occurring in pitchers of fast-pitch softball. Am J Sports Med 1991;19:317–21. [7] Polu KR, Schenck Jr RC, Wirth MA, et al. Stress fracture of the humerus in a collegiate baseball pitcher: a case report. Am J Sports Med 1999;27(6):813–6. [8] Schickendantz MS, Ho CP, Koh J. Stress injury of the proximal ulna in professional baseball players. Am J Sports Med 2002;30(5):737–41. [9] Lord MJ, Ha KI, Song KS. Stress fractures of the ribs in golfers. Am J Sports Med 1996; 24(1):118–22. [10] Gurtler R, Pavlov H, Torg JS. Stress fracture of the ipsilateral first rib in a pitcher. Am J Sports Med 1985;13(4):277–9. [11] Nussbaum AR, Treves ST, Micheli L. Bone stress lesions in ballet dancers: scintigraphic assessment. AJR Am J Roentgenol 1988;150:851–5. [12] Kiuru MJ, Niva M, Reponen A, et al. Bone stress injuries in asymptomatic elite recruits: a clinical and magnetic resonance imaging study. Am J Sports Med 2005;33(2):272–6.

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[13] Major NM, Helms CA. Sacral stress fractures in long distance runners. AJR Am J Roentgenol 2000;174:727–9. [14] Provencher MT, Baldwin AJ, Gorman JD, et al. Atypical tensile-sided femoral neck stress fractures: the value of magnetic resonance imaging. Am J Sports Med 2004;32(6): 1528–34. [15] Shin AY, Morin WD, Gorman JD, et al. The superiority of magnetic resonance imaging in differentiating the cause of hip pain in endurance athletes. Am J Sports Med 1996;24: 168–76. [16] Devas MB. Stress fractures of the femoral neck. J Bone Joint Surg Br 1965;47B:728–38. [17] Slocum KA, Gorman JD, Puckett ML, et al. Resolution of abnormal MR signal intensity in patients with stress fractures of the femoral neck. AJR Am J Roentgenol 1997;168:1295–9. [18] Bergman AG, Fredericson M, Ho C, et al. Asymptomatic tibial stress reactions: MRI detection and clinical follow-up in distance runners. AJR Am J Roentgenol 2004;183:635–8. [19] Lazzarini KM, Troiano RN, Smith RC. Can running cause the appearance of marrow edema on MR images of the foot and ankle? Radiology 1997;202:540–2.

Clin Sports Med 25 (2006) 63–73

CLINICS IN SPORTS MEDICINE Pharmacologic Agents in Fracture Healing Michael C. Koester, MD, ATC*, Kurt P. Spindler, MD Vanderbilt Sports Medicine, Medical Center East, South Tower, Suite 3200, Nashville, TN 37232, USA

B

one fractures are a known risk of athletic participation. Hame and colleagues [1] found a fracture incidence of 5.9% in collegiate athletes over a 15-year observation period. Stress fractures represented nearly 25% of all of the reported fractures. Although much less common than soft tissue injuries, fractures typically result in significant time lost from activity. Recovery is time-dependent and interrupts participation, unless the fracture can be protected properly. In certain circumstances, surgical fixation may allow a quicker return to activity, but the healing process usually cannot be accelerated. Pharmacologic interventions to enhance fracture healing have been the subject of animal studies for years, yet few trials involving humans have been conducted. This article discusses the current understanding of the potential role for bisphosphonates, parathyroid hormone (PTH), and vitamin D supplementation in the treatment of sports-related fractures. The available evidence regarding nonsteroidal anti-inflammatory drugs (NSAIDs) and their effects on fracture healing are also reviewed. Discussion focuses on the applicability of these findings to the sports medicine population; the potential role of pharmacologic agents for implant fixation and osteoporosis treatment are not discussed.

BISPHOSPHONATES Over the past decade, bisphosphonates have been widely used to treat a variety of bone diseases. The marked inhibitory action of bisphosphonates on osteoclast-mediated bone resorption has led to success in the treatment of pathologic processes with increased bone turnover such as Paget’s disease, bone tumors, and osteoporosis. More recently, investigators have speculated on whether bisphosphonates can play an important role in fracture repair by enhancing the healing process and limiting disuse osteoporosis. Two separate studies [2,3] have evaluated the effect of bisphosphonate therapy on fracture healing in osteoporotic women with distal radius fractures. Each study assessed bone mineral density at the fracture site as the primary outcome measure. Post-fracture bisphosphonate treatment increased bone mineral den* Corresponding author. E-mail address: [email protected] (M.C. Koester). 0278-5919/06/$ – see front matter doi:10.1016/j.csm.2005.08.004

© 2005 Elsevier Inc. All rights reserved. sportsmed.theclinics.com

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sity at the site of fracture, compared with placebo. However, the clinical significance of these findings was not established. Adolphson and colleagues [2] have reported no differences in pain and elapsed time until return to function between treatment groups, whereas van der Poest Clement and colleagues [3] have not attempted to assess patient-oriented outcomes. The clinical relevance of increased bone mineral density within a fracture callous is uncertain because neither morphologic appearance nor mineral content correlate with mechanical bone strength [4]. Calcium may be present in either cartilage or bone, thus the mechanical properties of the callus may vary greatly. In an animal model, Li and colleagues [5] have reported that bisphosphonate treatment resulted in a larger fracture callus, but the maturation of the fracture was delayed. These changes may be secondary to the inhibition of bone resorption, because bone formation and resorption are intimately linked. Given their inhibitory action on osteoclast activity, a potential role exists for the prophylactic use of bisphosphonates in stress fracture prevention. When placed under cyclic stress, microtrauma is inflicted on bone. The bone must then remodel while attempting to repair areas of microfracture. The first stage of bone remodeling involves bone resorption, further weakening the already compromised bone. In theory, if the initial turnover of bone is suppressed, it may not be transiently weakened as the normal healing process ensues [6]. Milgrom and colleagues [7] randomized a group of male Israeli military recruits to receive risedronate or placebo during the first 12 weeks of basic training. The primary outcome measure was the occurrence of a stress fracture during the study period. Over one third of the entire study group discontinued treatment because of concerns regarding potential adverse side effects, although only two soldiers actually reported symptoms. No patients were lost to followup. Intention-to-treat analysis and per-protocol analysis showed no difference in stress fracture incidence between the groups. Because of the large early dropout rate, the study was no longer adequately powered to detect a difference between the treatment groups, introducing the possibility of a type II statistical error. Further research is warranted regarding stress fracture prevention in both military and athletic populations. A case series [8] has recently detailed the successful use of intravenous pamidronate in five intercollegiate female athletes with tibia stress fractures. The five subjects showed bone scan results consistent with stress fracture, with four of the five athletes having symptoms more than 5 months before treatment. According to the report, only one athlete missed any time from activity, and the symptoms resolved in all five athletes within a few weeks of treatment. No decision regarding the efficacy of bisphosphonates in stress fracture treatment can be made from this uncontrolled study. The proper role of bisphosphonates in stress fracture treatment can be determined only by a well-designed clinical trial with fractures graded by MRI and groups randomized according to gender, fracture site, MRI findings, and activity. To date, bisphosphonates have been most widely used in post-menopausal women for the treatment of osteoporosis. However, the safety of bisphospho-

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nates has yet to be clearly established in women who are pregnant or of childbearing age. In rat studies, alendronate has been found to cross the placenta and accumulate in fetal bone [9]. Obviously, the presence of alendronate may interfere with fetal bone mineralization and development. Such changes have been reported in animal studies [9,10], but there have been no case reports of teratogenic effects in humans, to date. The half-life of the bisphosphonates is proportional to bone turnover time, which may be as long as 433 days in rats [11]. Therefore, it may take several years for a young woman to completely clear the drug from her body. Any harmful effects on the fetus could potentially persist for years after the initial treatment. Current studies of the use of bisphosphonates in young athletes should be limited to men. If it is found to be efficacious in the prevention or treatment of stress fractures, further studies in women, along with post-treatment surveillance for the occurrence of birth defects, should then be initiated. PARATHYROID HORMONE PTH plays a significant role in both intra- and extracellular calcium homeostasis [12]. Although the overall effect of PTH is to conserve calcium in the body, an anabolic effect on bone was discovered in 1932 [13]. Selye found that rats given a daily injection of PTH developed denser bones, but a large dose of the hormone resulted in bone resorption [13]. The availability of purified PTH in the 1970s led to a variety of animal studies assessing the role of PTH in fracture healing. The anabolic effect that PTH has on bone is not fully understood. The effect appears to be secondary to the activation of resting osteoblasts, resulting in an increased number of circulating cells [14]. Because this action appears to depend on the existing number of cells within the bone, PTH is less active in rats with severe osteopenia [15]. PTH also stimulates osteoprogenitor cells to become osteoblasts in rats [16], and it has been shown to postpone osteoblast apoptosis in mice [17]. The rat model has been used to conduct the majority of research into the effects of PTH on bone. However, there are many differences between rat and human bones that hinder the clinical application of these findings. In human bone, a larger portion of the organic matrix is composed of collagen. Human bone also demonstrates higher levels of haversian remodeling and better ordered cortical osteons [12]. Cancellous bone remodeling also occurs much faster in rats than in humans. Despite these limitations, Frost and Jee [18] found that the rat skeleton provides an appropriate model for evaluating the effects of therapeutic agents on bone mass, structure, strength, and composition. Animal studies as well as a few clinical trials involving humans have shown that the anabolic effects of PTH may be more pronounced in specific bones. Two studies have examined bone mass in osteoporotic women and showed a better response to PTH in the lumbar spine than in the proximal femur [19,20]. These findings are likely the result of the difference in marrow, because the lumbar spine consists of hematopoietic marrow with a greater number of osteo-

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progenitor cells and “resting” osteoblasts, whereas the femur consists of a less vascular, fatty marrow. Dempster and colleagues [21] have suggested that PTH may have a greater anabolic effect on cancellous bone than on cortical bone. Some animal studies suggest that the response to PTH may vary within regions of the same bone [22], with an increased effect in areas with a higher mechanical load [23]. More recent evidence suggests that the effects of PTH are even more pronounced in healing fractures, with evidence of increased callus formation and mechanical strength [24–27]. Two randomized clinical trials involving women with osteoporosis have found increases in bone mass density and a decrease in fracture risk [28,29]. In 2002, the US Food and Drug Administration approved teriparatide, a synthetic form of PTH, for the treatment of osteoporosis. Although it is likely that PTH will not promote the healing of fracture nonunions because of the need for viable osteoblasts, it may play a role in the treatment of other fractures by allowing an earlier return to competition. PTH could also potentially play a vital role in the treatment of slowly resolving stress fractures. VITAMIN D AND CALCIUM SUPPLEMENTATION Adequate dietary intake of vitamin D and calcium is essential to building and maintaining healthy bones. Animal studies have shown increased mechanical strength of the callous and other beneficial effects with vitamin D treatment after a fracture [30–32]. Given the few potentially harmful side effects, calcium and vitamin D supplementation have long been advocated in an effort to augment bone healing. In the only trial reported in the literature, Doetsch and colleagues [33] examined the role of vitamin D and calcium supplementation in treating osteoporotic women who had experienced an acute fracture of the proximal humerus. Thirty women (mean age 78 years) were randomized into treatment and placebo groups. The primary outcome measure was the difference in bone mass density at the fracture site between the two groups. There was a significant difference in callous formation 6 weeks after fracture in the treatment group, but this was not sustained at 12 weeks. No patient-oriented outcome measures (ie, pain, function, reoccurrence of fracture) were assessed. The clinical relevance of this study is questionable, even if applied to the study population, and it certainly cannot be generalized to other populations. NONSTEROIDAL ANTI-INFLAMMATORY DRUGS Primarily known as mediators of inflammation, prostaglandins also play an important role in bone metabolism and repair. Prostaglandins are derived from arachidonic acid in an enzymatic reaction catalyzed by cyclooxygenase (COX)-1 and COX-2. Previous convention held that COX-1 was constitutively produced and acted to maintain physiologic homeostasis (mainly gastrointestinal

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and renal function), whereas COX-2 acted as a stress response gene responsible for prostaglandin production at sites of inflammation. Thus, the development of the COX-2-specific inhibitors (coxibs) arose, with the intention of inhibiting the inflammatory process while avoiding the side effects of the nonspecific NSAIDs. The relative contributions of the COX-1 and COX-2 products to bone healing have been well studied. Fracture healing is a complex process, initially requiring the recruitment, proliferation, and differentiation of mesenchymal stem cells into chondrocytes and osteoblasts [34]. COX-2 has been found to be essential to bone repair through a series of experiments using mice genetically manipulated to produce no COX-2 isoenzymes [34]. Among other findings, the COX-2 deficient mice demonstrated significant impairment of healing 21 days post-fracture, characterized by the persistence of mesenchyme, reduced bone formation, and evidence of nonunion. These findings suggest that COX-2 may provide a regulatory effect on the maximal induction of osteogenesis. Although Zhang and colleagues [34] provide compelling evidence of the role of COX-2 in fracture healing, evidence of a significant in vivo effect of COX-2 inhibition has been inconsistent. Simon and colleagues [35] have reported impaired fracture healing in rats given valdecoxib and celecoxib, with increased rates of nonunion as well as radiographic, histologic, morphologic, and biomechanical evidence of delayed healing. However, other researchers [36,37] have reported normal fracture healing in animal models using COX-2 inhibitors. The effects of nonspecific NSAIDs have been studied extensively over the years, with the majority of research indicating a detrimental effect on fracture healing in animal models [38–42]. NSAIDs are among the most widely used pharmaceutical agents in the world. They are commonly administered for their analgesic and anti-inflammatory effects on a variety of musculoskeletal conditions. Because of basic science data and retrospective reports of delayed healing of fractures in humans, many sports medicine experts [43,44] now caution against the use of NSAIDs in athletes with a fracture. Although animal models may provide a starting point for clinical research, results of such investigations should not be extrapolated to humans. In addition, clinical decisions regarding patient care should not be based on low-level evidence from poorly conducted retrospective reviews, case reports, or expert opinion. The following discussion examines the best available evidence on which to base clinical decisions regarding NSAID use in fracture care. A systematic review of the literature regarding NSAID use and fracture healing in humans was performed by searching the MEDLINE database and the references of all retrieved articles. A total of nine relevant articles were reviewed (Table 1) [45–53]. Only two of the studies [45,52] were randomized clinical trials, with the remainder consisting of retrospective reviews. Three reports [45,47,52] have noted no effect on fracture healing in patients given NSAIDs. In a retrospective patient chart review, Burd and colleagues [48] have shown an increased rate of nonunion of long bone fractures in trauma patients

1993 2005

2003 2003

1998

2000 1998

2005

2005

Adolphson et al [45] Bhattacharyya et al [46]

Bhandari et al [47] Burd et al [48]

Deguchi et al [49]

Giannoudis et al [50] Glassman et al [51]

Reuben and Ekman [52]

Reuben et al [53]

Retrospective

Prospective RCT

Retrospective Retrospective

Retrospective

Observational Retrospective

Prospective RCT Retrospective

Study design

Fracture

Spinal arthrodesis

Spinal arthrodesis

ORIF femur Spinal arthrodesis

Spinal arthrodesis

ORIF tibia ORIF acetabulum

Distal radius Humeral shaft

Drugs

NSAIDs (patient recall) Ketorolac, 60 mg IV, 1 dose, then 30 mg every 6–8 h as needed Celecoxib, 400 mg, 1 dose before surgery, then 200 mg every 12 h for 5 d Given for 5 consecutive postoperative days: Celecoxib, 200–600 mg/d, Rofecoxib, 50 mg/d, Ketorolac, 20–110 mg/d, or Ketorolac 120–240 mg/d

NSAIDs (patient recall)

NSAIDs (patient recall) Indomethacin, 25 mg tid for 6 wk

Piroxicam, 20 mg/d for 8 wk NSAIDs (prescription records)

Outcome

OR of NU with high-dose ketorolac, 8.8 OR of NU with low-dose ketorolac, 3.0 No difference between placebo, celecoxib, rofecoxib

No difference between groups

No difference between groups Relative risk of nonunion with NSAID use 61–90 days after fracture, 3.9. No effect of NSAID on healing NSAID increased NU rate of long bone fractures of 26% versus 7% NSAID increased NU rate of 56% versus 22% OR of NU with NSAID use, 10.74 OR of NU with NSAID use, 4.9

Abbreviations: IV, intravenous; NU, nonunion; OR, odds ratio; ORIF, open reduction internal fixation; RCT, randomized clinical trial.

Year

Study

Table 1 Studies assessing the clinical effects of NSAID use on bone healing

68 KOESTER, SPINDLER

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receiving long-term indomethacin after acetabular fracture fixation. The patients were treated for a total of 6 weeks after surgery as prophylaxis against heterotopic ossification. Giounoudis and colleagues [50] and Deguchi and colleagues [49] each have reported a significant increase in nonunions, with postoperative NSAID use in femur fractures and spinal fusions, respectively. Each study was a retrospective review with NSAID use determined by patient report. The validity of selfreported medication use after a poor surgical outcome is a classic example of recall bias, and therefore, the conclusions are in doubt. [54]. Bhattacharyya and colleagues [46] used a Medicare database to track NSAID and opioid prescriptions given to a cohort of elderly patients who had humeral shaft fractures. They found that patients who developed nonunions were more likely to be those to whom NSAIDs and opioids were prescribed 61 to 90 days after fracture. The results strongly suggest that NSAID use in retrospective reviews likely reflect an increased use secondary to the pain of nonunion, rather than causation on the part of NSAIDs. Reuben and colleagues [52] randomized 80 patients undergoing spinal fusion to receive celecoxib or placebo perioperatively for 5 days. They found no significant difference in arthrodesis nonunion 1 year after surgery. In a separate retrospective chart review, Reuben and colleagues [53] examined the use of several NSAIDs and their effects on nonunion rates after spinal surgery. Rofecoxib and celecoxib had no detrimental effect on fusion success; however, patients given ketorolac had significantly higher rates of nonunion, with the risk of nonunion increased in the “high-dose” ketorolac group (see Table 1). The detrimental effect of ketorolac on spinal fusion success was also found by Glassman and colleagues [51] in a review of 288 patient charts. They noted a 5-fold increased risk for nonunion in patients who received ketorolac for postoperative pain. A significant association between the risk of nonunion and greater number of ketorolac doses received was also found. The external validity of the reviewed studies to a sports medicine population is limited. Of note, no effects on fracture healing were seen with the COX-2 inhibitors, a finding that contrasts with many published animal studies. In addition, spinal fusion is a complex procedure with multiple variables, comorbidities, and co-interventions, which may greatly affect healing. The studies that found an association between nonunion and NSAIDs use involved either high doses of ketorolac given over several days or long-term use of indomethacin. Neither of these medications is used routinely in such a manner, in clinical practice. Based on the current literature, no firm evidence-based recommendation can be made regarding the use of NSAIDs in fracture treatment. Theoretically, NSAIDs may delay fracture healing, and this effect could potentially be more detrimental when healing is already compromised or the bones vascular supply is tenuous (ie, tarsal navicular). However, the benefits of appropriate pain control must also be considered in the acute injury period. In terms of patientoriented outcomes, many patients may be willing to accept a potential 1-week

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delay in return to full function if it means adequate analgesia in the first several days. This same risk-benefit ratio may be unacceptable to a competitive athlete. Only future randomized clinical trials will answer these questions. Based on the available evidence, the use of oral NSAIDs at appropriate doses for early acute traumatic fracture care in athletes is not contraindicated. FUTURE DIRECTIONS Athletes may potentially benefit from pharmaceutical agents that prevent stress fractures or speed the healing process of acute and stress fractures. The value of such medications will depend on how quickly the athlete returns to competition in relation to the financial costs and possible negative side effects. As discussed, there is currently no clear evidence that any of the discussed agents either facilitate or impede human fracture healing. The recent discoveries of several bone-forming growth factors will ensure that research continues in this field. Bone morphogenic proteins, fibroblast growth factors, transforming growth factor-β, and other growth factors may eventually play a pivotal role in both fracture prevention and treatment. Interestingly, insulin-like growth factor (IGF)-I may interact significantly with PTH as a mediator of bone formation, in part by secreting IGF-I binding proteins in osteoblast-like cells [12]. The efficacy of any pharmaceutical agents will be determined only through large, randomized clinical trials. Although disease-oriented outcome measures such as bone mass density and callous size have been used in previous trials, future research must focus on patient-oriented outcomes such as time to return to full activity and decreased pain. The trials should consist of multicenter efforts, enrolling a large number of individuals participating in a variety of sports to allow for a representative number of different fractures. Without such highlevel evidence, any definitive comment on the positive or negative effects of PTH, bisphosphonates, or NSAIDs is purely speculative. References [1] Hame SL, LaFemina JM, McAllister DR, et al. Fractures in the collegiate athlete. Am J Sports Med 2004;32:446–51. [2] Adolphson P, Abbaszadegan H, Boden H, et al. Clodronate increases mineralization of callus after Colles’ fracture: a randomized, double-blind, placebo-controlled, prospective trial in 32 patients. Acta Orthop Scand 2000;71:195–200. [3] van der Poest Clement E, Patka P, Vandormael K, Haarman H, et al. The effect of alendronate on bone mass after distal forearm fracture. J Bone Miner Res 2000;15:586–93. [4] Fleisch H. Can bisphosphonates be given to patients with fractures? J Bone Miner Res 2001;16:437–40. [5] Li C, Mori S, Li J, et al. Long-term effect of incadronate disodium (YM-175) on fracture healing of femoral shaft in growing rats. J Bone Miner Res 2001;16:429–36. [6] Burr DB. Pharmaceutical treatments that may prevent or delay the onset of stress fractures. In: Burr DB, Milgrom C, editors. Musculoskeletal fatigue and stress fractures. Boca Raton (FL): CRC Press; 2001. p. 259–70. [7] Milgrom C, Finestone A, Novack V, et al. The effect of prophylactic treatment with risedronate on stress fracture incidence among infantry recruits. Bone 2004;35:418–24.

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[8] Stewart GW, Brunet ME, Manning M, et al. Treatment of stress fractures in athletes with intravenous pamidronate. Clin J Sport Med 2005;15:92–4. [9] Patlas N, Golomb G, Yaffe P, et al. Transplacental effects bisphosphonates on fetal skeleton ossification and mineralization in rats. Teratology 1999;60:68–73. [10] Geddes AD, D’Souza SM, Ebetino FH, et al. Bisphosphonates structure-activity relationships and therapeutic implications. J Bone Miner Res 1994;8:265–306. [11] Minsker DH, Manson JM, Peter CP. Effects of the bisphosphonate, alendronate, on parturition in rats. Toxicol Appl Pharmacol 1993;121:217–23. [12] Skripitz R, Aspenburg P. Parathyroid hormone: a drug for orthopaedic surgery? Acta Orthop Scand 2004;75:654–62. [13] Selye H. On the stimulation of new bone-formation with parathyroid extract and irradiated ergosterol. Endocrinology 1932;16:547–8. [14] Dobnig H, Turner RT. Evidence that intermittent treatment with parathyroid hormone increases bone formation in adult rats by activation of bone lining cells. Endocrinology 1995;136:3632–8. [15] Qi H, Li M, Wronski TJ. A comparison of the anabolic effects of parathyroid hormone at skeletal sites with moderate and severe osteopenia in aged ovariectomized rats. J Bone Miner Res 1995;10:948–55. [16] Jilka RL, Weinstein RS, Bellido T, et al. Increased bone formation by prevention of osteoblast apoptosis with parathyroid hormone. J Clin Invest 1999;104:439–46. [17] Bellido T, Ali AA, Plotkin LI, et al. Proteasomal degradation of Runx2 shortens PTH-induced anti-apoptotic signaling in osteoblasts: a putative explanation for why intermittent administration is needed for bone anabolism. J Biol Chem 2003;278:50259–72. [18] Frost HM, Jee WS. On the rat model of human osteopenias and osteoporoses. Bone Miner 1992;18:227–36. [19] Hodsman AB, Fraher LJ, Watson PH, et al. A randomized controlled trial to compare the efficacy of cyclical parathyroid hormone versus cyclical parathyroid hormone and sequential calcitonin to improve bone mass in postmenopausal women with osteoporosis. J Clin Endocrinol Metab 1997;82:620–8. [20] Cosman F, Lindsay R. Is parathyroid hormone a therapeutic option for osteoporosis? A review of the clinical evidence. Calcif Tissue Int 1998;62:475–80. [21] Dempster DW, Cosman F, Kurland ES, et al. Effect of daily treatment with parathyroid hormone on bone microarchitecture and turnover in patients with osteoporosis: a paired biopsy study. J Bone Miner Res 2001;16:1846–53. [22] Halloran BP, Birkle DD, Harris J, et al. Regional responsiveness of the tibia to intermittent administration of parathyroid hormone as affected by skeletal unloading. J Bone Miner Res 1997;12:1068–74. [23] Zhang L, Takahashi HE, Inoue J, et al. Effects of intermittent administration of low dose human PTH (1–34) on cancellous and cortical bone of lumbar vertebral bodies in adult beagles. Bone 1997;21:501–6. [24] Andreassen TT, Ejersted C, Oxlund H. Intermittent parathyroid hormone (1–34) treatment increases callus formation and mechanical strength of healing rat fractures. J Bone Miner Res 1999;14:960–8. [25] Skripitz R, Andreassen TT, Aspenberg P. Strong effect of PTH (1–34) on regenerating bone: a time sequence study in rats. Acta Orthop Scand 2000;71:619–24. [26] Holzer G, Majeska RJ, Lundy MW, et al. Parathyroid hormone enhances fracture healing: a preliminary report. Clin Orthop 1999;366:258–63. [27] Nakajima A, Shimoji N, Shiomi K, et al. Mechanisms for the enhancement of fracture healing in rats treated with intermittent low-dose human parathyroid hormone (1–34). J Bone Miner Res 2002;17:2038–47. [28] Neer RM, Arnaud CD, Zanchetta JR, et al. Effect of parathyroid hormone (1–34) on fractures and bone mineral density in postmenopausal women with osteoporosis. N Engl J Med 2001;334:1434–41. [29] Body JJ, Gaich GA, Scheele WH, et al. A randomized double-blind trial to com-

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[46] [47] [48] [49] [50]

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pare the efficacy of teriparatide [recombinant human parathyroid hormone (1–34)] with alendronate in postmenopausal women with osteoporosis. J Clin Endocrinol Metab 2002; 87:4528–35. Omeroglu H, Ates Y, Akkus O, et al. Biomechanical analysis of the effects of single highdose vitamin D3 on fracture healing in a healthy rabbit model. Arch Orthop Trauma Surg 1997;116:271–4. Delgado-Martinez AD, Martinez ME, Carrascal MT, et al. Effect of 25-OH-vitamin D on fracture healing in elderly rats. J Orthop Res 1998;16:650–3. Brumbaugh PF, Speer DP, Pitt MJ. 1-alpha, 25-Dihydroxyvitamin D3 a metabolite of vitamin D that promotes bone repair. Am J Pathol 1982;106:171–9. Doetsch AM, Faber J, Lynnerup N, et al. The effect of calcium and vitamin D3 supplementation on the healing of the proximal humerus fracture: a randomized placebocontrolled study. Calcif Tissue Int 2004;75:183–8. Zhang X, Schwarz EM, Young DA, et al. Cyclooxygenase-2 regulates mesenchymal cell differentiation into osteoblast lineage and is critically involved in bone repair. J Clin Invest 2002;109:1405–15. Simon AM, Manigrasso MB, O’Connor JP. Cyclo-oxygenase 2 function is essential for bone fracture healing. J Bone Miner Res 2002;17:963–76. Gerstenfeld L, Thiede M, Seibert K, et al. Differential inhibition of fracture healing by nonselective and cyclooxygenase-2 (COX2) selective non-steroidal anti-inflammatory drugs. J Orthop Res 2003;21:67. Brown KM, Saunders MM, Kirsch T, et al. Effect of COX-2 specific inhibition on fracturehealing in the rat femur. J Bone Joint Surg Am 2004;86A:116–23. Allen H, Wase A, Bear W. Indomethacin and aspirin: effect of nonsteroidal antiinflammatory agents on the rate of fracture repair in the rat. Acta Orthop Scand 1980; 51:595–600. Altman RD, Latta LL, Keer R, et al. Effect of nonsteroidal anti-inflammatory drugs on fracture healing: a laboratory study in rats. J Orthop Trauma 1995;9:392–400. Elves M, Bayley I, Raylance P. The effect of indomethacin upon experimental fractures in the rat. Acta Orthop Scand 1982;53:35–41. Hogevold H, Grogaard B, Reikeras O. Effects of short-term treatment with corticosteroids and indomethacin on bone healing. Acta Orthop Scand 1992;63:600–11. Suddmann E, Tveita T, Hald J. Lack of effect of indomethacin on ordered growth of the femur in rats. Acta Orthop Scand 1982;53:43–9. Bennell K, Brukner P. How should you treat a stress fracture? In: MacAuley D, Best T, editors. Evidence based sports medicine, volume 26. London: BMJ Books; 2002. p. 491–517. Wheeler P, Batt ME. Do non-steroidal anti-inflammatory drugs adversely affect stress fracture healing? A short review. Br J Sports Med 2005;39:65–9. Adolphson P, Abbaszadegan H, Jonsson U, et al. No effects of piroxicam on osteopenia and recovery after Colles’ fracture: a randomized, double-blind, placebo-controlled, prospective trial. Arch Orthop Trauma Surg 1993;112:127–30. Bhattacharyya T, Levin R, Vrahas MS, et al. Nonsteroidal anti-inflammatory drugs and nonunion of humeral shaft fractures. Arthritis Rheum 2005;53(3):364–7. Bhandari M, Tornetta P, Sprague S, et al. Predictors of reoperation following operative management of fractures of the tibial shaft. J Orthop Trauma 2003;17:353–61. Burd T, Hughes M, Anglen J. Heterotopic ossification prophylaxis with indomethacin increases the risk of long-bone nonunion. J Bone Joint Surg Br 2003;85B:700–5. Deguchi M, Rapoff AJ, Zdeblick TA. Posterolateral fusion for isthmic spondylolisthesis in adults: analysis of fusion rate and clinical results. J Spinal Disord 1998;11:459–64. Giannoudis PV, MacDonald DA, Matthews SJ, et al. Nonunion of the femoral diaphysis: the influence of reaming and non-steroidal anti-inflammatory drugs. J Bone Joint Surg Br 2000;82B:655–8. Glassman SD, Rose SM, Dimar JR, et al. The effect of postoperative nonsteroidal antiinflammatory drug administration on spinal fusion. Spine 1998;23:834–8.

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[52] Reuben SS, Ekman EF. The effect of cyclooxygenase-2 inhibition on analgesia and spinal fusion. J Bone Joint Surg Am 2005;87A:536–42. [53] Reuben SS, Ablett D, Kaye R. High dose nonsteroidal anti-inflammatory drugs compromise spinal fusion. Can J Anaesth 2005;52:506–12. [54] Mayer D. Sources of bias. In: Mayer D, editor. Essential evidence-based medicine. Cambridge (UK): Cambridge University Press; 2004. p. 74–86.

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CLINICS IN SPORTS MEDICINE Stress Fractures in the Spine and Sacrum Lyle J. Micheli, MD*, Christine Curtis, BS, MEd Division of Sports Medicine, Department of Orthopedics, Children’s Hospital Boston, 319 Longwood Avenue, 6th Floor, Boston, MA 02115, USA

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veruse injuries of the spine are seen commonly in clinical practice. It is estimated that 10% to 15% of the athletic population experiences back injuries [1,2]. The high performance athlete seen frequently in the sports medicine clinic may be at an increased risk for back injury [3]. Athletes who participate in sports that require repeated hyperextension and flexion may be at particularly high risk [4–6]. Athletes with back injuries present typically with the complaint of back pain caused by acute traumatic injuries or overuse injuries or a combination of both [7]. Acute traumatic injuries may result from a single fall or torsion, whereas overuse injuries are the result of repetitive micro trauma, usually resulting from excessive training [7]. Reports of stress fractures are becoming more prevalent in the pediatric literature. There are a number of reasons for this, including increased participation in recreational and competitive sports, increased training time and competition, and an increased awareness of athletic injuries by physicians and trainers [8]. Prospective studies have reported annual incidence rates as high as 20% in military recruits and young female athletes [9]. Although stress fractures in the lower extremities have been reported extensively [10–12], stress fractures of the lumbar spine, particularly the pars (spondylolysis), pedicle, and sacrum, also are of concern to the physician. These conditions may manifest as lower back pain, a condition experienced by 35% of adolescent athletes [13]. What is of additional concern is that overuse back injuries are difficult to overcome once they are present and can recur in 26% of males and 33% of females [14]. Early diagnosis and proper medical management of stress fractures of the pars (spondylolysis), pedicle, and sacrum are crucial to avoid significant morbidity and to return athletes safely to competition. This article reviews current concepts in the assessment and management of stress fractures of the lumbosacral spine, particularly of the pars (spondylolysis), pedicles, and sacrum. * Corresponding author. E-mail address: [email protected] (L.J. Micheli).

0278-5919/06/$ – see front matter doi:10.1016/j.csm.2005.08.001

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OVERVIEW OF STRESS FRACTURES A stress fracture can be defined as a skeletal defect that results from repeated applications of stress of lower intensity than that required to fracture a bone in a single loading [9,15]. Stress fractures in athletes were first described by Devas [16] in 1958. They are commonly referred to as fatigue fractures in the adolescent athletic population. CAUSE The cause of stress fractures remains controversial. Most clinicians agree that stress fractures in the lumbar spine result from a repetitive process as opposed to a single traumatic event. Two theories, the overload theory and the muscle fatigue theory, have been proposed to explain stress fractures [17]. In the overload theory, rhythmic and repetitive contractile activity of the muscles produces stress at their osseous insertions, which reduces the mechanical resistance of the bone [18]. Stress fractures resulting from non-weight-bearing activities can be explained by this theory [18]. The muscle fatigue theory states that progressive exhaustion during activity decreases the ability of the muscle to act as a shock absorber [19,20]. Abnormal load distribution occurs, leading to the concentration of stress in certain areas of the bone [17]. STRESS FRACTURES IN THE LUMBAR SPINE The lumbar spine consists of five lumbar vertebrae joined to the sacrum at the pelvis. Stress fractures of the lumbar vertebral column are relatively common, and the site of injury depends on the direction in which the stress is applied [17]. The main components of lumbar motion are believed to occur at the L3–L4 and L5–S1 levels [7]. Fractures of the pedicle [21–23] and sacrum [24–29] occur, but fractures of the pars are most frequent [17,30,31]. Risk Factors for Stress Fractures in the Lumbar Spine in Adolescent Athletes There are several major risk factors in the adolescent spine that make it susceptible to stress fractures. Growth Cartilage The adolescent spine has immature areas of growth cartilage and ossification centers that are subject to torsion injury, compression, and distraction [4]. These areas are the weakest links in the transfer of forces through the spine [4]. There is one ossification center at each side of the neural arch at the pedicles. Ossification may be incomplete and may be congenitally incomplete on the superior portion of the pars interarticularis of the lower vertebrae, especially L5 [4]. The superior arch is subject to stress from the abutting inferior articular facet of L4 [32], and spondylolytic stress fractures may result [4]. Biomechanics The motion of the spine involves constantly changing repetitive flexion and extension [7]. In sports and activities such as ballet and gymnastics, repetitive

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motions and hyperextensions place high demand on the lumbar spine [5,33]. Compression forces across the spine can result in stress fractures of the pars (spondylolysis) as well as other elements of the neural arch. Nutrition Teenaged girls constitute the fastest growing segment of children and adolescents participating in organized athletics [34]. These young athletes may be at increased risk for the female athlete triad, a condition that describes the interrelatedness of disordered eating, amenorrhea, and low bone density [34]. In the female athlete triad, poor nutrition (disordered eating) leads to decreased body weight, which leads to decreased estrogen. It also leads to decreased bone density. Poor nutrition (disordered eating), decreased weight, and over-exercising can lead to amenorrhea, which in turn can result in decreased estrogen levels and low bone density and, thus, place females at an increased risk for stress fractures. SPONDYLOLYSIS Spondylolysis, a stress fracture of the pars interarticularis (the part of the lamina located between the superior and inferior articular processes of the vertebrae), is one of the most common conditions associated with lower back pain in adolescent athletes [35]. In the adolescent athlete population, the fracture of the pars interarticularis occurs at a time of spinal growth in the posterior elements, as well as anterior elements of the attached growth plate [36]. A recent study at Children’s Hospital Boston [37] examined 100 athletic patients under the age of 18 who had back pain and found spondylolysis present in 47 of these patients. Spondylolysis caused by overuse injuries is increasingly being diagnosed in younger patients between 5 and 10 years of age [7,37–39]. These findings demonstrate the high occurrence of spondylolysis in the adolescent athletic population and the increasing importance of physician vigilance in its early detection. In a prospective study by Beutler and colleagues [40], 500 first-grade students were examined for spondylolysis and were followed for 45 years. Over the 45-year period, the authors found spondylolysis in 6% of the subjects; 4.4% of the total population had developed spondylolysis by the age of 6; and an additional 1.6% of the subjects had developed the condition by the age of 14. Studies such as these suggest that the onset of spondylolysis in the general population may be a preadolescent condition [36]. Cause The cause of spondylolysis is controversial. The precipitating factor in the condition is considered to be mechanical, arising from fatigue failure [30,31]. This notion has been demonstrated in biomechanical studies. In a study by Cyron and colleagues [30,31], the inferior articular facets of lumbar vertebrae were subjected to various loading patterns. Results indicate that the lumbar neural arch at the pars interarticularis is vulnerable to mechanical fatigue. This is

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Fig. 1. Lysis of one or both of the pars interarticularis in the posterior elements of the lumbar spine may result from repetitive extension or rotation of the lower spine. G, LS vertebral body; R, LS spinous process.

further supported in a study by Merbs [41] in which Alaskan Eskimos crouch in positions for long periods of time, subjecting them to unusual stresses becoming concentrated in the lower back. Other proposed origins of spondylolysis include trauma, genetics, and developmental defects (Fig. 1) [5]. Epidemiology In the general population the prevalence of spondylolysis is 4% to 6% [7,36]. Bilateral spondylolysis is more common than unilateral spondylolysis, and L5 is the most commonly affected level of the vertebrae [40,42–44]. In the athletic population, females may be at an increased risk for spondylolysis. This is in contrast to the general population in which males are twice as likely to develop the condition. This gender difference may be attributed to a wide range of factors that include hormonal abnormalities and nutritional factors [5,45,46]. The recent increase in female sports participation also may play a role [45,46]. The number of female athletes participating at the high school, collegiate, and elite levels has increased nearly 10-fold since the passage of Title IX [46]. Title IX requires that all schools that receive federal funding must provide equal opportunities for men and women. As with all other stress fractures, a thorough medical history of a female athlete is important to rule out amenorrhea and low mineral bone density, which are prevalent in female athletes and may put them for increased risk of stress fractures [4,9]. The general athletic population is not necessarily at a higher risk than the general population for developing spondylolysis; however, athletes in certain sports with repetitive hyperextension, extension, and rotational movements of the back show an increase in the incidence of a spondylolytic cause [4–8]. Examples of such sports are ballet, gymnastics, diving, and soccer [4–8,37,39]. In a study by Ciullo and Jackson [47], there was an 11% incidence of spondylolysis in female gymnasts, approximately four times the anticipated rate in North America.

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Clinical Presentation Spondylolysis in the athletic population is commonly symptomatic [6,7,37,48]. The adolescent athlete presents with lower back pain, which becomes worse with activity. A thorough history of the onset of back pain is important, including gradual or acute onset, associated factors such as growth spurt or increased training, and the presence of systemic symptoms or night pain [4,7]. On physical examination, there may be tenderness to palpation at the affected vertebral level. Range of motion may be limited or painful in flexion and extension but is usually more compromised in extension. Hamstrings are typically tight on popliteal angle testing as well as straight leg raises. Eighty percent of patients are noted to have tight hamstrings on physical examination [49]. Single leg lumbar extension will often reproduce the pain on the ipsilateral side [47]. To establish the diagnosis of spondylolysis, certain diagnostic imaging modalities can be helpful. Diagnostic Imaging The initial diagnostic workup consists of plain radiographs, which include anterior and posterior views of the lumbar spine [4,5,36]. A sign suggestive of spondylolysis on the anteroposterior (AP) view is lateral deviation of the spinous process caused by associated rotation of the spinous process toward the shorter of the laminae [35]. Plain radiographs have a low sensitivity for diagnosing spondylolysis, and early radiographic changes may not be detected [50]. They are, however, more helpful in detecting spondylolisthesis, the slipping of all or part of the vertebrae forward over one another. In addition, the presence of spina bifida occulta on plain films increases the likelihood of spondylolysis (Fig. 2) [47]. SPECT bone scans are more sensitive at detecting spondylolysis than initial radiographs or planar bone scans [47,51]. Single photon emissioncomputed tomography (SPECT) bone scans are used to identify areas of bone turnover at the pars interarticularis in patients with spondylolysis and are

Fig. 2. Spina bifida occulta, as observed on standard AP radiographs of the lumbosacral spine, increases the likelihood of spondylolysis as a cause of lower back pain in adolescents.

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Fig. 3. CT scan of L5 demonstrates bilateral spondylolysis.

advantageous because they can remain positive for 6 to 9 months, even when the patient is asymptomatic [35]. CT scans have become the accepted method of characterizing fractures [13,52]. They are currently the gold standard for detailing bony morphology and depicting osseous pathoanatomy (Fig. 3) [13]. Recently, many physicians and researchers have put more emphasis on the use of the advanced multiplanar cross-sectional imaging modality of MRI [53–55] in the diagnosis and evaluation of spondylolysis [6]. As Lim and colleagues [13] have espoused, MRI could potentially offer a more streamlined way to evaluate spondylolysis because it can demonstrate both bony anatomy and bony edema and inflammation in one single test, as opposed to combining the complementary modalities of CT and SPECT imaging, which currently serve as adjuncts to each other. A recent investigation by Campbell and colleagues [56] has shown good correlation between MRI with CT and with SPECT imaging. In the future, MRI may prove useful in the follow-up examination of these fractures. Treatment Treatment for spondylolysis varies and reflects a lack of consensus among practitioners. At Children’s Hospital Boston, an athlete with spondylolysis is taken out from sports and treated initially with a 0°-extension Boston overlapping brace, which is worn for 23 hours per day. The primary goal of bracing is to decrease the lumbar lordosis, rendering the sagittal alignment of the pars more vertical, thus reducing shear forces, while also promoting healing of the lesion [7,36]. In addition, a physical therapy regimen that initiates both peripelvic flexibility and antilordotic strengthening is prescribed. Activity is restricted to physical therapy, the stationary bike, and swimming (excluding the butterfly stroke and breaststroke). All hyperextension maneuvers of the spine are avoided. After a period of 4 to 6 weeks, the athlete is reexamined. If the athlete is painfree, particularly on extension, he or she is returned to sports, while continuing bracing, provided that he or she remains asymptomatic and continues with physical therapy. The initial goal of physical therapy is spinal stabilization. If the

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athlete continues to experience pain, wearing the brace and physical therapy (antilordotic and peripelvic flexibility exercises) are continued until he or she is pain-free. At the 4-month mark of treatment, a CT scan is performed to assess healing. The patient is clinically assessed. The optimal goal of the treatment is a pain-free bony union. Patients who exhibit bony union or a persistent pain-free nonunion at the site of the lysis (fibrous union) are allowed to fully return to activities at this point and are weaned from the brace. Therefore, the clinical status of the patient predominates radiographic healing [7]. According to one study, 78% of patients with symptomatic spondylolysis who were treated with a Boston overlapping brace demonstrated good or excellent results with full return to sports [5]. Electrical stimulation is considered in patients who exhibit a painful nonunion at the 4-month mark. This technology has been used successfully in an attempt to heal established nonunions in long bone fractures [57]. It is believed that electrical stimulation mimics the negative potential created by the body’s electrical impulses at the fracture site. Research is currently underway at the present authors’ institution and several others to determine the effectiveness of electrical stimulation in healing patients with spondylolysis (Fig. 4) [36]. Surgical stabilization may be considered in patients who have failed conservative treatment and have persistent pain with sports and activities of daily living. The typical form of treatment is a posterolateral transverse process fusion [7]. After surgery, the patient is immobilized in a cast or brace for 3 to 6 months [7]. Sports activities are not permitted until 12 months after fusion occurs. A return to contact sports must be individualized after lumbar fusion [58,59]. PEDICLE FRACTURES Pedicle stress fractures are an uncommon cause of lower back pain [60]. Of increasing interest in the pediatric literature is the development of pedicle stress

Fig. 4. (A) Painful spondylolysis in a 19-year-old volleyball player, unhealed despite 9 months of bracing and physical therapy. (B) Bony union and pain relief was attained after 4 months of electric bone stimulation.

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fractures among athletes with spondylolysis [21–23]. Defects of the pedicle of the lumbar spine may be congenital [61]. Pedicle stress fractures also may result as a complication of posterolateral lumbar fusion, laminectomy, and surgery for idiopathic thoracolumbar scoliosis [61,62]. Cause The cause of pedicle stress fractures remains controversial among clinicians. In mechanical testing of the neural arch, the pedicle has been shown to be the second point of weakness after the pars [61]. Cyron and colleagues [31] have found that the pars interarticularis failed 10 times more than the pedicles did when the lumbar spine was loaded in flexion [23,31]. The two main reasons for this are the pedicle is mechanically stronger than the pars interarticularis [23], and the anatomy and biomechanics of the lumbar spine serve to selectively concentrate shear stress at the pars interarticularis [63–65]. Biomechanics Pedicle stress fractures result from abnormal forces distributed across the neural arch [66–68]. This condition may be explained partly by the location of the pedicles near the pars and the relatively immature ossification center in the pediatric athlete at each side of the neural arch at the pedicles [4]. Abnormal forces across the neural arch that result in fractures of the pars may also result in a redistribution of forces, leading to a pedicle fracture in the contralateral side [66,67]. In a study by Sairyo and colleagues [66], two of 13 patients (15.4%) with unilateral spondylolysis developed a stress fracture of the contralateral pedicle. This study supports the hypothesis that the stresses in the contralateral pedicle increase in response to axial loads, especially in axial rotation. In another study, Abel [68] has demonstrated that spondylolytic defects begin at the inferior margin of the pedicle, which is under the highest concentration of stress, and are then propagated obliquely across the pars interarticularis as the forces increase [23,68]. Prevalence The exact prevalence of pedicle stress fractures is unknown, yet there are a number of case reports in the athletic population [21–23]. In addition to their biomechanical findings, Sairyo and colleagues [66] have demonstrated that, with advancing stages of spondylolysis, the stress at the contralateral pedicle side begins to increase, causing the sclerosis-fracture. The present author (LJM) [23] has demonstrated that isolated lesions may occur in the pedicles in dancers who repeatedly flex and extend the spine. Pedicle stress fractures also have been described in Olympic athletes and female athletes [21,22]. Diagnostic Imaging As in all stress fractures, the early detection of pedicle stress fractures is important for early diagnosis and early return to sport for athletes. Plain radiography may reveal sclerosis of the pedicle [69]. Bone scintigraphy with single photon emission-CT is favored for the initial evaluation [70].

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TREATMENT Conservative treatment includes rest and bracing. Exercises such as pelvic tilting, stretching of the thoracolumbar fascia, and strengthening of the gluteal muscles have been shown to be effective [23]. In cases in which conservative treatment fails, surgical intervention may be necessary. SACRAL STRESS FRACTURES A once uncommon cause of lower back and buttock pain, sacral stress fractures are being reported now with increasing frequency in the medical literature [6,24–29,71–74]. In 1989, Volpin and colleagues [75] reported the first series of sacral stress fractures among a health population. In their study, they identified three military recruits with stress fractures of the sacral wing. Since then, there have been numerous case reports of sacral stress fractures in athletes, particularly long distance runners [24–27,29,74,76]. Mechanism of Injury The sacrum is the keystone in the arch of the pelvis [77]. Large stresses pass through it into the innominate bones, causing a stress fracture [77]. The sacrum, like every bone in the pelvis and the lower limb, participates in bearing weight and may be susceptible to stress fractures. Cause Sacral stress fractures are caused by stress concentrations of the vertical body forces that are dissipated from the spine to the sacrum and ala sacralis and then to the alae illi [76]. The proposed causes of sacral stress fractures include leg length discrepancies leading to unequal stride length and corresponding asymmetrical movements of hips, sacroiliac structures, and the lower spine [76]. These causes, however, have not been confirmed in biomechanical studies. Some case reports have shown that these sorts of fractures appear commonly after increasing the intensity of an activity or altering the manner in which a given activity is performed [24,27]. Patient Population There are two types of sacral stress fractures: insufficiency fractures and fatigue fractures. Insufficiency fractures are more common and usually occur in osteoporotic bone, with minimal or unremembered trauma [78,79]. Thus, this type occurs more commonly in elderly females and are frequently bilateral, presenting as lower back pain [78]. In the athletic population, sacral stress fractures (considered fatigue fractures resulting from their mechanical cause) are an uncommon cause of lower back pain [6]. The prevalence is unknown [6]; however, studies have shown that they appear to be more common in female athletes [27,28,80]. They have been reported in such athletes as distance runners and volleyball players (Fig. 5) [24,25,71,72,74].

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Fig. 5. Bone scan of sacral stress fracture in a young female runner.

Clinical Presentation Because the sacral pain may radiate downward to the buttock area, patients present with vague, nonspecific lower back, buttock, or hip pain. There may be paramedian point tenderness on one side of the sacrum or sacroiliac joint. The Faber test (figure-of-four test of the lower extremity) may be positive on the ipsilateral side [6]. A hopping test in which pain is reproduced by bouncing on the leg and the affected side has been described [81]. The flamingo test (patient standing on the ipsilateral leg) also may be positive [6]. Differential Diagnosis In patients presenting with lower back pain, differential diagnoses include degenerative disk disease and sacroiliac joint dysfunction [6,24,27]. Diagnostic Imaging Plain radiographs are not sensitive enough to reveal sacral stress fractures. This may in part be because of the geometry of the sacrum, soft tissues, overlying bowel gas, and attempts to shield the reproductive organs from radiation [24]. A study by Eller and colleagues [74] reported sacral stress injuries evident on two of 17 radiographs in patients who were later confirmed to have stress fractures. Bone scintigraphy and MRI have been found to be effective means to diagnose sacral stress fractures that were not identified previously identified by plain radiography [24]. Bone scans are used for their high sensitivity for detecting areas of bone turnover. The limitations of bone scans are that increased activity in the sacral region, symmetric or asymmetric, may be interpreted as arising in the sacroiliac joints when caused by either sacroiliac joint dysfunction or sacroiliitis [24]. MRI may offer a way to evaluate bony anatomy and bony edema [13]. This method of diagnostic imaging has been used in several studies to detect sacral stress fractures [24]. MRI offers the absence of ionizing radiation. It is also advantageous in that it can define the anatomic location [24]. CT scans also can be used to stage the fracture line, which is why they are believed currently to be the gold standard for demonstrating details of bony morphology and osseous pathoanatomy [13].

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Treatment of Sacral Stress Fractures The treatment regimens that have been reported consist of rest periods lasting from 6 weeks to 8 months [24–26]. A return to sports should be based on each patient's extent of pain and severity of injury. Treatment should be tailored to the specific underlying cause, which may first include non-weight-bearing activities and then exercise that builds back into the original activities performed before the fracture occurred. SUMMARY Stress fractures of the pars, pedicle, and sacrum are important considerations in the differential diagnosis of lower back pain in the child or adolescent athlete. A thorough history and physical examination as well as a high index of suspicion are essential when assessing a patient with lower back pain . Diagnostic imaging, including radiographs, bone scans, CT scans, and other imaging modalities are important for further narrowing the diagnosis. The early identification and proper management of stress fractures of the pars, pedicle, and sacrum are integral in the prevention of stress fractures in the adolescent athlete population. References [1] Spencer GW, Jackson DW. Back injuries in the athlete. Clin Sports Med 1983;2:191–216. [2] Gerbino PG, Micheli LJ. Low back injuries in the young athlete. In: Sports medicine and arthroscopy review. Philadelphia: Lippincott-Raven; 1996. p. 122–31. [3] Ferguson RH, McMaster JF, Stanitski CL. Low back pain in college football lineman. Am J Sports Med 1974;2:63–9. [4] D’Hemecourt P, Gerbino P, Micheli L. Back injuries in the young athlete. Clin Sports Med 2000;19(4):663–75. [5] D’Hemecourt PA, Zurakowski D, Kriemler S, et al. Spondylolysis: returning the athlete to sports participation without brace treatment. Orthopedics 2002;25(6):656–7. [6] Bono CM. Low-back pain in athletes. J Bone Joint Surg Am 2004;86A(2):382–6. [7] Micheli LJ, Mintzer CM. Overuse injuries of the spine. In: Harries M, Williams C, Standish WD, et al, editors. Oxford textbook of sports medicine. 2nd edition. New York: Oxford University Press; 1998. p. 709–20. [8] Coady CM, Micheli L. Stress fractures in the pediatric athlete. Clin Sports Med 1997; 16(2):225–38. [9] Loud KJ, Gordon CM, Micheli LJ, et al. Correlates of stress fractures among preadolescent and adolescent girls. Pediatrics 2005;115(4):e399–406. [10] Mattheson GO, Clement D, McKenzie DC, et al. Stress fractures in athletes. A study of 320 cases. Am J Sports Med 1987;15(1):46–58. [11] Korpelainen R, Orava S, Karpakka J, et al. Risk factors for recurrent stress fractures in athletes. Am J Sports Med 2001;29(3):304–10. [12] Brown TD, Micheli LJ. Foot and ankle injuries in dance. Am J Orthop 2004;33(6):303–9. [13] Lim MR, Yoon SC, Green DW. Symptomatic spondylolysis: diagnosis and treatment. Curr Opin Pediatr 2004;16(1):37–46. [14] Taimela S, Kujala UM, Salinen JJ, et al. The prevalence of low back pain among children and adolescents: a nationwide cohort-based questionnaire survey in Finland. Spine 1997; 22:1132–6. [15] Martin AD, McCulloch RG. Bone dynamics: stress, strain, and fracture. J Sports Sci 1987; 5:155–63. [16] Devas MB. Stress fractures in athletes. Nurs Times 1971;67(8):227–32. [17] Puddu GC, Guglielmo C, Alberto S, et al. Stress fractures. In: Harries M, Williams C,

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[45] D’Hemecourt PA, Micheli LJ, Gerbino P. Spinal injuries in female athletes. Sports Medicine and Arthroscopy Review 2002;10:91–7. [46] Donaldson ML. The female athlete triad: a growing health concern. Orthop Nurs 2003; 22(5):322–4. [47] Ciullo JV, Jackson DW. Pars interarticularis stress reaction, spondylolysis, and spondylolisthesis in gymnasts. Clin Sports Med 1985;4(1):95–110. [48] Wimberly RL, Lauerman WC. Spondylolysis in the athlete. Clin Sports Med 2002;21(1): 133–45. [49] Phalen GS, Dickson JA. Spondylolysis and tight hamstrings. J Bone Joint Surg Am 1961; 43A:505–12. [50] Miller S, Congeni J, Swanson K. Long term functional and anatomical follow up of early detected spondylolysis in the young athlete. Am J Sports Med 2004;32(4):928–33. [51] Anderson K, Sarwark J, Conway JJ, et al. Assessment with SPECT imaging of stress injuries of the pars interarticularis and response to bracing. J Pediatr Orthop 2000;20(1):28–33. [52] Morita T, Ikata T, Katoh S, et al. Lumbar spondylolysis in children and adolescents. J Bone Joint Surg Br 1995;77B(4):620–5. [53] Logroscino G, Mazza O, Aulisa G, et al. Spondylolysis and spondylolisthesis in the pediatric and adolescent population. Childs Nerv Syst 2001;17(11):644–55. [54] Hollenberg GM, Beattie PF, Meyers SP, et al. Stress reactions of the lumbar pars interarticularis: the development of a new MRI classification system. Spine 2002;27(2):181–6. [55] Udeshi UL, Reeves D. Routine thin slice MRI effectively demonstrates the lumbar pars interarticularis. Clin Radiol 1999;54(9):615–9. [56] Campbell RS, Grainger AJ, Hide IG, et al. Juvenile spondylolysis: a comparative analysis of CT, SPECT and MRI. Skeletal Radiol 2005;34(2):63–73. [57] Mooney V. A randomized double-blind prospective study of the efficacy of pulsed electromagnetic fields for interbody lumbar fusions. Spine 1990;15(7):708–12. [58] Micheli LJ. Sports following spinal surgery in the young athlete. Clin Orthop 1985;152–7. [59] Wright A, Ferree B, Tromanhuser S. Spinal fusion in the athlete. Clin Sports Med 1993;12: 599–602. [60] Sirvanci M, Ulusoy L, Duran C. Pedicular stress fracture in lumbar spine. Clin Imaging 2002;26(3):187–93. [61] Robertson PA, Grobler LJ. Stress fracture of the pedicle: a late complication of posterolateral lumbar fusion. Spine 1993;18(7):930–2. [62] Chong VF, Htoo MM. Pedicular stress fracture in the lumbar spine. Australas Radiol 1997; 41(3):306–7. [63] Grogan JP, Hemminghytt S, Williams AL, et al. Spondylolysis studied with computed tomography. Radiology 1982;145(3):737–42. [64] Hollinshead WH. Anatomy for surgeons. 3rd edition. New York: Harper and Row; 1982. [65] Jackson DW, Wiltse LL, Cirincoine RJ. Spondylolysis in the female gymnast. Clin Orthop 1976;117:68–73. [66] Sairyo K, Katoh S, Sasa T, et al. Athletes with unilateral spondylolysis are at risk of stress fracture at the contralateral pedicle and pars interarticularis: a clinical and biomechanical study. Am J Sports Med 2005;33(4):583–90. [67] Macdessi SJ, Leong AK, Bentivoglio JE. Pedicle fracture after instrumented posterolateral lumbar fusion: a case report. Spine 2001;26(5):580–2. [68] Abel MS. The radiology of low back pain associated with posterior element lesions of the lumbar spine. Crit Rev Diag Imag 1996;20:311–52. [69] Gunzburg R, Fraser RD. Stress fracture of the lumbar pedicle: case reports of “pediculolysis” and review of the literature. Spine 1991;16(2):185–9. [70] Traughber PD, Havlina Jr JM. Bilateral pedicle stress fractures: SPECT and CT features. J Comput Assist Tomogr 1991;15(2):338–40. [71] McFarland EG, Giangarra C. Sacral stress fractures in athletes. Clin Orthop 1996;329: 240–3. [72] Bottomley MB. Sacral stress fracture in a runner. Br J Sports Med 1990;24(4):243–4.

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CLINICS IN SPORTS MEDICINE Stress Fractures of the Femur in Athletes Michael J. DeFranco, MDa, Michael Recht, MDb, Jean Schils, MDb, Richard D. Parker, MDa,* a

Department of Orthopaedic Surgery, A-41, The Cleveland Clinic, 9500 Euclid Avenue, Cleveland, OH 44195, USA b Emergency Radiology, Department of Radiology, RC-35, The Cleveland Clinic, 9500 Euclid Avenue, Cleveland, OH 44195, USA

S

tress fractures are common injuries of the lower extremities in athletes and military recruits. Indeed, stress fractures account for approximately 10% of all injuries seen by sports medicine specialists [1]. The fourth most common type of stress fracture occurs in the femur [1]. Generally, stress fractures of the femur can be subdivided into two categories based on etiology fatigue fractures or insufficiency fractures. The former results from excessive, repetitive stress on normal bone, whereas the latter occurs as secondary to normal activity in bone that is deficient in structure or quantity. Femoral stress fractures are associated with specific activities, such as long-distance running, jumping, and ballet dancing [1–3]. Athletes who are older, female, and white are at a greater risk for developing this injury [1,4–10]. The true incidence of femoral stress fractures is difficult to determine because of the variability in studies and because it is an underdiagnosed condition [2,11,12]. Anatomically, stress fractures can occur anywhere along the length of the femur. The most common sites are in the femoral neck and shaft [13,14]. Femoral neck stress fractures account for approximately 11% of stress fractures in athletes [15,16]. The incidence of stress fractures in the femoral shaft has been reported as approximately 3.5% [6,14,17]. Recently, however, Johnson and colleagues [7] have reported that this injury was underdiagnosed in athletes. According to the authors, the incidence is closer to 20%. This result is similar to a recent study on military recruits in which the incidence was approximately 22% [18]. There is also a difference in the distribution of femoral shaft stress fractures when comparing military recruits with athletes [7]. Provost and Morris [19] have reported that, for military recruits, 51% of femoral shaft stress fractures occur in the distal shaft. In athletes, femoral shaft stress fractures are more common in the mid-medial or posteromedial cortex [6,7]. Distal femoral stress fractures are rare. They may occur in the supracondylar or condylar regions of the distal femur [20–22]. The specific incidence in athletes has not * Corresponding author. E-mail address: [email protected] (R.D. Parker).

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been reported. However, in one study evaluating military recruits, the incidence was approximately 9.2% [20]. There are few reported cases of femoral stress fractures in healthy children and adolescents, all of which have occurred on the inferior (compression) side of the femoral neck [23]. Although it is a relatively uncommon injury, femoral stress fractures require prompt diagnosis. Otherwise, a delayed or missed diagnosis can result in a complete or displaced fracture that requires more aggressive treatment and poses a higher risk for chronic morbidity. A thorough understanding of the pathoanatomy, cause, clinical assessment, and treatment options will facilitate the care of athletes with a femoral stress fracture and the return to a preinjury level of competition. DEFINING FEMORAL SHAFT FRACTURES Pathoanatomy The femur is the largest bone in the body. Stress is produced in the femur whenever it is subjected to a loading force. During normal physiologic activity, the femur is subjected to forces several times the body’s weight. Like most bones, the femur fails under tension but is also at risk in compression. Weight-bearing forces of the proximal femur are approximately 1200 pounds per square inch in a man weighing 200 pounds [24]. In the medial cortex, this force may be exceeded 1 to 3 inches below the lesser trochanter. The force usually is less just opposite the lateral cortex. Bending rather than compressive or torsional forces are most important in the pathogenesis of the majority of stress fractures [20]. With regard to bending forces, two critical factors are the geometric distribution of bone mass rather than bone mass itself and the collagen composition of the bone. Maintaining bone mass is determined partly by bone remodeling. The most widely accepted theory about the development of stress fractures is based on an imbalance in this process. The frequency of loading, the magnitude of load, and the number of repetitions are factors that define the fatigue process. Repetitive stress causes periosteal resorption that occurs at a faster rate than bone formation. As a result, the cortex is weakened and becomes fractured. This microdamage within bone develops with each loading cycle. In moderate and high doses of exercise, bone is unable to adapt to this stress. As a result, cumulative microdamage results in cracks in bone that act as stress raisers and allows for the development of fractures. These fractures may be incomplete, complete, nondisplaced, or displaced. Hormonal disorders and nutritional deficiency may impair the normal response to stress. Certain characteristics of the lower extremity also may influence the stress response of bone by altering the transfer of load to the femur, such as inequality in leg length, coxa vara, and cavus feet [1,20,25,26]. Overall, stress injury to bone represents a spectrum of diseases, from bone stress reaction to stress fracture, which initially may be subclinical. Some authors suggest that muscle fatigue contributes to the development of stress fractures. Bone stress is reduced by contracting muscles that counter

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the load transferred to bone during weight bearing [26]. Functioning muscles with broad attachments to bone normally prevent areas of stress concentration, whereas fatigued muscles do not perform in this manner. Muscle fatigue secondary to physical activity may alter gait and the distribution of stress along weight-bearing bones. This process results in excess concentration of force transmitted to focal sites on the underlying bone, where stress fractures can develop [27]. The location of stress concentration within the femur predisposes certain areas to fracture. The tension side of the femoral neck is considered a high-risk area for progression to a complete fracture. The femoral shaft, on the other hand, is a low-risk area for the development of stress fractures but is susceptible to repetitive stresses [28]. Repetitive forces on the femoral shaft may result in a stress fracture on the medial (compression side) of the femur at the junction of the proximal and middle third of the shaft. The vastus medialis originates in this area, and it also serves as the insertion point for the adductor brevis. Forces transmitted to the femur from the activity of these muscles during weight bearing are considered a causative factor in the development of stress fractures at this site [5,28]. The adductors and vastus medialis may increase compressive strain in this area. Oh and Harris [29] have defined the medial cortex of the femur as the site of greatest compression strain, which diminishes from proximal to distal. The magnitude of compressive strain on the medial side of the femur exceeds the lateral tensile strain, and it decreases progressively from the neck to the distal femur. In the sagittal plane, the highest strain is in the posterior proximal shaft [29]. The iliotibial tract and vastus lateralis also decrease the tensile strain along the lateral aspect of the femur and, as a result, decrease the risk of fatigue fractures in this area [6]. Therefore, despite bone strength being greater in compression, repetitive loads coupled with muscular forces may

Fig. 1. (A) Compression-type femoral neck stress fracture in a child. T1-weighted MR image reveals nonspecific edema, which could be consistent with a stress fracture. (B) Compressiontype femoral neck stress fracture in a child. T2-weighted MR image reveals edema and definitive fracture line in the femoral neck.

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Fig. 2. (A) Adult femoral neck fracture. T1-weighted MR image shows nonspecific changes in the right femoral neck but no definite fracture. (B) Adult femoral neck fracture. STIR MRI image (T2 with fat suppression) reveals edema and a fracture within the right femoral neck.

account for the fatigue fractures that occur on the compression rather than tension side of the femur [6]. Classification Proximal femoral stress fractures are divided into those that occur in the head (subchondral), neck, or subtrochanteric area. Femoral neck fractures can be described as compression-type, tension-type, or displaced. Fig. 1 shows a femoral neck stress fracture in a skeletally immature patient. Fig. 2 shows a femoral neck stress fracture in a skeletally mature patient. Fig. 3 shows the classic radiographic appearance of a femoral neck stress fracture. Stress fractures in the shaft of the femur are described simply as proximal, middle, or distal third femoral shaft stress fractures. Shaft and distal femoral stress fractures may occur medially or laterally. Figs. 4 and 5 show proximal and distal femoral shaft fractures, respectively. Distal femoral stress fractures are also classified as supracondylar,

Fig. 3. Adult femoral neck stress fracture. Radiograph of the left hip reveals classic appearance of stress fracture with sclerotic density located in the inferior aspect of the neck. Orientation of density is perpendicular to the trabeculae of the femoral neck.

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Fig. 4. (A) Initial radiograph from a patient suspected of having a proximal femoral shaft stress fracture. No obvious fracture was diagnosed at the time of presentation. (B) Radiograph obtained approximately 2 months after the initial presentation reveals a proximal femoral stress fracture. (C ) Bone scan image confirms the diagnosis of stress fracture on the proximal shaft of the femur.

condylar, or subchondral. Femoral condyle insufficiency fractures may occur as shown in Fig. 6. In pediatric patients, assessment of the physis is an important part of defining the injury. Several classification systems exist for stress fractures of the femoral neck [30–32]. Fullerton and Snowdy [15] have suggested a four-stage classification

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Fig. 5. (A) Initial radiograph from a patient suspected of having a distal femoral stress fracture. (B,C ) Radiographs reveal progressive stages of healing in the stress fracture of the distal femoral cortex after initial radiograph (Fig. 4A) was obtained.

system based on biomechanical factors and degree of displacement. Generally, the compression-side fracture occurs on the compression side of the femoral neck and usually causes sclerosis in this area. The tension-side fracture occurs on the tension side of the femoral neck, where either callus forms or displacement occurs. Stage 1 is a patient with normal radiographs but positive bone scans. Stage 2 is endosteal or periosteal callus without fracture. Stage 3 is a cortical crack without displacement. Stage 4 is widening of the cortical crack and then displacement [32]. Shin and colleagues [33] (Naval

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Fig. 6. (A) T1-weighted MR image suggestive of distal femoral condyle insufficiency fracture. Image reveals nonspecific edema and replacement of bone marrow. (B) T2-weighted MR image suggestive of distal femoral condyle insufficiency fracture. Image reveals nonspecific edema.

Medical Center, San Diego, CA) have created another classification for femoral neck stress fractures by defining the relevant MRI findings for each stage of injury. Overall, in the classification of femoral stress fractures, it is important to define location, extent of injury (incomplete or complete), and degree of displacement. CAUSES Athletes are at risk for developing either fatigue or insufficiency fractures. Extrinsic risk factors include training schedule, diet, playing surfaces, and equipment such as footwear. Intrinsic risk factors include age, gender, lowerextremity alignment (leg length inequality, coxa vara, or cavus foot), low bone mass, menstrual cycles, and metabolic disorders [3,27,34,35]. Generally, training errors are the most frequently encountered causes of stress fractures [1,10]. Athletes suddenly either increase the intensity of a routine workout or start a new exercise at a level that is beyond the normal physiologic response of bone. Insufficiency fractures in athletes are most commonly related to a metabolic problem related to diet or hormonal imbalance. A daily diet needs to provide sufficient calories to support certain levels of physical activity in athletes. Daily recommended doses of calcium and vitamin D also should be taken to maintain adequate bone density. Female athletes deserve special consideration. Bone mineral density and menstrual disturbance are interrelated and predispose athletes to stress fractures [26]. Age of menarche, menstrual disturbance, low dietary intake of calcium, low bone density, less lean mass in lower limbs, eating disorder, and a history of high intensity training for several years are risk factors for the development of stress fractures in female athletes [36]. Prepubescent girls who initiate serious training and competition before menarche have delayed menarche and may be at increased subsequent risk for secondary amenorrhea and stress fracture [36].

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PRINCIPLES OF DIAGNOSIS Diagnosing femoral stress fractures requires a high degree of suspicion, a detailed medical history, thorough physical examination, and, in most cases, confirmation by an imaging study. Early diagnosis can be difficult. In 75% of the initial examinations, the diagnosis may be missed or the condition may be misdiagnosed [37]. In some cases, the diagnosis may be delayed by 4 to 12 weeks [7]. Additionally, 18% of midshaft and 51% of distal femoral stress fractures in athletes and military recruits are diagnosed after displacement occurs [6,18]. Correct diagnosis in the early phase of stress injury allows for prompt treatment and avoids long-term morbidity. History A detailed medical history begins with inquiring about an athlete’s workout schedule, diet, pain pattern, medical problems, and, if applicable, menstrual cycle irregularities. Typically, pain begins after a change in the usual activity regimen or an increase in its intensity. The pain is usually nonspecific, insidious in onset, and activity-related. The severity of the pain may limit or prohibit activity. Some patients also may experience night pain. The location of pain as described by the patient can help to identify the site of the fracture. Other musculoskeletal problems involving the spine or ipsilateral knee can cause referred pain to the femur. In stress fractures of the femoral neck, the onset of progressive hip pain can be as early as 2 weeks after initiating or changing a conditioning program [32]. Patients with stress fractures of the femoral neck commonly have anterior groin (inguinal) pain [32]. In femoral shaft fractures, pain may be localized to the thigh, but in one study, the most common symptom was ipsilateral knee pain [19]. Distally, patients may complain of pain in a specific point of the femur or describe a more general pattern of knee pain. Physical Examination The clinical presentation can be variable. Swelling of the thigh may or may not be present. Muscle bulk, tone, and strength are usually normal. The point of maximal tenderness is more difficult to localize in the femur than in other common areas of stress fractures such as the tibia and metatarsals, which are more subcutaneous. However, palpation of the groin over the hip joint can reproduce a patient’s symptoms related to stress fractures of the femoral neck [32]. Pain at the extremes of passive range of motion of the hip is another sign of a proximal femur fracture [15]. Patients may ambulate with an antalgic gait, but heel strike and percussion tests correlate poorly with femoral neck fatigue fractures [15]. An active straight leg raise and logrolling of the thigh may accentuate pain [13]. In femoral shaft stress fractures, a torsional or bending stress may be helpful in accentuating the pain associated with the fractures. In the distal femur, the supracondylar and condylar area of the femur are more subcutaneous and readily palpable, which may allow areas of tenderness associated with stress fractures to be localized. Knee range of motion and stability testing may exacerbate this pain. Joint line tenderness and a positive

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Appley grinding test also are signs suggestive of a distal femoral stress fracture [38]. The hop and fulcrum tests are used to exacerbate pain and to localize the site of the femoral stress fracture. The hop test is performed by asking the patient to hop on the involved extremity while being examined. Approximately 70% of patients with a positive hop test have a femoral stress fracture [16]. The fulcrum test assists in diagnosing a femoral shaft stress fracture. To perform this test, the patient is seated while the examiner applies a gentle downward pressure on the knee. At the same time the other arm is used as a fulcrum by applying anterior pressure on the posterior thigh. The patient will experience pain with apprehension during this maneuver when the location of the stress injury is reached, as the examiner progressively advances his fulcrum arm in the direction from hip to knee [7]. In addition to a focused examination of the involved femur, a thorough evaluation of the spine (lumbar, sacrum, and sacroiliac joint), entire lower extremity, and contralateral hip should be completed. Laboratory Studies Laboratory studies are not particularly helpful in the evaluation of patients suspected of having a femoral stress fracture [9,13,31,32,39]. A complete blood cell count, alkaline phosphatase, calcium, phosphorus, and sedimentation rate are helpful in determining the cause of a femoral insufficiency or pathologic fracture. Imaging Studies Most femoral stress fractures require imaging studies to confirm the diagnosis. Currently, the imaging modalities commonly used to assess stress fractures of the femur include plain radiographs, bones scans, and MRI [40]. CT is not a technique routinely used in the evaluation of these stress fractures. Although it may show a cortical break, CT is most useful in assessing the presence of an associated soft tissue mass and cortical destruction [41]. Plain radiography is usually the first imaging study ordered. Any radiolucency, cortical disruption, periosteal thickening, or early callus formation is suspicious for a stress fracture. Many times, however, the initial radiographs are negative in the early stages of injury [5,6,10,30,31]. Within 1 week, less than 10% of radiographs demonstrate changes consistent with stress fractures [1,33,41]. Even serial radiographs obtained at least 2 to 3 weeks after the onset of symptoms may not demonstrate callus formation and early fracture healing [28,30]. Periosteal bone formation is greatest at 6 weeks [41]. Typically, radiographs will depict late changes with periosteal and endosteal bone formation and only occasionally demonstrate a radiolucent fracture line [33]. The inability to readily identify these fractures on plain radiographs early in the course of the stress injury creates problems in terms of management. Specifically, this is the case with femoral neck stress fractures, in which a missed diagnosis can lead to a complete fracture and displacement [42]. In pediatric patients, radiographic assessment includes evaluation of the femoral physes [43]. During the

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past 30 years, technetium bone scans have developed into the gold standard for the identification of stress fractures within 72 hours after injury [28,33,40, 44–46]. The diagnostic finding for stress fractures is increased uptake on all three phases of a technetium 99m diphosphonate bone scan. A negative bone scan can strongly exclude the diagnosis of stress fracture. Single photon emission-computed tomography scans may more precisely localize the area of uptake, especially in the femoral neck [47,48]. Several of the studies on femoral stress fractures in athletes have used bone scans as an essential component to the diagnosis of this injury [5,10,32,33]. Any athlete who experiences lowerextremity symptoms for more than 2 weeks should be considered to have a stress fracture. Roub and colleagues [49] used scintigraphy to reveal that 20% to 40% of patients with negative radiographs had increased isotope uptake consistent with stress fractures. If the radiographs do not reveal a fracture, then a bone scan should be used to help confirm the diagnosis. However, a technetium bone scan delivers a radiation dose (440 mrem) that is equivalent to 44 times the dosage received by a single chest radiograph (10 mrem). Consideration should be given to the radiation dose associated with these imaging studies in the evaluation of patients suspected of having a femoral stress fracture. Recently, MRI has played a more important role in the diagnosis of femoral stress fractures and the differentiation of femoral stress fractures from other causes of thigh pain in athletes [2,33,37,40,50–52]. If an initial radiograph is negative, an MRI may be ordered instead of or in addition to a bone scan. On short tau inversion recovery imaging, fat bone marrow is suppressed, and the fracture appears as a high signal intensity. These images allow for the identification of early marrow edema, which is an initial sign of bone response to stress. T1- and T2-weighted images also can be used to identify areas of femoral stress fracture. Classification systems exist to grade stress injury according to MRI appearance [33,53]. MRI can precisely define the anatomic location and extent of injury as well as any associated soft tissue conditions. Overall, MRI is becoming a more popular diagnostic tool for stress fractures and does play an important role in evaluating athletes with lower-extremity pain. Differential Diagnosis Femoral shaft fractures are difficult to diagnose because of the vague nature of pain, poor localization of tenderness, and few reliable physical examination findings [1,6,10,19]. Other disorders must be considered before proceeding with treatment for a stress fracture of the femur. Vascular, metabolic, inflammatory, infectious, and neoplastic conditions as well as other overuse injuries should be considered in the differential diagnosis. In the proximal femur, these conditions include avascular necrosis, infection, transient osteoporosis, bursitis, tendonitis, synovitis, synovial herniation, muscle or tendon injury, and neoplasm. Femoral shaft pain may be the result of muscle strain, contusion, infection, or neoplasm. Distal femoral pain may be related to internal knee derangement, femoral condyle avascular necrosis, infection, tendon or ligament injury, or neoplasm. In elderly athletes, it is particularly important to con-

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sider spontaneous osteonecrosis of the femoral condyle as a reason for distal femoral pain [54]. The most common misdiagnosis of a stress fracture is bone sarcoma because of the periosteal reaction. The differential diagnosis of problems consistent with this finding includes osteomyelitis, eosinophilic granuloma, osteogenic sarcoma, and Ewing’s sarcoma [19,27]. Hypothyroidism, hyperparathyroidism, hypercortisolism, and neoplastic disease must be considered for pathologic fractures. MANAGEMENT General Principles The management of stress fractures is defined in terms of prevention, nonoperative care, and surgical intervention. Prevention involves education and identification of risk factors. Athletes, coaches, and parents, in the pediatric population, need to understand the impact of excessive physical activity on the musculoskeletal system and its relationship to the development of stress fractures. The importance of early management, whether nonoperative or operative, is evident by the poor results reported following the management of displaced fractures [27,30,31,39]. Although the mechanism of injury for femoral stress fractures is often similar, including military recruits in the discussion of athletes with this injury is difficult and can be confusing for two reasons. First, the incidence and anatomic location of these fractures are different with respect to each group. Second, each group has different training regimens, “playing surfaces,” and equipment. McBryde [55] compared these two groups and has determined that the differences are significant. These differences make it difficult to compare studies between athletes and soldiers and among athletes alone [55]. Published data on femoral stress fractures in athletes consists of single case reports and studies that are the equivalent of case series evidence. The results suggest that most athletes and military recruits do well with nonoperative management. This conclusion is based largely on observational data. Indeed, most studies on both groups are retrospective, lack control groups, and do not include enough patients to detect potentially important trends. Furthermore, there is no standardization between studies on treatment protocols or tools used to assess clinical outcome. Despite these problems, a review of the literature does help to define some of the salient points to consider in the treatment of athletes with femoral stress fractures. Nonoperative Care Most athletes with femoral stress fractures are treated nonoperatively with excellent results [3,5–10,23,56]. Nonoperative care means no surgical intervention, but it does not imply complacency. These patients require a period of rest, which allows the process of bone repair to dominate over resorption. In the literature, the definition of rest ranges from complete bed rest to weight bearing as tolerated, with or without crutches. A more detailed medical evaluation is required for patients who sustain a fracture secondary to a suspected metabolic disorder or hormonal imbalance. Deficiencies of calcium, vitamin D, copper,

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and magnesium disrupt the normal metabolism of bone, which has significant effects on the internal structure and strength of bone [41]. Part of this treatment option is determining the appropriate use of hormone replacement therapy in amenorrheic females. A critique of the athlete’s diet is also important to ensure adequate caloric intake and appropriate vitamins and minerals to maintain adequate bone density. Psychologic assessment may be needed in athletes with eating disorders. A supervised, graduated physical therapy program is required to define and control the duration, frequency, and intensity of activity as the athlete moves closer to full competition. The correction of training errors that led initially to the stress fracture is essential to the rehabilitation process. Athletes are allowed to continue conditioning exercises such as swimming or cycling during the period of rest for their injured femur. In some patients, the use of unloader braces may be appropriate to decrease stress on the involved femoral condyle. To heal the fracture, the process takes approximately 6 to 8 weeks. Repeated radiography is necessary at subsequent follow-up visits. Improvement is gradual, and in most cases, a full recovery is achieved. To return to competition athletes must be pain free. The return to on-field competition is gradual. Operative Care Operative intervention for stress fractures of the femur in athletes is rare [3,9,57]. The potential for certain stress fractures to progress is based on an individual assessment of each fracture and patient. Surgical management of this injury is considered under the following circumstances: failure of nonoperative management, prophylactic stabilization of a fracture at high risk for displacement, a tension-side femoral neck stress fracture, any displaced femoral stress fracture, and a malunion or nonunion. Internal fixation is supported in these cases to restore the stability of the lower extremity and to return the athlete to activity as soon as possible. Complications Complications are associated with both nonoperative care and surgical intervention. Nonoperative care can result in displacement of the fracture. Both strategies can result in nonunion, malunion, osteonecrosis, and arthritic changes [8,30,31,39]. Displaced fractures increase the risk of developing these complications [12,58]. Specifically in athletes, Johansson and colleagues [8] have noted a 30% complication rate, with no athlete returning to a previous level of function regardless of the fracture type. In the young athlete, these complications can be sources of chronic morbidity. The prognosis for young adults after femoral neck fractures is poor, with an estimated 20% to 86% of them going on to develop avascular necrosis [59]. According to Lee and colleagues [59], 23.8% of patients develop avascular necrosis after stress fracture of the femoral head displacement within an average of 5.6 years. Return to Play The return-to-play criteria are based on asymptomatic full weight bearing, no palpable tenderness over the involved area, and usually follow-up imaging

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studies with signs of a healed fracture. Resuming athletic activity occurs at a frequency, intensity, and duration well below the preinjury level of competition. Close follow-up in these patients is essential to avoid recurrence, complete fracture, or nonunion. Persistent pain requires the consideration of an alternative diagnoses, which may involve obtaining more laboratory and imaging studies and, if necessary, a biopsy. SUMMARY Femoral stress fractures represent an uncommon, but important lower-extremity injury in athletes and soldiers. Even though there are differences between these two groups, the principles of evaluation defined in this article can be applied to both of them. Careful assessment of the entire involved and contralateral lower extremity as well as the spine is required to make the diagnosis. Based on a review of the literature, specific treatment depends on the assessment of the individual patient. In most cases, nonoperative management results in an excellent outcome. Certain fractures will require operative intervention to prevent displacement or to reduce a displaced fracture and return stability to the lower extremity. Complications in athletes with femoral stress fractures are rare. Most athletes can expect to return to their preinjury level of competition, if they are compliant with the treatment plan. References [1] Matheson G, Clement D, McKenzie D, et al. Stress fractures in athletes: a study of 320 cases. Am J Sports Med 1987;15:46–58. [2] Arendt E, Agel J, Heikes C. Stress injuries to bone in college athletes. Am J Sports Med 2003;31:959–68. [3] Hulkko A, Orava S. Stress fractures in athletes. Int J Sports Med 1987;8:221–6. [4] Bennell K, Brukner P. Epidemiology and site specificity of stress fractures. Clin Sports Med 1997;16:179–96. [5] Butler J, Brown S, McConnell B. Subtrochanteric stress fractures in runners. Am J Sports Med 1982;10:228–32. [6] Hershman E, Lombardo J, Bergfeld J. Femoral shaft stress fractures in athletes. Am J Sports Med 1990;9:111–9. [7] Johnson A, Weiss C, Wheeler D. Stress fractures of the femoral shaft in athletes: more common than expected. Am J Sports Med 1994;22:248–56. [8] Johansson C, Ekenman I, Tornkvist H, et al. Stress fractures of the femoral neck in athletes. Am J Sports Med 1990;18:524–8. [9] Lombardo S, Benson D. Stress fractures of the femur in runners. Am J Sports Med 1982; 10:219–27. [10] Orava S, Puranen J, Ala-Ketola L. Stress fractures caused by physical exercise. Acta Orthop Scand 1978;49:19–27. [11] Hallal T, Amit S, Segal D. Fatigue fractures of the tibial and femoral shaft in soldiers. Clin Orthop 1976;118:35–43. [12] Blickenstaff L, Morris J. Fatigue fracture of the femoral neck. J Bone Joint Surg Am 1966;48A:1031–47. [13] Shin A, Gillingham B. Fatigue fractures of the femoral neck in athletes. J Am Acad Orthop Surg 1997;5:293–302. [14] Orava S. Stress fractures. Br J Sports Med 1980;14:40–4. [15] Fullerton L, Snowdy H. Femoral neck stress fractures. Am J Sports Med 1988;16:365–77.

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[16] Monteleone G. Stress fractures in the athlete. Orthop Clin North Am 1995;26:423. [17] Stanitski C, McMaster J, Scranton P. On the nature of stress fractures. Am J Sports Med 1978;6:391–6. [18] Volpin R. Stress fractures of the femoral neck following strenuous activity. J Orthop Trauma 1990;4:394–8. [19] Provost R, Morris J. Fatigue fractures of the femoral shaft. J Bone Joint Surg Am 1969; 51A:487–98. [20] Milgrom C, Giladi M, Stein M. Stress fractures in military recruits. J Bone Joint Surg Br 1985;67B:732–5. [21] Muralikuttan K, Sankarart-kutty M. Supracondylar stress fracture of the femur. Injury 1999; 30:66–7. [22] Weber P. Salter-Harris II stress fracture in a young adult. Orthopaedics 1988;11:309–11. [23] Bailie D, Lamprecht D. Bilateral femoral stress fractures in an adolescent male runner. Am J Sports Med 2001;29:811–3. [24] Koch J. Laws of bone architecture. Am J Anat 1917;21:177–200. [25] Bennell K, Malcolm S, Thomas S, et al. Risk factors for stress fractures in track and field athletes. Am J Sports Med 1996;24:810–8. [26] Tuan K, Wu S, Sennett B. Stress fractures in athletes: risk factors, diagnosis, and management. Orthopaedics 2004;27:583–91. [27] Coady C, Micheli L. Stress fractures in the pediatric athlete. Clin Sports Med 1997;16: 225–36. [28] Boden B, Osbahr D, Jimenez C. Low-risk stress fractures. Am J Sports Med 2001;29: 100–11. [29] Oh I, Harris W. Proximal strain distribution in the loaded femur. J Bone Joint Surg Am 1978;60A:75–85. [30] Devas M. Stress Fractures of the femoral neck. J Bone Joint Surg Br 1965;47B:728–37. [31] Beck T, Ruff C, Shaffer R, et al. Stress fractures in military recruits: gender differences in muscle and bone susceptibility factors. Bone 2000;27:437–44. [32] Fullerton L. Femoral neck stress fractures. Injury Clinic 1990;9:192–7. [33] Shin A, Mortin W, Gorman J, et al. The superiority of magnetic resonance imaging in differentiating the cause of hip pain in endurance athletes. Am J Sports Med 1996; 24:168–76. [34] Korpelainen R, Orava S, Karpakka J, et al. Risk factors for recurrent stress fractures in athletes. Am J Sports Med 2001;29:304–10. [35] Giladi M, Milgrom C, Simkin A, et al. Stress fractures. Identifiable risk factors. Am J Sports Med 1991;19:647–52. [36] Braam L, Knapen M, Geusens P, et al. Factors affecting bone loss in female endurance athletes. Am J Sports Med 2003;31:889–95. [37] Provencher M, Baldwin A, Gorman J, et al. Atypical tensile-sided femoral neck stress fractures. Am J Sports Med 2004;32:1528–34. [38] Milgrom C, Chisin R, Marguiles J. Stress fractures of the medial condyle. J Trauma 1986; 26:199–200. [39] Ernst J. Stress fractures of the femoral neck. J Trauma 1964;4:71–83. [40] Deutsch A, Coel M, Mink J. Imaging of stress injuries to bone. Clin Sports Med 1997; 16:275–90. [41] Knapp T, Garrett W. Stress fractures: general concepts. Clin Sports Med 1997;16: 339–56. [42] Lynch S, Renstrom A. Groin injuries in sport. Injury Clinic 1999;28:137–44. [43] Maezawa K, Nozawa M, Sugitomo M. Stress fractures of the femoral neck in child with open capital femoral epiphysis. J Pediatr Orthop 2004;13:407–11. [44] Zwas S, Elkanovitch R, Frank G. Interpretation and classification of bone scintigraphic findings in stress fractures. J Nucl Med 1987;28:452–7. [45] El-Khoury G, Wehbe M, Bonfiglio M. Stress fractures of the femoral neck: a scintigraphic sign for early diagnosis. Skeletal Radiol 1981;6:271–3.

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[46] Greaney R, Gerber F, Laughlin R. Distribution and natural history of stress fractures in US Marine recruits. Radiology 1983;146:339–46. [47] Yildirim M, Gursoy R, Varoglu E. 99mTc-MDP bone SPECT in evaluation of the knee in asymptomatic soccer players. Br J Sports Med 2004;38:15–8. [48] Provan I, Murray C. The role of SPECT in the evaluation of skeletal trauma. Ann Nucl Med 1993;7:1–9. [49] Roub L, Gumerman L, Hanley E, et al. Bone stress: a radionuclide imaging perspective. Radiology 1979;132:431–8. [50] Craig J, Widman D, van Holsbeeck M. Longitudinal stress fracture: patterns of edema and the importance of the nutrient foramen. Skeletal Radiol 2003;32:22–7. [51] Kiuru M, Niva M, Reponen A, et al. Bone stress injuries in aymptomatic elite recruits. Am J Sports Med 2005;33:272–6. [52] Slocum K, Gorman J, Puckett M, et al. Resolution of abnormal MR signal intensity in patients with stress fractures of the femoral neck. AJR Am J Roentgenol 1997;168:1295–9. [53] Arendt E, Griffiths H. The use of MR imaging in the assessment and clinical management of stress reactions of bone in high-performance athletes. Clin Sports Med 1997;16: 291–306. [54] Narvaez JA, Narvaez J, Delama E, et al. Spontaneous osteonecrosis of the knee associated with tibial plateau and femoral condyle insufficiency fracture. Eur Radiol 2003;13: 1843–8. [55] McBryde A. Stress fractures in athletes. J Sports Med 1975;3:212–7. [56] Masters S. Stress fractures of the femoral shaft. Br J Sports Med 1986;20:14–6. [57] Leinberry C, McShane R, Stewart W. A displaced subtrochanteric stress fracture in a young amenorrheic athlete. Am J Sports Med 1992;20:485–7. [58] Visuri T. Stress osteopathy of the femoral head. Acta Orthop Scand 1997;68:138–41. [59] Lee C, Huang G, Chao K, et al. Surgical treatment of displaced stress fractures of the femoral neck in military recruits: a report of 42 cases. Arch Orthop Trauma Surg 2003; 123:527–33.

Clin Sports Med 25 (2006) 105–115

CLINICS IN SPORTS MEDICINE Stress Fractures Around the Knee Raymond R. Drabicki, MDa, William J. Greer, MDa, Patrick J. DeMeo, MDb,* a

Allegheny General Hospital, 320 East North Avenue, Pittsburgh, PA 15212, USA Department of Orthopedic Surgery, Allegheny General Hospital, 320 East North Avenue, Pittsburgh, PA 15212, USA b

S

tress fractures of the lower extremity are common, especially in the younger athletic population. The majority of these lower-extremity fractures are located in the femoral neck, tibial diaphysis, calcaneus, and metatarsals. Stress fractures around the knee (ie, the supracondylar distal femur, femoral condyles, proximal tibial and fibular metaphyses, and patella) occur with a lower incidence. The current literature consists mainly of a variety of case reports but is devoid of any sizeable series investigating knee stress fractures. Diagnosing a stress fracture around the knee can be a challenge. The proximity of the stress fracture to the knee joint may lead the clinician to investigate intra-articular or other periarticular pathology. The differential diagnosis can be large, including bursitis, tendonitis, mechanical causes, insufficiency fracture, and tumor. A high index of suspicion is necessary to confirm the underlying diagnosis. A patient's medical history combined with a physical examination and imaging modalities will aid the physician in arriving at the diagnosis of stress fracture.

PROXIMAL TIBIA Most tibial stress fractures occur posteromedially, along the popliteal-soleal line in the middle and distal third of the tibial diaphysis [1,2]. Although much less common, the proximal medial tibial condyle has been cited as an area subject to stress fracture. Insufficiency fractures of this area have been reported. These fractures are the result of bone that is deficient in strength that is loaded under normal physiologic conditions. Typically, elderly patients with osteoarthritis of the knee and postpartum female patients are at risk for the development of insufficiency fractures [3,4]. The incidence of proximal medial tibial condylar fatigue fractures is unknown. In contrast to the insufficiency fracture, the bone is normal and fails secondary to excessive and repetitive stress [5]. The typical patient is a distance runner [6]. Both intrinsic and extrinsic risk factors have been identified in runners, predis* Corresponding author. E-mail address: [email protected] (P.J. DeMeo). 0278-5919/06/$ – see front matter doi:10.1016/j.csm.2005.08.002

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posing them to fatigue fracture. Intrinsic risk factors include limb malalignment, cavus deformity, and a hyperpronated foot [7]. The primary extrinsic risk factor has been linked to a change in running conditions. Notably, uphill running significantly increases the compressive forces across the knee joint [8]. It is surmised that this sudden increase in load is the cause for the fatigue and failure of the underlying cancellous bone of the medial tibial condyle [9]. Physical examination reveals tenderness in proximity to the medial joint line. This tenderness, in association with a usually present effusion, may lead the clinician to believe that the patient has sustained an injury to the medial meniscus. In addition, the point of maximal tenderness is often close to the insertion of the pes anserinus. Thus, the diagnosis of pes anserinus bursitis also should be considered [9]. Provocative physical examination tests as well as diagnostic injections should be performed to rule out these other causes of medial tibial pain. Standard imaging, beginning with plain radiographs, should be obtained. Images should be scrutinized closely for any findings consistent with tumor. However, acute stress fractures illicit no radiographic findings. It has been suggested that interval radiographs will show changes consistent with stress fracture (eg, periosteal bone formation and thickening of the involved cortex). This diagnostic feature is not necessarily true for condylar fractures. Some cases have reported no radiographic evidence of fatigue fracture even after 4 months have elapsed since the onset of symptoms [9]. Although bone scanning has been advocated in the past, new magnetic resonance imaging has been advocated as the most sensitive test for diagnosing stress fracture. Fredericson and colleagues [10] have proposed an MRI grading system for tibial stress injury. Fat-suppression

Fig. 1. Fat-suppressed MRI, anteroposterior view. The bright area represents marrow edema associated with the fracture. (Adapted from Vossinakis IC, Tasker TP. Stress fractures of the medial tibial condyle. Knee 2000;7(3):187–90.)

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MR images often reveal significantly associated marrow edema in the presence of a medial tibial condyle fractures (Fig. 1). MRI not only assists with confirming the diagnosis, it also affords information regarding the extent of bony involvement and severity of the pathology. Once medial tibial condylar stress fracture has been diagnosed, treatment consists of educating the patient in avoiding the offending activity. Depending on the amount of marrow involvement, cessation of running may be advised for up to 6 months, with the initiation of lower impact training such as swimming or bicycling after 6 weeks [9]. There have been no reports of delayed union, nonunion, or displacement of proximal tibia medial condyle fatigue fractures. An increased awareness by a surgeon, a high level of clinical suspicion, and patient education are requisite for an optimal outcome. PROXIMAL FIBULA Only 10 reports of proximal fibula stress fracture in athletes were found at the time the literature search was performed for this article. However, there have been numerous reports of fatigue fracture in the military [11,12]. Fibular injuries were associated with repetitive jumping and subsequent landing in parachute school recruits. The incidence of fibular stress fractures in athletes has not been reported. Biomechanical studies have shown that the fibula receives between 6.4% and 16.7% of the load transmitted from the lower extremity. The relative decrease in load assumed by the fibula likely accounts for the rarity of this entity. The position of the foot and ankle when the foot is in contact with ground determines the force transmitted. With the foot in an inverted, plantar-flexed position, the load to the fibula is diminished. However, with the foot in an everted, dorsiflexed position, increased force is transmitted to the fibula. Repeated forceful contraction of the soleus and biceps femoris while the fibula is loaded with the foot in forced dorsiflexion has been postulated as the mechanism that causes fatigue fractures of the proximal fibula [13–15]. Similar to the tibia, diagnosis is predicated on a medical history and physical examination. Plain radiographs, bone scannning, and MRI are useful confirmatory adjunct studies. Although bone scanning is sensitive, MRI has a greater specificity for stress fracture [16]. The value of MRI is its ability to differentiate between stress fracture and sarcoma. Once the diagnosis of proximal fibular stress fracture is obtained, conservative treatment is undertaken. PATELLA Stress fractures of the patella are exceedingly rare. The first cases appearing in the orthopedic literature were presented by Devas [17] and Müller [18]. Despite the paucity of information on patellar stress fractures available in orthopedic literature, the rare occurrence of this condition has been seen predominantly in two patient populations, young athletes [18–25] and cerebral palsy patients [26–28].

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As found in the literature, patellar stress fractures present with pain, swelling, and localized tenderness in the anterior knee that resolves with periods of rest or immobilization. Often these stress fractures go undetected. On resuming high performance athletic activity, these patients often relapse and experience similar symptoms. In most reports, these stress fractures were not discovered until there was separation of the proximal and distal fragments. Athletes reported a crack or pop sensation in the absence of direct trauma, with immediate anterior knee pain and the variable ability to bear weight and extend at the knee. Fig. 2 shows a nondisplaced, transverse patellar stress fracture in a weight lifter who was performing a squat when the patella failed. After this stress fracture occurred, the patient was unable to bear weight or perform a straight leg raise. The patella is the largest sesamoid bone in the body and begins its ossification process in the third year of life. Ossification is completed before or during puberty. However, segmentation of the patella may persist. Most frequently, a bipartite patella exists at the superolateral portion of the patella. This entity can be confused with a patellar stress fracture because it also may cause pain in the adolescent athlete. The diagnosis of patellar stress fracture can be misleading. In children, early bony reparative responses conceal stress fractures, and often, the early callus can be misinterpreted as a neoplasm or infection [29]. In a review of 8542 primary bone tumors, only 0.06% occurred in the patella. These rare and often benign neoplasms are virtually always radiographically apparent on presentation, and in the presence of fracture, the diagnosis of pathologic fracture should be made [25]. In patients who have osteoporosis or osteomalacia, fractures of the patella are often secondary to weakened bone caused by an underlying disorder.

Fig. 2. Radiograph obtained at the initial office visit demonstrates a nondisplaced transverse fracture of the patella. (From Mayers LB, Khabie V, Castorina R, et al. Acute transverse patellar fracture associated with weightlifting: case report and literature review. Am J Sports Med 2001;29(2):232–3; with permission.)

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This type of stress fracture has been termed an insufficiency fracture. In addition, patellar fractures that occur after resurfacing in total knee arthroplasty are also the result of bone weakening and hence can be classified as insufficiency fractures. Patellar stress fractures in athletes and cerebral palsy patients often occur in previously normal bone that has become fatigued and weakened by the forces exerted on the patella in the absence of direct trauma. This second type of stress fracture has been referred to as a fatigue stress fracture. The radiographic appearance of a patellar stress fracture is marked by sclerotic edges, in contrast to traumatic patellar fractures, which characteristically occur in the middle one third, lack sclerotic edges, and display significant comminution [29]. The medial and lateral patellar retinaculum is often intact in stress fractures, thus complicating diagnoses secondary to lack of displacement. Stress fractures of the patella occur predominantly at the junction of the middle and distal one third of the patella. At this transitional site, the most distal fibers of the quadriceps and the most proximal fibers of the patellar tendon insert on the anterior patella [29]. Although they can be longitudinal or transverse in nature, the most frequent orientation of patellar stress fractures is in the transverse plane [25]. Initial radiographs are sensitive in only one third to one half of patients [30]. Hence, more sensitive studies such as bone scans have been advocated for detecting progressive damage before the completion of a stress fracture [19,21,23]. Early diagnosis in such cases is of significant value, providing more conservative treatment plans. Alternatively, serial radiographs at short intervals may prove to be beneficial. The mechanism of patellar stress fracture can be attributed to the mechanical stresses placed on the patella by the extensor mechanism and the cellular response to physical stress. The location of the patella within the extensor mechanism compresses its articular surface against the trochlea and condyles of the femur. This patellofemoral compression force, which is a resultant force vector (consisting of the force vectors invoked by the quadriceps and patellar tendons), is equal in magnitude to the patellofemoral joint reactive forces throughout the range of knee flexion and extension. The patellofemoral joint reactive forces are a function of knee flexion angle and quadriceps force. With each increased degree of knee flexion, there is a corresponding 6% increase in the patellofemoral joint reactive force [31]. When a person is standing in a position of 30° of flexion, the quadriceps force required to maintain this position and stabilize the knee is 210% of body weight. Perry and colleagues [32] also found the necessary quadriceps force required to produce this stabilization equaled only 50% of the average maximum quadriceps strength. The compressive forces incurred on the articular surface of the patella are transmitted to the anterior surface through a three-point bending mechanism. This three-point bending stress coupled with the axial tension applied by the quadriceps and patellar tendons on the anterior patella have been examined with finite elemental analysis and microradiographic studies. These studies have

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demonstrated that the trabecular bony architecture conforms to the direction of linear stress and the trabecular density is related to the magnitude of applied stress [22]. As a result, it has been postulated that these forces are directly responsible for the propagation of stress fractures in the patella [19,22]. Stress fractures of the patella occur secondarily to mechanical stress and changes at the cellular level. Repetitive, cyclic loading of the patella results ultimately in damage at the microstructural level, which renders the patella prone to a stress fracture. Despite the submaximal intensity of these tensile forces to cause failure of the patella, their accumulation results in alterations in the bone reparative process [19,20,22]. The dynamic process of osteoclastic resorption and osteoblastic bone formation are skewed in such a manner that bone resorption exceeds formation in the presence of frequent stress loading [33,34]. This alteration in bone remodeling decreases the strength of the patellar bone stock and, thereby, decreases the threshold of failure. Alternatively, fatigue fractures of the patella may occur with shorter periods of repetitive loading if the applied stress is increased. This is likely the manner in which stress fractures manifest in weight lifting athletes [19,22,35]. Historically, nondisplaced patellar fractures have been treated conservatively. Casting or bracing in knee extension and activity modification have been the mainstays of treatment [21,24,29]. Progression to passive range of motion exercises, quadriceps strengthening and unrestricted activity has been advocated after a 4- to 6-week immobilization period. Alternatively, some authors have advocated an open reduction and internal fixation procedure for treating minimally displaced fractures [19,20,22,36]. This procedure enables the patient to return to normal activities and often eliminates the need for postoperative bracing [29]. However, delayed separation of the fragments has been observed with cast immobilization [17,37]. Open reduction and internal fixation has been universally accepted as the gold standard for treatment of widely displaced fatigue fractures with or without disruption of the extensor mechanism in the young athlete [20,22]. TIBIAL TUBERCLE The tibial tubercle has been identified as an area affected by stress fracture. Osgood-Schlatter disease has been implicated as a predisposing factor for developing a stress fracture [38]. Repetitive stress transmitted to the tubercle through contraction of the extensor mechanism is believed to cause separation of the cartilaginous and osseous structures in the anterior aspect of the tibia [39,40]. However, by the time of skeletal maturity, the interposing tissue ossifies, giving the appearance of an “overgrowth” of the tibial tubercle. Conservative treatment is the norm. In the instance when the cumulative stress applied to the tubercle exceeds the tensile load to failure, acute avulsion of the tubercle may be precipitated. In this setting, open reduction and internal fixation is the gold standard for all but the smallest of undisplaced fragments. Numerous cases have been described, all with the common characteristic of the skeletally immature patient [41,42].

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Fig. 3. Axial T2-weighted MRI of the right tibia demonstrates linear enhancement at the base of the tibial tubercle (arrows) and edema in the surrounding cancellous bone and tibial tubercle (arrowheads), consistent with a tibial tubercle stress fracture. (Adapted from Tejwani SG, Motamedi AR. Stress fracture of the tibial tubercle in a collegiate volleyball player. Orthopedics 2004;27(2):219–22; with permission.)

One report [43] exists of a stress fracture of the tibial tuberosity in a skeletally mature individual. This patient had a history of Osgood-Schlatter disease, which responded to conservative therapy in his youth. Five years after skeletal maturity, while continuing his regular active lifestyle as a collegiate volleyball player, the patient presented with a 3-month history of anterior knee pain. Plain radiographs were difficult to interpret because of the overgrowth of the tuberosity.

Fig. 4. Sagittal T1-weighted MRI reveals an intact patellar tendon without signs of tearing, degeneration, or calcification. (Adapted from Tejwani SG, Motamedi AR. Stress fracture of the tibial tubercle in a collegiate volleyball player. Orthopedics 2004;27(2):219–22; with permission.)

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A provisional diagnosis of patellar tendonitis was made. Without achieving improvement after a prolonged course of conservative treatment modalities, MR images were obtained which confirmed the diagnosis of tubercle stress fracture (Figs. 3 and 4). The authors recommended that stress fractures should be suspected in patients with presumed patellar tendonitis, who do not respond to conservative therapy in the face of an atraumatic history [43]. DISTAL FEMUR The incidence of distal femoral stress fractures in the civilian athletic population is unknown. Various cohort studies have analyzed the occurrence of stress fractures in military recruits. An Israeli study documented that 9.2% of recruits who suffered from any stress fracture sustained a stress fracture to the distal femur. None of these recruits experienced any symptoms before basic training [44]. The diagnosis of femoral stress fractures should be kept in mind when a patient presents with a complaint of vague knee pain. A case report [45] has documented the iatrogenic completion of a supracondylar stress fracture caused by stressing the leg in an arthroscopic leg holder. At initial presentation, the patient reported a 1-week history of knee pain, which failed to improve after he stopped training. After a course of conservative therapy without relief of

Fig. 5. MRI of the left knee before initial arthroscopic surgery was performed. Coronal fatsuppressed image with a medial supracondylar line of low signal intensity and a surrounding intramedullary and periosteal edema of high signal intensity are shown. (From Huber W, Treib K. Serious consequences of the wrong diagnosis of meniscal lesion in a case of stress fracture of the distal femur. Arthroscopy 2002;18(8):935–8; with permission.)

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Fig. 6. MRI of a transverse fracture of the femur, 8 cm proximal to the knee joint. (Adapted from Huber W, Treib K. Serious consequences of the wrong diagnosis of meniscal lesion in a case of stress fracture of the distal femur. Arthroscopy 2002;18(8):935–8.)

symptoms, an MRI was obtained that reported a degenerative meniscal tear. An increased signal on T2-weighted MRI located in the supracondylar region of the femur was overlooked (Fig. 5). The patient underwent arthroscopy for a presumed medial meniscal tear, which resulted in completion and displacement of his supracondylar stress fracture. The post-arthroscopy MRI showed a transverse fracture of the femur (Fig. 6). Although it is presumed to occur rarely, a stress fracture of the distal femur must be placed on the differential for nonspecific knee pain. MRI imaging should be scrutinized for the possibility of stress fracture. SUMMARY Stress fractures around the knee present a taxing entity for the orthopedic surgeon. Because these fractures have a low incidence, the surgeon must have a high index of suspicion when presented with a patient with knee pain supported by a history of “overuse.” The treatment of the majority of these stress fractures is conservative in nature. Rest with gradual return to training will optimize outcomes. In the event of fracture completion or displacement, standard AO principles apply. Identification of the pathology, not necessarily the treatment, is the challenge to the physician. References [1] Ekenman I, Halvorsen K, Westbald P, et al. Local bone deformation at two predominant sites for stress fractures of the tibia: an in vivo study. Foot Ankle Int 1988;19:479–84. [2] Daffner RH, Martinez S, Gehweiler Jr JA, et al. Stress fractures of the proximal tibia in runners. Radiology 1982;142(1):63–5. [3] Yang K, Yeo S, Lo N. Stress fracture of the medial tibial plateau after minimally invasive unicompartmental arthroplasty: a report of 2 cases. J Arthroplasty 2003;18(6):801–3. [4] Clemetson IA, Popp A, Lippuner K, et al. Postpartum osteoporosis associated with proximal tibial stress fractures. Skeletal Radiol 2004;33(2):96–8.

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[5] Boden BP, Speer KP. Femoral stress fractures. Clin Sports Med 1997;16(2):307–17. [6] Devas MB. Stress fractures of the tibia in athletes or “shin soreness”. J Bone Joint Surg Br 1958;40B:227–39. [7] Ekenman I, Tsai-Fellander L, Westbald P, et al. A study of intrinsic risk factors in patients with stress fractures of the tibia. Foot Ankle Int 1996;17:477–82. [8] Beck BR. Tibial stress injuries: an aetiological review for the purposes of guiding management. Sports Med 1998;26:265–79. [9] Vossinakis IC, Tasker TP. Stress fractures of the medial tibial condyle. Knee 2000;7(3): 187–90. [10] Fredericson M, Bergman AG, Hoffman KL, et al. Tibial stress reaction in runners: correlation of clinical symptoms with a new magnetic imaging grading system. Am J Sports Med 1995;23:472–81. [11] Symeonides PP. High stress fractures of the fibula. J Bone Joint Surg Br 1980;62B:192–3. [12] Lord CD, Coutts JW. A study of typical parachute injuries occurring in two hundred and fifty thousand jumps at the parachute school. J Bone Joint Surg Br 1971;26B:547–53. [13] Goh JC, Mech AM, Lee EH, et al. Biomechanical study on the load-bearing characteristics of the fibula and the effects of fibular resection. Clin Orthop 1996;16:578–84. [14] Lambert KL. The weight-bearing function of the fibula: a strain gauge study. J Bone Joint Surg Am 1971;53A:507–13. [15] Takebe K, Nakagawa A, Minami H, et al. Role of the fibula in weight-bearing. Clin Orthop 1984;184:289–92. [16] Lehman TP, Belanger MJ, Pascale MS. Bilateral proximal third fibular stress fractures in an adolescent female track athlete. Orthopedics 2000;25(3):329–32. [17] Devas MB. Stress fractures of the patella. J Bone Joint Surg Br 1960;42B(1):71–4. [18] Müller W. Der militarische Abrissermudungsschaden [The fatigue tear injuries in the military]. Deutsch Militararzt 1943;8:283–6 [in German]. [19] Brogle PJ, Eswar S, Denton JR. Propogation of a patellar stress fracture in a basketball player. Am J Orthop 1997;26(11):782–4. [20] Jerosch JG, Castro WH, Jantea C. Stress fractures of the patella. Am J Sports Med 1989; 17(4):579–80. [21] Piétu G, Hauet P. Stress fracture of the patella. Acta Orthop Scand 1995;66(5):481–2. [22] Tietz CC, Harrington RM. Patellar stress fracture. Am J Sports Med 1992;20(6):761–5. [23] Rockett JF, Freeman III BL. Stress fracture of the patella: confirmation by triple-phase bone imaging. Clin Nucl Med 1990;15(12):873–5. [24] Dickason JM, Fox JM. Fracture of the patella due to overuse syndrome in a child: a case report. Am J Sports Med 1982;10:248–9. [25] Mason RW, Moore TE, Walker CW, et al. Patellar fatigue fractures. Skeletal Radiol 1996; 25:329–32. [26] Kaye JJ, Freiberger RH. Fragmentation of the lower pole of the patella in spastic lower extremities. Radiology 1971;101:97–100. [27] Mann M. Fatigue fracture of the lower patellar pole in adolescents with cerebral movement disorders. Z Orthop Ihre Grenzgeb 1984;122:167. [28] Rosenthal RK, Levine DB. Fragmentation of the distal pole of the patella in spastic cerebral palsy. J Bone Joint Surg Am 1977;59A:934–9. [29] Mata SG, Ovejero AH, Grande MM. Transverse stress fracture of the patella in a child. J Pediatr Orthop 1999;8(3):208–11. [30] Norfray JF, Schlacteri L, Kernahan WT. Early confirmation of stress fractures in joggers. JAMA 1980;243:1647–9. [31] Reilly DT, Martens M. Experimental analysis of the quadriceps muscle force and patellofemoral joint reaction force for various activities. Acta Orthop Scand 1972;43:126–37. [32] Perry J, Antonelli D, Ford W. Analysis of knee-joint forces during flexed-knee stance. J Bone Joint Surg Am 1975;57A:961–7. [33] Johnson LC, Stradford HT, Geis RW. Histogenesis of stress fractures. J Bone Joint Surg Am 1963;45A:1542.

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[34] Li G, Zhang S, Chen G, et al. Radiographic and histologic analysis of stress fracture in rabbit tibias. Am J Sports Med 1985;13:285–94. [35] Mayers LB, Khabie V, Castorina R, et al. Acute transverse patellar fracture associated with weightlifting: case report and literature review. Am J Sports Med 2001;29(2):232–3. [36] Hanel DP, Burge RE. Consecutive indirect patella fractures in an adolescent basketball player. Am J Sports Med 1981;9(5):327–9. [37] Oginni LM. Stress fracture of the patella in a palmwine tapper. Tropical and Geographical Medicine 1993;45(1):37–8. [38] Ogden JA, Tross RB, Murphy M. Fractures of the tibial tuberosity in adolescents. J Bone Joint Surg Am 1980;62A:205–15. [39] Osgood RB. Lesions of the proximal tibial tubercle occurring during adolescence. Boston Med Surg J 1903;148:114–7. [40] Schlatter C. Verletzenger des schnabelformigen fortsatzes der oberen tibiaeepiphyses [Injuries to the tibial tuberosity]. Beitr Klin Chir 1903;38:874–87. [41] Deliyannis SN. Avulsion of the tibial tuberosity: report of two cases. Injury 1974;4:341–4. [42] Levi JH, Tross RB, Murphy M. Fractures of the tibial tubercle. Am J Sports Med 1976;4: 254–63. [43] Tejwani SG, Motamedi AR. Stress fracture of the tibial tubercle in a collegiate volleyball player. Orthopedics 2004;27(2):219–22. [44] Milgrom C, Giladi M, Stein M, et al. Stress fractures in military recruits: a prospective study showing an unusually high incidence. J Bone Joint Surg Br 1985;67B(5):732–5. [45] Huber W, Treib K. Serious consequences of the wrong diagnosis of meniscal lesion in a case of stress fracture of the distal femur. Arthroscopy 2002;18(8):935–8.

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CLINICS IN SPORTS MEDICINE Evaluation and Treatment of Tibial Stress Fractures Andrea J. Young, MDa,*, David R. McAllister, MDb a

Pacific Sports Medicine at MultiCare, 3315 S. 23rd Street, Suite 200, Tacoma, WA 98405-1616, USA Department of Orthopaedics, University of California Los Angeles, 10833 LeConte Avenue, Box 956902, Los Angeles, CA 90095-6902, USA b

M

any individuals participate in recreational and professional activities each year. The health benefits are many: improved cardiovascular structure and decreased body weight, cholesterol, triglycerides, glucose, and systemic blood pressure. With the beneficial health effects, however, come overuse injuries. Stress fractures are a relatively common injury in athletes, and the amount of time lost from sports can be considerable. Stress fractures can have devastating consequences, even when they are treated. First reported in 1855 by Briethaupt in Prussian soldiers, stress fractures are common injuries in athletes and military recruits. The reported incidence of fractures ranges from as low as 1% to up to 20% of sports injuries [1]. In military recruits, the incidence may be 5% to 12% depending on the study [2]. Certain sports, such as running, also have a higher incidence. In a review of 320 athletes, the most common stress fracture location was the tibia (49.1%), followed by the tarsals (25.3%) and metatarsals (8.8%) [1]. This high incidence of tibial stress fractures was confirmed in a more recent study that found that they occurred in the tibia in 40.3% of athletes who had stress fractures [3]. There is also some evidence to suggest that female athletes may be at more of a risk than their male counterparts for a given sport. In a recent study on runners, 56 of the 99 (57%) tibial stress fractures occurred in women [4]. There has been increased awareness of tibial stress fractures and improvement in the diagnosis of such injuries with the use of MRI. This imaging modality has led to increased attention to this problem, and new strategies are emerging to improve treatment and prevention. PATHOPHYSIOLOGY There have been a number of studies trying to identify risk factors for stress fractures [5–10]. Younger age and gender have been shown to increase the risk of stress fractures [1,3,4]. Other biomechanical risk factors may also exist. In a

* Corresponding author. E-mail address: [email protected] (A.J. Young). 0278-5919/06/$ – see front matter doi:10.1016/j.csm.2005.08.015

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study of military recruits, Giladi and colleagues [11] found that only tibial bone width and increased external rotation of the hip increased the risk of tibial stress fractures. These variables were independent and cumulative. In this specific population, the incidence of tibial stress fractures was 17% without either risk factor and 45% when both risk factors were present. Other investigators have found that acute weight loss may be a significant contributing risk factor [2]. DIAGNOSIS Symptoms vary and may be vague in nature. Athletes may complain of insidious onset of leg pain after a period of weight-bearing activity. As the stress fracture progresses, patients may begin to have pain on ambulation or even at rest. They may not report a change in workout regimen, so further questioning on this issue is important. The physical examination may reveal a specific location of tenderness. There may be swelling and, in chronic cases, a palpable callus. It is important to assess for leg alignment and leg-length discrepancy. The compartments should be palpated and a thorough neurovascular examination completed. The differential diagnosis for stress fracture is extensive and may include muscle strain, medial tibia stress syndrome (shin splints), stress reaction, periostitis, infection, bursitis, neoplasm, and exertional compartment syndrome or nerve entrapment. A few of these deserve further explanation. Stress reaction is a weakened bone due to the osteoclastic activity stimulated by exercise. The bone is weak but not significantly biomechanically disrupted. Stress reaction may or may not progress into a clinical stress fracture. Exercise-induced compartment syndrome also occurs during activity and is relieved with rest but is described as more of a tight or tired feeling, with burning rather than the pain typical of stress fractures. In unusual cases, some of these other diagnoses may coexist with a tibial stress fracture. IMAGING Plain radiographs are usually normal early in the disease process. In advanced lesions, radiographs may reveal periosteal reaction, new bone formation, or even a distinct fracture line. Radiographs may remain normal for several weeks, even in the face of continued symptoms. If a stress fracture is suspected based on the history and physical examination, then a period of rest followed by repeat radiographs or advanced imaging is necessary. If repeat radiographs obtained in 2 to 3 weeks after the onset of symptoms are still negative but the athlete continues to have symptoms, then advanced imaging maybe required. Bone scans have long been considered the standard for diagnosing stress fracture. Acute stress fractures show increased uptake in all three phases of a technetium 99m diphosphonate bone scan. During healing, phase 1 (flow phase) normalizes first, followed by phase 2 (blood-pool phase). Phase 3 (delayed phase) images gradually decrease in intensity over a period of months to years as the bone remodels. Bone scan is therefore not a useful tool to monitor healing progress. Bone scans may be positive in other conditions, making it less specific.

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Soft tissue injuries are generally distinguishable by increased uptake in only phases 1 and 2; shin splints have increased signal only in the delayed-phase images. Bone scan, however, cannot distinguish between other conditions such as infection or neoplasm. In addition to this lack of specificity, bone scan may be overly sensitive to bone strain. The increased signal in focal remodeling or stress reaction may be interpreted as stress fracture but may not have the same natural history. MRI has emerged as an excellent diagnostic modality for stress fractures. It has a higher specificity and may be more useful in grading lesions and, therefore, guiding treatment options. A grading system (Table 1) has been proposed by Fredrickson and colleagues [12]. Grade 1 stress fracture or reaction shows up in the short T1 inversion recovery images, with edema only in the periosteum. This fracture corresponds clinically to periostitis or shin splints. As the process advances, the T2 and T1 sequences become positive. The marrow begins to show edema, followed by a clearly visible fracture line in grade 4 (Fig. 1). It has been suggested that grade 1 and grade 2 lesions are less symptomatic, allowing return to sport after 4 to 6 weeks. Patients who have grade 3 or 4 lesions usually have symptoms with daily ambulation and require more time for healing [12]. MRI not only has the advantage of more clearly defining the extent of marrow edema but may also detect clinically insignificant lesions. It has been suggested that tibial injuries that result in ultimate failure of the involved bone be classified as stress fractures, whereas those that exhibit evidence of remodeling be classified as stress reactions [12]. Bergman and colleagues [13] noted that 43% of their 21 asymptomatic runners had radiographic findings of tibial stress reactions on MRI. None progressed to be symptomatic. This finding was confirmed in a subsequent study that found that only 1 in 25 stress reactions progressed to be symptomatic [14]. Therefore, careful correlation between MRI findings and symptoms is necessary. Table 1 Grading system for radiographs, bone scan, and MRI Grade

Radiographs

Bone scan

MRI

1

Normal

Mild uptake

2

Normal

Moderate uptake Increased lesion size

3

± Periosteal reaction

4

Fracture or periosteal reaction

Significantly increased uptake Bicortical increased activity

Positive STIR Mild periosteal edema Positive STIR and T2 Moderate to severe periosteal edema Marrow edema on T2 Positive T1 Marrow edema on T1/T2 Discrete fracture line

Abbreviation: STIR, short T1 inversion recovery.

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Fig. 1. Sagittal T2 fat saturation showing diffuse marrow edema. (A) Sagittal showing diffuse marrow edema. (B) Axial image with cortical edema.

Dual energy absorptiometry (DEXA) scans can be a useful tool in identifying those athletes who have low bone mass and, therefore, theoretically have increased risk of stress fractures. The diagnosis of osteopenia per the Word Health Organization is a bone density less than 1 standard deviation below the standard age-matched control. Osteoporosis is defined as greater than 2.5 standard deviations below the standard age-matched control. Marx and colleagues [15] did a retrospective analysis of athletes diagnosed with a stress fracture and evaluated the DEXA results. They found that 8 of the 9 cancellous stress fractures had osteopenia, but only 3 of the 11 cortical stress fractures had an abnormal DEXA. They concluded that DEXA should be performed in athletes who have cancellous stress fractures and in those who have risk factors. It is unclear at this time whether DEXA scans could be used as a predictive tool in screening athletes at risk. TREATMENT After the diagnosis of tibial stress fracture has been made by history, physical examination, and imaging modalities, treatment needs to be initiated. The typical tibial stress fracture that occurs on the posteromedial portion of the tibia usually responds to a period of rest followed by gradual resumption of activities. It is also important to identify and modify any risk factors. Training regimen and footwear are easily correctable. Intrinsic causes such as nutritional, hormonal, or other medical abnormalities also need to be addressed. Female athletes need to be evaluated for eating disorders, amenorrhea, or oligomenorrhea and for decreased bone density. Replacing estrogen returns the female athlete to a normal menstrual state and will likely improve bone mineral density.

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Athletes who have multiple stress fractures or those who have delayed healing should also have a thorough medical evaluation and a DEXA scan. Many practitioners divide treatment options based on the personality of the fracture. The typical posteromedial stress fracture is considered lower risk, whereas the anterior or “dreaded black line” stress fractures are considered higher risk. Low-risk fractures respond to rest for 2 to 6 weeks, with progressive return to activities. After the rest period, if the athlete is pain-free, then low-impact activities such as biking and swimming may be initiated. If the site continues to be asymptomatic, then higher-impact activities may gradually be reintroduced. This process can take several months. If symptoms return, then the athlete may need to decrease activities again. Most posteromedial stress fractures heal in 1 to 2 months, but return to play may take 3 to 4 months on average. Not all of these so-called “low-risk fractures,” however, respond favorable to rest. More uncertain than a period of decreased activity is the weight-bearing status. Intuitively, it makes sense that when an athlete has pain with activities of daily living, he or she should be non–weight bearing or partial weight bearing to decrease the force seen on the tibia. There have been no good studies to date showing that weight-bearing status affects the rate of healing. There have been several studies that have investigated the role of pneumatic braces. In one study, a small number of athletes were able to continue to compete with the pneumatic brace, and 11 of 13 became asymptomatic within 1 month despite the continued strain on the tibia [16]. In a randomized prospective study, Swenson and colleagues [17] found that patients who wore the pneumatic brace returned to activity significantly faster than patients whose fractures were treated only with rest. There are two proposed mechanisms as to how pneumatic leg braces aid healing. The first is the decreased force seen by the tibia due to the structural support. The second is that the brace causes venous congestion, increasing interstitial fluid, thereby increasing the electronegative charge. This electronegative charge has been shown to increase bone healing [10]. Others propose the use of bone stimulators, although there are no conclusive data that this treatment improves or accelerates healing. Clinical investigation continues into the role of medications. It has been well established that those who have nutritional deficiencies should take supplemental calcium (1500 to 2000 mg/d) along with vitamin D. Female athletes who are amenorrheic or oligomenorrheic should have supplemental estrogen to return them to a eumenorrheic state. Recently, investigators looked into the role of bisphosphonates in treating stress fractures. Bisphosphonates such as pamidronate have long been used to treat patients who have osteoporosis and those who have insufficiency fractures (normal stress on abnormal bone). Bisphosphonates bind to hydroxyapatite crystals in bone and may block dissolution of the matrix by osteoclasts, which may allow the balance to tip back in favor of bone formation. In a small study of five collegiate-level athletes, subjects were treated with intravenous pamidronate administered weekly [18]. Four were able to continue training and competing within 1 week of initiating therapy, the other

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missed only 3 weeks of training. These results suggest that pamidronate may be a useful adjuvant therapy. In another study, military recruits were prophylactically administered risedronate to determine whether it could prevent stress fractures in this high-risk population [19]. There was no statistically significant difference in the total stress fracture incidence between the treatment and placebo groups. More research into the role of bisphosphonates for the treatment and prevention of stress fractures is clearly needed. Researchers are investigating other medications that may promote healing. It is unclear whether other hormones may play a role in prevention or treatment of stress fractures. In a rat femoral osteotomy model after pin fixation, human parathyroid hormone was noted to accelerate fracture healing [20]. It is not known what role, if any, parathyroid hormone may have in accelerating healing in human stress fractures. There are no clinical studies that have evaluated the safety of nonsteroidal anti-inflammatory drugs (NSAIDs) on stress fracture healing. Animal studies suggest that NSAIDs may decrease healing in complete fractures; therefore, cautious use of NSAIDs for stress fractures is warranted [21]. Other modalities such as pulsed ultrasound have been proposed. In a recent study, Rue and colleagues [22] performed a prospective randomized doubleblind study of 43 tibial stress fractures randomized to pulsed ultrasound or placebo. The patients in the pulsed ultrasound group did not have a significant reduction in healing time. Despite rest, stress fractures can often progress or fail to heal. Chronic stress fractures (as indicated by a fracture line visualized on plain radiographs, the dreaded black line, sclerosis, or cyst formation) often do not respond to conservative treatment and require surgical intervention. In addition, some practitioners advocate surgery for high-level athletes to minimize time lost, with the assumption that return to play may be allowed sooner. Currently, the surgical intervention of choice is intramedullary fixation. Surgery is not without risks. Aside from the risk of infection, there may be pain at the insertion site and completion of fracture despite the intramedullary device. Support for intramedullary nailing is largely based on case reports. In 1996, Chang and Harris [23] reported on five athletes treated with intramedullary nailing for chronic tibial stress fractures. These military recruits had failed 1 year of conservative treatment. All had significant canal narrowing and thickened anterior cortex with a linear transverse lucent line. After intramedullary nailing, all had good to excellent results. A case report in 2004 [24] highlights the fallibility of intramedullary nailing. In the reported case, a collegiatelevel athlete underwent surgery after failure of 10 months of conservative treatment. He was asymptomatic and returned to play 6 weeks later. Shortly thereafter, he had acute pain at the fracture site. Radiographs revealed a spiral fracture centered at the previous fracture site. The anterior fracture or dreaded black line deserves additional mention. This tension fracture may be fundamentally different from other tibial stress fractures. It is on the anterior tension side of the bone and has shown a proclivity

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Fig. 2. Anterior tibial stress fracture dreaded black line.

for delayed healing. The radiographic appearance is a thickened anterior cortex with a lucent line in the anterior midshaft tibia (Fig. 2). It has been proposed that this area may be hypovascular, which predisposes it to delayed or nonunion. This fracture may also not have the same presenting history and may be minimally symptomatic despite nonunion [25]. It is this fracture pattern that has been suggested to benefit from intramedullary fixation; however, intramedullary fixation does not guarantee healing and has the additional risk of the surgery itself. Not all anterior stress fractures need to be addressed surgically; conservative management still plays an important role. Rettig and colleagues [26] found that seven of eight basketball players who had anterior stress fractures achieved union with rest and electrical stimulation, with a mean treatment time of 8.7 months and return to sports at a mean of 12.7 months. In a more recent case series of three patients with delayed healing of anterior midtibial stress fractures, Batt and coworkers [27] reported successful healing in all three in a mean of 8 months with use of a pneumatic leg brace. These reports suggest that although surgical intervention may become necessary, conservative measures may still be successful and should be considered.

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PREVENTION Perhaps more important than treatment is prevention of such injuries. The most important factor is education of athletes and coaches as to the importance of a training regimen to prevent overuse injuries. Despite this awareness, there may be a number of athletes who continue to be at risk. Numerous researchers have investigated the role of orthotics in the prevention of stress fractures. Recently, Ekenman and colleagues [28] took in vivo tibial strain measurements in five military recruits. They found that tibial strain was not significantly reduced with the use of soft or semirigid orthotics while running. Others maintain that the increased cushion and improved mechanics can minimize the stresses seen. Preparticipation history and physical examination are important tools for identifying athletes at risk. Those who have a history of multiple stress fractures, amenorrhea, oligomenorrhea, or disordered eating deserve further evaluation. CASE EXAMPLES The authors’ institution has had considerable experience with tension-sided tibial stress fractures in competitive athletes. This fracture has been found to be difficult with respect to bony healing. Tibial nailing has been successful in some but not all athletes who have this condition. There is no single algorithm that can drive treatment decisions. As the following case examples illustrate, each athlete must be individually assessed, and treatment and work-up decisions must be made based on the unique characteristics of the fracture and the athlete. Case 1 An elite-level gymnast began having begun having pain in her tibia at age 17 years. MRI confirmed an anteromedial tibial stress fracture. After continued symptoms despite conservative treatment, she underwent intramedullary nailing. Her symptoms improved after a period of recovery, but she continued to have localized pain despite rest and use of a bone stimulator. Nutritional factors were addressed, as was her oligomenorrhea. Radiographs showed no evidence of healing, and she underwent exchange intramedullary nailing 3 years after her initial symptoms (Fig. 3). Her symptoms improved and the nail was removed several months later due to pain at the insertion site. She was able to compete on a limited basis only. Radiographs continued to show lack of complete healing, and with resumption of full activities, her symptoms recurred. One year later, an intramedullary nail was again placed due to concerns for catastrophic failure should full-impact activities continue. In the postoperative period, she gradually improved until approximately 6 weeks after surgery. At that time, she began having increased pain and swelling, which resolved with a period of non–weight bearing. Three months after her third intramedullary nail, radiographs showed lysis and scalloping around the nail that were not present in radiographs taken 2 months previously. Despite systemic or local symptoms, the radiographic appearance suggested an indolent

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Fig. 3. (A,B) Intramedullary nailing for anterior stress fracture.

infection. She therefore underwent removal of the nail with debridement; cultures were positive for a Bacillis species. She was treated with 6 weeks of intravenous antibiotics, with normalization of her sedimentation rate. After an extended period of cross-training, the gymnast gradually increased her activities until she was able to tolerate full participation, almost 5 years after her first symptoms occurred. Of interest, complete union of the fracture did not occur until after the infection was treated (Fig. 4).

Fig. 4. Healed stress fracture after removal of intramedullary nail and treatment of infection. (A) AP view. (B) Lateral view.

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Case 2 An 18-year-old elite collegiate soccer player presented to the athletic trainers with a 7-month history of left shin pain. She had a history of a previous left tibial stress fracture at age 16 years that had resolved after a period of rest; no other medial problems were noted. On examination, there was a palpable mass midshaft tibia that was painful to palpation. Radiographs revealed an anteromedial stress fracture with some callus formation. Treatment options were discussed and symptoms improved after a period of activity modification. Later that season, she was hit in the left leg during a game and had acute pain and deformity at the stress fracture site. Radiographs confirmed a complete fracture through the anterior stress fracture (Fig. 5). She was treated with intramedullary fixation. Radiographs continued to show lack of healing at the fracture site, so 4 months later, the nail was dynamized and 2 months after that she was able to return to soccer. The fracture did not heal and she continued to have some symptoms with any increase in her activities. She was unable to fully return to soccer at that time due to persistent pain. Nine months after her acute injury, she underwent exchange nailing, and 4 months later she was able to fully participate without pain, with radiographs indicating complete healing (Fig. 6). She was able to compete at the collegiate and national level until she began having symptoms in her contralateral limb 3 years later. Radiographs again revealed an anterior tibial stress fracture. She was again treated with rest, and she cross-trained for several months. Four months later, while

Fig. 5. Acute fracture through previously identified anterior stress fracture. (A) AP view. (B) Lateral view showing completion of fracture line posteriorly.

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Fig. 6. Healed fracture after intramedullary nailing.

participating in a coaching clinic, she had an increase in pain. Repeat radiographs revealed no evidence of healing. Intramedullary nailing, although effective in many cases, does not lead to healing in all cases. Perhaps the pain relief promoted by the nail allows return to sports before complete bony healing. With continued stress, it may be difficult for complete bony healing to occur. SUMMARY Tibial stress fractures should be suspected on the basis of history and physical examination and confirmed by radiographs, MRI, or bone scan. Treatment typically consists of rest, with gradual resumption of activities after the pain has resolved. Occasionally, despite conservative treatment, surgical intervention is warranted. Despite surgical stabilization, not all fractures proceed to union, and intramedullary fixation is not without complications. It is important to assess the individual athlete for risk factors and other medical conditions. Treatment decisions should be made only after careful consideration of the individual athlete, based on the type and duration of symptoms, fracture pattern, and level of competition. Surgical intervention may be needed but does not guarantee healing. Prevention may be the key to this injury, and there are exciting areas of research aimed at this treatment modality. References [1] Matheson GO, Clement DB, McKenzie DC, et al. Stress fractures in athletes: a study of 320 cases. Am J Sports Med 1987;15(1):46–58. [2] Armstrong DW, Rue JP, Wilckens JH, et al. Stress fracture injury in young military men and women. Bone 2004;35:806–16. [3] Iwamoto J, Takeda T. Stress fractures in athletes: review of 196 cases. J Orthop Sci 2003; 8:273–8.

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[4] Tauton JE, Ryan MB, Clement DB, et al. A retrospective case-control analysis of 2002 running injuries. Br J Sports Med 2002;36:95–101. [5] Boden BP, Osbahr DC. High-risk stress fractures: evaluation and treatment. J Am Acad Orthop Surg 2000;8(6):344–53. [6] Sonoda N, Chosa E, Totoribe K, et al. Biomechanical analysis for stress fractures of the anterior middle third of the tibia in athletes: nonlinear analysis using a three-dimensional finite element method. J Orthop Sci 2003;8:505–13. [7] Barrow GW, Saha S. Menstrual irregularity and stress fractures in collegiate female distance runners. Am J Sports Med 1988;16(3):209–16. [8] Khan KM, Liu-Ambrose T, Sran MM, et al. New criteria for female athlete triad syndrome? Br J Sports Med 2002;36:10–3. [9] Voss LA, Fadale PD, Hulstyn MJ. Exercise-induced loss of bone density in athletes. J Am Acad Orthop Surg 1998;6:349–57. [10] Boden BP, Osbahr DC, Jimenez C. Low-risk stress fractures. Am J Sports Med 2001;29(1): 100–11. [11] Giladi M, Milgrom C, Simkin A, et al. Stress fractures. Identifiable risk factors. Am J Sports Med 1991;19(6):647–52. [12] Matheson GO, Bergman AG, Hoffman KL, et al. Tibial stress reaction in runners. Am J Sports Med 1995;23(4):472–81. [13] Bergman AG, Fredericson M, Ho C, et al. Asymptomatic tibial stress reactions: MRI detection and clinical follow-up in distance runners. Am J Radiol 2004;183:635–8. [14] Kiuru MJ, Niva M, Reponen A, et al. Bone stress injuries in asymptomatic elite recruits. Am J Sports Med 2005;33(2):272–6. [15] Marx RG, Saint-Phard D, Callahan LR, et al. Stress fracture sites related to underlying bone health in athletic women. Clin J Sport Med 2001;11(2):73–6. [16] Dickson TB, Kishline D. Functional management of stress fractures in female athletes using a pneumatic leg brace. Am J Sports Med 1987;15(1):86–9. [17] Swenson EJ, DeHaven KE, Sebastianelli WJ. The effect of a pneumatic leg brace on return to play in athletes with tibial stress fractures. Am J Sports Med 1997;25:322–8. [18] Stewart G, Brunet ME, Manning MR, et al. Treatment of stress fractures in athletes with intravenous pamidronate. Clin J Sport Med 2005;15(2):92–4. [19] Milgrom C, Finestone A, Novack V, et al. The effect of prophylactic treatment with risedronate on stress fracture incidence among infantry recruits. Bone 2004;35(2): 418–24. [20] Komatsubara S, Mori S, Mashiba T, et al. Human parathyroid hormone accelerates the fracture healing process of woven to lamellar bone replacement and new cortical shell formation in rat femora. Bone 2005;36(4):678–87. [21] Wheeler P, Batt ME. Do non-steroidal anti-inflammatory drugs adversely affect stress fracture healing? A short review. Br J Sports Med 2005;39:65–9. [22] Rue JP, Armstrong DW, Frassica FJ, et al. The effect of pulsed ultrasound in the treatment of tibial stress fractures. Orthopedics 2004;27(11):1192–5. [23] Chang PS, Harris RM. Intramedullary nailing for chronic tibial stress fractures. Am J Sports Med 1996;24(5):688–92. [24] Baublitz SD, Shaffer BS. Acute fracture through an intramedullary stabilized chronic tibial stress fracture in a basketball player. Am J Sports Med 2004;32(8):1968–72. [25] Brukner P, Fanton G, Bergman AG, et al. Bilateral stress fractures of the anterior part of the tibial cortex. J Bone Joint Surg Am 2000;82(2):213–8. [26] Rettig A, Shelbourne KD, McCaroll JR, et al. The natural history and treatment of delayed union stress fractures of the anterior cortex of the tibia. Am J Sports Med 1988;16:250–5. [27] Batt ME, Kemp S, Kerslake R. Delayed union stress fractures of the anterior tibia: conservative management. Br J Sports Med 2001;35(1):74–7. [28] Ekenman I, Milgrom C, Finestone A, et al. The role of biomechanical shoe orthoses in tibial stress fracture prevention. Am J Sports Med 2002;30(6):866–70.

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CLINICS IN SPORTS MEDICINE Stress Fractures of the Medial Malleolus and Distal Fibula Paul S. Sherbondy, MD*, Wayne J. Sebastianelli, MD* Penn State Orthopaedics, 1850 East Park Avenue, Suite 112, University Park, PA 16803, USA

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tress fractures of the medial malleolus and distal fibula are injuries that occur infrequently. Of the two, fibular stress fractures are encountered more frequently. Fibular stress fractures account for 4.6% to 21% of all stress factures and are the third to fifth most common stress fracture [1–3]. Epidemiologic studies of stress fractures often do not distinguish between proximal, middle, and distal (lateral malleolus) fibular fractures, which makes the incidence of fibular stress fractures occurring about the ankle difficult to discern. Although fractures at all levels have been reported, distal third fractures within 4 to 7 cm of the tip of the lateral malleolus are more common than fractures in the proximal two thirds [4–6]. There are numerous reports of distal fibular stress fractures [7–11], including reports of bilateral occurrences [5,12,13]. Fractures of the medial malleolus, first reported by Devas [14] in 1975, have received greater attention in the modern orthopedic literature than the more common lateral fractures, since the report by Shelbourne and colleagues [15] in 1988. Medial malleolar stress fractures occur almost entirely in athletes or runners and, reportedly, in skeletally immature patients [16]. The incidence of medial malleolar stress fractures varies from 0.6% to 4.1% of all stress fractures, depending on the series [1,2]. In contrast, the tibial shaft, which is usually the most common site of stress fracture, accounts for 20% to 60% of all stress fractures [1–3]. ANATOMY AND BIOMECHANICS Stress fractures of the lower third of the fibula have been classified into two types by Burrows [7]. He noted that young male athletes sustained fractures at 5 to 6 cm proximal to the tip of the malleolus, whereas middle-aged females were prone to injury at only 3 to 4 cm from the tip. The majority of distal fibular stress fractures are the more proximal distal variety, which are , termed “runner s fractures” [8,9,11,12]. Proximal distal fractures occur through * Corresponding authors. E-mail addresses: [email protected] (P.S. Sherbondy), wsebas [email protected] (W.J. Sebastianelli).

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Fig. 1. Sixty-four-year-old male who engaged in vigorous ethnic dancing and extensive walking during a 3-week vacation. (A) Subtle periosteal reaction of the lateral cortex of the distal fibula (arrows) with confirmation of stress fracture (B) on a bone scan (circle).

cortical bone that has a narrower diameter, and the distal fibular stress fractures happen through the predominantly cancellous bone of the malleolus (Figs. 1 and 2) [7]. Distal fibular stress fractures appear to be caused by a combination of muscular forces and axial loading, the latter of which may be amplified by

, Fig. 2. Twenty-one-year-old Division I women s basketball player who presented with progressive lateral ankle pain. (A) Initial radiographs appear to be negative. Closer evaluation of the initial radiographs suggest subtle cortical thickening (arrows). (B) Bone scan shows increased activity (circles) consistent with distal fibular stress fracture.

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alignment. The fibula plays a secondary role in weight bearing. The load borne by the fibula varies from 2.3% to 10.4% of the total load applied and depends on ankle position and loading orientation [17]. Muscular forces have been postulated to play a role in the occurrence of fibular fractures [8,18]. Strong contractions of the ankle plantar flexors in runners are believed to approximate the fibula to the tibia, with resultant stress concentration at the more proximal distal site [8]. As for the distal fibular stress fractures, which occur predominantly through cancellous bone, osteoporosis is believed to play a role because these fractures are more common in older females who are more prone to bone mineral density changes [5]. Recurrent forces of eversion, opposed by the stabilizing force of the syndesmotic ligaments, create a valgus moment at the ankle with stress concentration at the level of the ankle joint mortise [13]. Lateral malleolar insufficiency fractures in patients who have inflammatory arthritides are associated with valgus ankle alignment, which appears to cause a stress riser in this area [19].

Fig. 3. Twenty-one-year-old Division I cross-country runner who presented with progressive medial ankle pain. Initial radiographs were negative. Anteroposterior (A) and lateral (B) radionuclide bone scan projections indicate a diagnosis of medial malleolar stress injury. (C ) The patient continued to train and went on to develop a complete fracture.

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Stress fractures of the medial malleolus theoretically arise from abnormal weight transmission and torsional forces. Muscular forces are not believed to play a significant role on the medial side [14]. Medial malleolar stress fractures have a characteristic vertical or oblique fracture line arising from the junction of the medial malleolus and tibial plafond [15,20]. Shelbourne and colleagues [15] believe that closed-chain loading of the foot results in a series of obligatory events that can result in injury to the medial malleolus. As the forefoot pronates during the stance phase of gait, the navicular abducts, causing internal rotation of the talus. Talar internal rotation is then transmitted to the tibia through the medial malleolus, causing the characteristic stress fracture orientation (Fig. 3). RISK FACTORS Various intrinsic and extrinsic risk factors have been described for stress fractures. Fatigue fractures occur when normal bone is stressed at a rate that exceeds the ability of the bone to remodel to a stronger state and adapt to greater force and cycles. Insufficiency fractures occur when abnormal bone is routinely , stressed under conditions of, for example, osteoporosis, Paget s disease, and rickets. The majority of stress fractures about the ankle are fatigue fractures. Extrinsic risk factors include a recent increase in activity, running on hard or uneven surfaces, poor footwear, and other training errors [4,21]. Numerous intrinsic risk factors have been proposed, including a narrow tibia, increased hip external rotation, forefoot varus, subtalar varus, tibia varum, leg length discrepancy, pes cavus, pes planus, muscle weakness and fatigue, hyperpronation, previous injury, poor conditioning, female gender, menstrual irregularities, and increased age [4,22–25]. Foot structure is correlated to lower-extremity overuse injuries [26]. The pes cavus foot type tends to be more rigid and less energy absorbing, whereas the pes planus type is a more mobile foot. Both of these foot types are associated with a nearly twofold greater incidence of lower extremity stress fracture in military personnel, compared with feet with a normal arch height [26]. Abnormal weight transmission is believed to play a role in medial malleolar stress fractures [8,27]. Okada and colleagues [27] believe this develops because of an abnormally small angle between the tibial shaft and plafond that increases stress transmission to the medial malleolus (varus alignment). Theoretically, tibia vara is believed to be a risk factor for medial malleolar stress fractures [22,27]. Tibia vara can lead to increased force transmission across the ankle joint by escalating the varus moment between the talus and medial malleolus. All three medial malleolar stress fractures described by Kor and colleagues [22] “had various magnitudes of tibial varum.” Two of the larger series of medial malleolar stress fractures did not comment on significant malalignment as a precipitating factor [15,20]. A pronated foot with increased hindfoot valgus is believed to place the lateral malleolus at a greater risk [23]. In patients who had inflammatory arthritides, valgus deformity of the ankle was associated with the development of distal fibular stress fractures [19]. Running on hard ground is believed to be a causative

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factor in the development of the proximal distal fibular stress fracture [8,12]. Other authors have been unable to identify alignment or metabolic disorders that may contribute to the development of distal fibular stress fractures [5]. CLINICAL PRESENTATION Patients with stress fractures of the malleoli typically have a history of increased physical activity preceding the development of symptoms. For an established athlete, there may be a recent increase in training intensity or the addition of adjunctive training activities. Other patients may relate the recent commencement of a physical fitness program. Conversely, some patients report no recent changes to account for their symptoms. It is important to inquire regarding training habits, footwear, orthotics, and previous injuries. Patients who crosstrain are less likely to experience a stress injury. Shoe and orthotic quality and design should be investigated. A history of previous injuries, including previous stress-related problems, may be revealing. It is important to inquire about eating disorders, weight loss, and menstrual irregularities in females. There is usually no history of trauma. As with most stress injuries, symptoms are aggravated with activity and relieved with rest. The pain initially may be difficult to localize, but as the injury progresses, it generally localizes to the malleolar area. The pain generally does not radiate and is often associated with stiffness or swelling. Symptoms may have been present for days to months and are generally significant enough to affect performance or participation. Physical examination usually reveals normal range of motion and strength. Limping may be present. Tenderness should be localized over the malleolar area. A focal pitting or doughy edema may be present. As mentioned previously it is important to look for any malalignment and observe the gait pattern. The differential diagnosis can include neoplasm, infection, metabolic bone disease, ankle sprain, internal derangement of the ankle such as osteochondral lesion of the talus, ankle tendonitis, exertional compartment syndrome, peroneal tendon tear or subluxation, muscle strain or hernia, and periostitis (shin splints). DIAGNOSTIC IMAGING Plain radiographs are useful in the initial evaluation of an athlete in whom a stress fracture is suspected. In more advanced or established cases, cortical or medullary fracture lines, regional osteopenia, sclerosis, and callus formation may be noted. Unfortunately, radiographs are initially negative in up to 70% of stress fractures and may not show evidence of injury for 2 to 4 weeks after symptoms begin [28]. In two of the largest series of medial malleolar stress fractures, Shelbourne and colleagues [15] and Orava and colleagues [20] have noted only two of six and three of eight patients, respectively, who had positive initial radiographs. Other authors have reported positive initial radiographs in less than half of their patients who had a suspected medial malleolus stress fracture [22,27]. A characteristic cystic lesion associated with medial malleolar stress fractures caused by microfracture and bone resorption has been described [21,27].

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Fig. 4. STIR MR image of the distal right fibula. Note abnormally increased intramedullary signal (arrows). (From Slawson SH, Arendt E, Engebretsen L, et al. Fibular stress fracture in a 20-year-old woman. Orthopedics 1994;17(4):375–9; with permission.)

Because of the high incidence of false-negative radiographs early in the course of stress fractures, additional diagnostic imaging is often indicted. Radionuclide bone scanning has traditionally been the test of choice in this situation but is being supplanted by MRI. An increased uptake observed on a bone scan correlates with increased bone activity caused by fatigue failure and confirms the diagnosis of stress fracture [21]. Despite being sensitive, bone scanning is not specific and can yield false-positive rates between 13% and 24% [28]. Additionally, it can be difficult to localize the precise anatomic location of injury. MRI has numerous practical advantages over radionuclide scanning. MRI provides precise anatomic resolution and can differentiate between a stress reaction and stress fracture; and it is noninvasive, multiplanar, and uses no radiation. MRI also is more sensitive and specific, provides greater information,

Fig. 5. T1-weighted MRI of a medial malleolus stress fracture. (Copyright 1995 by the American Orthopaedic Foot and Ankle Society (AOFAS), originally published in Foot and Ankle International, January 1995, Vol. 16(1) page 50 and reproduced here with permission.)

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and is able to detect preradiographic bony changes. It has the disadvantages of greater cost and lacks the fine specialized resolution of CT scanning (Figs. 4 and 5) [28,29]. MRI has been used to detect both medial malleolar [27] and distal fibular [29] stress fractures. Okada and colleagues [27] were the first to report the MRI findings of medial malleolar stress fracture as a vertical, linear decreased T1-weighted signal at the plafond–malleolus junction. The early changes detectable on MRI show on short tau inversion recovery (STIR) sequences as increased signal representing edema and hemorrhage. Later, T2-weighted images demonstrate a linear area of decreased signal within a region of increased bone marrow signal. The corresponding T1-weighted images show a low signal line surrounded by an area of intermediate signal [28–30]. TREATMENT The treatment of medial malleolar and distal fibular stress fractures depends on several factors. The presence of a fracture line, fracture displacement, athletic participation, and season status may influence treatment decisions. Nonsurgical management is appropriate for essentially all stress-related factures of the distal fibula and most injuries on the medial side. Treatment involves modified rest for 3 to 8 weeks followed by a gradual return to elevated levels of activity. Complete rest is to be avoided, particularly in the high-level athlete, because of the adverse effects of atrophy and deconditioning. Pneumatic ankle braces have been used effectively for injuries on either side of the ankle [5,10,15]. Immobilization with a cast, fracture boot, or tape [22,27] has been reported for treating medial malleolar stress fractures, whereas other authors have simply used activity modification [20]. Crutches and protected weight bearing for a few weeks, particularly for the limping patient, may be useful on a selected basis [22]. An athlete can cross-train during the period of rest, but the intensity of crosstraining should fall short of provoking symptoms. An evaluation of lowerextremity alignment and orthotics used to correct predisposing mechanical problems should be performed where indicated. The return to activity in most cases can be expected in 6 to 8 weeks [15]. There have been numerous reports of surgical intervention for treating medial malleolar stress fractures [15,16,20,22]. The presence of a radiographically detectable fracture line, particularly in a high-level or in-season athlete, or displacement of the fracture is reported as an indication for surgical intervention [15,16,22]. A return to athletic participation has been reported in as short a period as 24 days [22] or as long as 6 months [20] after surgical treatment. Surgical treatment has been recommended to allow athletes to return to sports participation earlier [15,16]. However, these recommendations have been made based on small case series, and there have not been any established control groups to judge whether surgical intervention improves outcome or returns athletes to competition more quickly. Surgical treatment has consisted of closed or open reduction and internal fixation with screws (Fig. 6) [15,16,20,22]. Two cases have been reported of a delayed union treated with drilling, which

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Fig. 6. Radiographic view of closed reduction and percutaneous screw fixation procedures performed on the patient seen in Fig. 3.

healed within 6 months, postoperatively [20]. Reider and colleagues [31] have reported the successful treatment of a medial malleolar stress fracture nonunion by open reduction and internal fixation. Recurrent medial malleolar stress fractures have been reported after both surgical and nonsurgical management [16,21]. Surgical results have been uniformly good, without notable complication [15,20,22]. The present authors believe there have been no reports in the literature of surgical fixation of distal fibular stress fractures. SUMMARY Stress fractures of the medial malleolus and distal fibula are rarely encountered. They typically affect the athletic and running population and manifest typical signs and symptoms of stress fractures. Axial and torsional forces, muscular contractions, and alignment are believed to play roles in the development of these injuries. Plain radiographs are often initially nondiagnostic. The diagnosis can be confirmed with radionuclide bone scanning or MRI. Most injuries are amenable to nonsurgical management. Operative intervention for athletes with medial malleolar stress fractures has been advocated under certain circumstances. References [1] Brukner P, Bradshaw C, Khan KM, et al. Stress fractures: a review of 180 cases. Clin J Sport Med 1996;6(2):85–9. [2] Iwamoto J, Takeda T. Stress fractures in athletes: review of 196 cases. J Orthop Sci 2003;8(3):273–8. [3] Ohta-Fukushima M, Mutoh Y, Takasugi S, et al. Characteristics of stress fractures in young athletes under 20 years. J Sports Med Phys Fitness 2002;42(2):198–206. [4] Blivin SJ, Martire JR, McFarland EG. Bilateral midfibular stress fractures in a collegiate football player. Clin J Sport Med 1999;9(2):95–7. [5] Miller MD, Marks PH, Fu FH. Bilateral stress fractures of the distal fibula in a 35-year-old woman. Foot Ankle Int 1994;15(8):450–3.

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[6] DiFiori JP. Stress fracture of the proximal fibula in a young soccer player: a case report and a review of the literature. Med Sci Sports Exerc 1999;31(7):925–8. [7] Burrows HJ. Fatigue fractures of the fibula. J Bone Joint Surg Br 1948;30B:266–79. [8] Devas MB, Sweetnam R. Stress fractures of the fibula. J Bone Joint Surg Br 1956; 38B(4):818–29. , [9] Dugan RC, D Ambrosia R. Fibular stress fractures in runners. J Fam Pract 1983;17(3): 415–8. [10] Palamarchuk HJ, Sabo M. Fibular stress fracture in a female runner: a case report. J Am Podiatr Med Assoc 1998;88(1):34–6. [11] Pester S, Smith PC. Stress fractures in the lower extremities of soldiers in basic training. Orthop Rev 1992;21(3):297–303. [12] Burgess I, Ryan MD. Bilateral fatigue fractures of the distal fibula caused by a change of running shoes. Med J Aust 1985;143(7):304–5. [13] Richmond DA, Shafar J. A case of bilateral fatigue fractures of the fibula. BMJ 1955;29: 264–5. [14] Devas M. Stress fractures. New York: Churchill Livingstone; 1975. [15] Shelbourne KD, Fisher DA, Rettig AC, et al. Stress fractures of the medial malleolus. Am J Sports Med 1988;16(1):60–3. [16] Shabat S, Sampson KB, Mann G, et al. Stress fractures of the medial malleolus: review of the literature and report of a 15-year-old elite gymnast. Foot Ankle Int 2002;23(7): 647–50. [17] Takebe K, Nakagawa A, Miniami H, et al. Role of the fibula in weight-bearing. Clin Orthop 1984;184:289–92. [18] Symeonides PP. High stress fractures of the fibula. J Bone Joint Surg Br 1980;62B(2): 192–3. [19] Maenpaa H, Lehto MUK, Belt EA. Stress fractures of the ankle and forefoot in patients with inflammatory arthritides. Foot Ankle Int 2002;23(9):833–7. [20] Orava S, Karpakka J, Taimela S, et al. Stress fracture of the medial malleolus. J Bone Joint Surg Am 1995;77A(3):362–5. [21] Schils JP, Andrish JT, Piraino DW, et al. Medial malleolar stress fractures in seven patients: review of the clinical and imaging features. Radiology 1992;185(1):219–21. [22] Kor A, Saltzman AT, Wempe PD. Medial malleolar stress fractures: literature review, diagnosis, and treatment. J Am Podiatr Med Assoc 2003;93(4):292–7. [23] Haverstock BD. Stress fractures of the foot and ankle. Clin Podiatr Med Surg 2001; 18(2):273–84. [24] Giladi M, Milgrom C, Simkin A, et al. Stress fractures: identifiable risk factors. Am J Sports Med 1991;19(6):647–52. [25] Korpelainen KR, Orava S, Karpakka J, et al. Risk factors for recurrent stress fractures in athletes. Am J Sports Med 2001;29(3):304–10. [26] Kaufman KR, Brodine SK, Shaffer RA, et al. The effect of foot structure and range of motion on musculoskeletal overuse injuries. Am J Sports Med 1999;27(5):585–93. [27] Okada K, Senma S, Abe E, et al. Stress fractures of the medial malleolus: a case report. Foot Ankle Int 1995;16(1):49–52. [28] Steinbronn DJ, Bennett GL, Kay DB. The use of magnetic resonance imaging in the diagnosis of stress fractures of the foot and ankle: four case reports. Foot Ankle Int 1994; 15(2):80–3. [29] Slawson SH, Arendt E, Engebretsen L, et al. Fibular stress fracture in a 20-yeat-old woman. Orthopedics 1994;17(4):378–9. [30] Timins ME. MR imaging of the foot and ankle. Foot Ankle Clin 2000;5(1):83–100. [31] Reider B, Falconiero R, Yurkofsky J. Nonunion of a medial malleolus stress fracture: a case report. Am J Sports Med 1993;21(3):478–81.

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CLINICS IN SPORTS MEDICINE Metatarsal Shaft Fractures and Fractures of the Proximal Fifth Metatarsal Gary B. Fetzer, MD, Rick W. Wright, MD* Department of Orthopaedic Surgery, Washington University in St. Louis School of Medicine, Barnes-Jewish Hospital, One Barnes-Jewish Hospital Plaza, West Pavilion, Suite 11300, St. Louis, MO 63110, USA

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he forefoot has been described to serve two primary functions: (1) provide a broad rigid platform for weight bearing and (2) provide a mobile platform to accommodate uneven ground while ambulating [1]. The metatarsal bones, phalanges, and surrounding structures provide this platform. Fractures of the metatarsals are common injuries and can alter the functional characteristics of this platform. Although metatarsal fractures can occur from any traumatic event, high-performance and recreational athletes are at increased risk. The pertinent anatomy, evaluation, diagnosis, classification, and treatment of acute and chronic (stress) metatarsal shaft fractures are discussed in this article. Fractures of the proximal fifth metatarsal, which are unique and important injuries, are discussed and emphasized separately.

EVALUATION AND DIAGNOSIS Patients who have injury to the metatarsals typically present with a history of acute or repetitive trauma to the forefoot [1,2]. Pain exacerbated by weight bearing is the most common symptom. Swelling and ecchymosis are also associated with these fractures. Pain is fairly localized initially, but localization becomes difficult following forefoot and midfoot swelling. Deformity can be seen with significantly displaced fractures, so thorough examination of the skin and neurovascular status is important. With direct-injury mechanisms, the skin overlying the forefoot is especially vulnerable to laceration or contusion. Standard anteroposterior, oblique, and lateral radiographic views of the foot are mandatory. The lateral view can be difficult to interpret, but determination of sagittal plane displacement is important in the treatment algorithm. Weight-

* Corresponding author. E-mail address: [email protected] (R.W. Wright). 0278-5919/06/$ – see front matter doi:10.1016/j.csm.2005.08.014

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bearing radiographs, if tolerated, can be helpful for evaluation. Evaluation of the tarsometatarsal joints, the tarsal bones, and the phalanges is important to identify associated fractures or joint involvement (subluxation/dislocation). Radiographic classification of metatarsal fractures has been described by the Orthopaedic Trauma Association; however, this classification is useful only for descriptive purposes and does little for predicting overall stability, treatment, or outcome [1,2]. Several normal radiographic findings are also worth mentioning because they can mimic fractures [3]. The proximal fifth metatarsal base has an apophysis, which is first seen in girls aged 9 to 11 years and boys aged 11 to 14 years. This apophysis usually disappears 2 to 3 years after appearance. The apophysis is oriented parallel to the shaft, whereas avulsion fractures are usually perpendicular to the long axis of the shaft. Ossicles can also be confused with true fractures and are distinguished from fractures by their smooth border. Dameron [4] found an os perineum (located within the peroneus longus tendon) in 15% and an os vesalianum (located within the peroneus brevis tendon) in 0.1% of unselected foot radiographs. Radiographic evaluation is generally adequate to make the diagnosis; however, in the evaluation of stress fractures, initial radiographs are frequently normal. Serial radiographs, bone scan, or MRI may be required [5]. Subtle radiographic findings in stress fractures may consist of longitudinal cortical hypertrophy, narrowing of the medullary canal, and periosteal reaction. METATARSAL SHAFT FRACTURES Anatomy The anatomy of the forefoot has previously been described [1,2,6,7]. The first metatarsal is most important for weight-bearing activities because it bears , approximately one third the body s weight through its two sesamoid bones under the metatarsal head [1,5]. The first metatarsal is stronger than the lesser metatarsals despite its shorter and wider bony structure. Strong, thick ligaments form the capsule and stabilize its base at the first tarsometatarsal joint. Two strong muscle-tendon units (the anterior tibialis and the peroneus longus) attach to its base. As a result of its relative size, strength, and mobility, the first metatarsal is less frequently injured. The four lesser metatarsals each provide one contact point on the plantar aspect of the foot. The base of each metatarsal is stabilized to the midfoot by series of ligaments (tarsometatarsal ligaments). The central three metatarsals have no extrinsic motor insertions; however, they provide structural support and serve as the origin of the dorsal and plantar interossei muscles. Distally, the thick transverse intermetatarsal ligament connects the metatarsal heads indirectly by linking the plantar plates of the metatarsophalangeal joints. There is a gentle cascade of decreasing metatarsal length, progressing from the second through the fifth metatarsal. Increased mobility in the lateral metatarsals allows adaptability to terrain by the metatarsal heads.

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Mechanism of Injury and Classification Acute metatarsal fractures occur as a result of direct or indirect mechanisms [1,2,5–7]. Direct injuries are most commonly the result of dropping a heavy object on the forefoot. Indirect injuries occur most commonly by way of a twisting injury with the forefoot in a fixed position (eg, when a person catches the forefoot in a narrow opening). Avulsion fractures can occur and are most common at the base of the first and fifth metatarsals. Stress fractures are overuse injuries, the result of repetitive loads applied to the bone. Metatarsal stress fractures have been termed “march fractures”; the first known report is from the middle 1800s by a Prussian military physician [8]. Stress fractures are the result of excessive repetitive loads on the bone that cause an imbalance between bone resorption and formation [9]. An abrupt increase in the duration, intensity, or frequency of physical activity without adequate periods of rest may lead to a stress fracture. DeLee and colleagues [10] defined a stress fracture as a spontaneous fracture of normal bone that results from the summation of stresses of which any by itself would be harmless. The exact mechanical phenomenon remains unclear. One theory is that excessive forces are transmitted to bone when surrounding muscles become fatigued [11,12]. A second theory is that muscles contribute to stress fractures by concentrating forces across a localized area of bone, causing mechanical insults stronger than the stress-bearing capacity of the bone [9]. In general, there are many causal factors and variables that contribute to the development of stress fractures, including systemic factors (bone mass density, nutritional, hormonal), anatomic factors (structure and alignment, muscular attachments, vascular supply), and mechanical factors (applied load, type of athletic activity) [9,13–15]. Populations at risk include military personnel, athletes (especially runners), and ballet dancers [1,7,9,15–19]. Among athletes who have stress fractures, the metatarsals are involved 9% to 19% of the time, with the second and third metatarsal shafts accounting for 80% of the fractures [16,18,19]. Other locations include the proximal fifth metatarsal, the metatarsal neck/head, and the base of the second metatarsal [9]. Iatrogenic causes are found following a dorsal malunion of a first metatarsal osteotomy in which increased force is transferred to the second metatarsal [9]. Treatment From a weight-bearing perspective, the first metatarsal is important because it supports one third of the weight-bearing forces [1,5]. Weight-bearing radiographs may help to determine fracture stability and resting position of the metatarsal heads. Significant medial displacement of the first metatarsal causes widening of the forefoot and subsequent footwear problems [6]. Isolated, minimally displaced first metatarsal fractures can usually be treated in a non– weight-bearing short-leg cast for approximately 4 to 6 weeks. Evidence of instability, significant displacement, or loss of normal anatomic position is an indication for operative stabilization [1,2,6]. Methods of operative stabilization include closed reduction with percutaneous Kirschner wires and open reduction

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internal fixation with a plate and screw construct or Kirschner wires. External fixation is usually reserved for severe open fractures, fractures with significant bone loss, or fractures that present with significant comminution and loss of length. Treatment of lesser metatarsal shaft fractures also emphasizes the resting position of the metatarsal heads [1]. There is no definitive study describing the exact millimeter or angular displacement that is acceptable; however, the criteria most often mentioned include less than 10° of angulation or 3 to 4 mm of translation in any plane [1,2,5,7]. Moderate displacement in the coronal plane is usually well tolerated; however, displacement of any fracture in the sagittal plane changes the weight-bearing characteristics across the metatarsal heads [6,7]. An isolated fracture with minimal or no displacement is generally treated with a hard-sole postoperative shoe, a prefabricated walker boot, or a short-leg cast with progressive weight bearing, with transition to a well-padded shoe at 3 to 4 weeks. Displacement outside the suggested parameters should be reduced by open or closed methods. The vast majority of diaphyseal fractures can be reduced by closed manipulation and held in position by a short-leg cast until fracture healing. Failure to obtain or maintain adequate reduction is an indication for operative management. Closed or open reduction, with stabilization obtained with Kirschner wires, interfragmentary screws, or plate and screw constructs, is suggested [1,2,5–7,20]. Protected weight bearing for 4 to 6 weeks is usually required for bony healing. Diagnosis of a stress fracture is the key step in the treatment algorithm. The mainstay of treatment is nonoperative, involving removal of all aggravating factors and a “relative” restriction of activity. Occasionally, a hard-sole postoperataive shoe can be used for symptomatic relief [5]. Surgical treatment is usually reserved for delayed unions, nonunions, or stress fractures that become displaced. Restriction of activity for approximately 3 to 4 weeks is usually adequate, with a gradual return to activity. PROXIMAL FIFTH METATARSAL FRACTURES In 1902, Sir Robert Jones [21] was the first to describe a fracture of the proximal fifth metatarsal. Since this first report, extensive clinical research and basic science reports have characterized fractures in this region and demonstrated that some fractures of the proximal fifth metatarsal are troublesome to treat [4,22–31]. Thus, all fractures at the proximal end of the fifth metatarsal cannot be considered together when discussing mechanism of injury, treatment options, and outcomes. Anatomy Anatomy of the proximal fifth metatarsal has been previously described and reviewed [3,32–34]. The fifth metatarsal bone consists of the base, tuberosity (ie, the styloid process), diaphysis, neck, and head. The metaphyseal base articulates proximally with the cuboid bone and medially with the fourth metatarsal bone. Dorsal and plantar cuboideometatarsal ligaments, an inter-

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metatarsal ligament, and the joint capsule provide stability at the proximal tarsometatarsal joint. On the dorsolateral aspect of the tuberosity, the tendon of the peroneus brevis inserts. Distal to the tuberosity, the peroneus tertius inserts on the dorsal surface of the metatarsal diaphysis. A lateral band of the plantar aponeurosis inserts on the tip of the tuberosity, linking the tuberosity to the lateral margin of the medial calcaneal tubercle. The flexor digiti minimi brevis muscle of the small toe originates from the plantar surface of the base of the fifth metatarsal bone. Dorsal and plantar interosseous muscles also arise from the diaphysis of this bone. Blood supply to the proximal fifth metatarsal is important with regard to fracture healing. In 1927, Carp [23] reported on 21 fractures of the proximal fifth metatarsal and cited vascular insufficiency as a potential etiology contributing to the high incidence of observed delayed unions in his series. Subsequently, Smith and colleagues [24] described the intraosseous blood supply of the fifth metatarsal from a cadaver model. Blood supply originates from three potential sources: the nutrient artery, the metaphyseal perforators, and the periosteal arteries (Fig. 1). The nutrient artery enters the bone medially from the middle one third of the diaphysis and terminates in linear branches proximally and distally. Metaphyseal arteries arise from the surrounding soft tissue and penetrate the metaphysis, branching in a random distribution. A watershed area between these two distributions corresponds to the region of poor fracture healing noted clinically. The proximal fifth metatarsal has been classified into three separate fracture zones (Fig. 2) [4,22,34]. Zone 1 is most proximal and includes the metatarsocuboid articulation, the insertion of the peroneus brevis tendon, and the lateral plantar aponeurosis. Fractures in this zone are typically avulsion-type fractures and can extend intra-articularly. These fractures usually result from an indirect mechanism of injury, such as an acute inversion of the foot [3,22,33,34]. Zone 2 corresponds to the metaphyseal–diaphyseal junction (fractures here are “true” Jones fractures). Stewart [35] defined a true Jones fracture as a transverse fracture at the junction of the diaphysis and the metaphysis without extension distal to the fourth-fifth intermetatarsal articulation. Fractures gener-

Fig. 1. Intraosseous blood supply to the proximal fifth metatarsal demonstrating a potential watershed area between the randomly distributed metaphyseal perforators and the linear terminal branches of the nutrient artery.

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Tuberosity avulsion fracture Jones' fracture Diaphyseal stress fracture

Fig. 2. Anatomatic fracture zones of the proximal fifth metatarsal. (Copyright 1993 by the American Orthopaedic Foot and Ankle Society (AOFAS), originally published in Foot and Ankle International, July/August 1993, Vol. 14(6) page 360 and reproduced here with permission.)

ally begin laterally in the more distal portion of the tuberosity and extend transversely or obliquely into the area of the medial cortex where the fifth metatarsal articulates with the fourth metatarsal [3,33,34]. Mechanism of injury is believed to occur when a large adduction force is applied to the forefoot with the ankle plantar flexed (eg, pivoting or cutting maneuver with most of the body weight on the metatarsal heads) [33,34]. When high load on the plantar aspect of the fifth metatarsal head creates a large bending motion, the bone fractures at the junction of the proximal diaphysis and the metaphysis. Zone 3 includes the proximal 1.5 cm of the diaphysis. Injuries in this region usually represent a stress or fatigue mechanism: repeated normal loads applied beneath the fifth metatarsal head over a relatively short period of time. The prevalence of proximal diaphyseal stress fractures from the literature is difficult to assess because many clinical series do not distinguish between zone 2 and zone 3 fractures. Kavanaugh and colleagues [36] reported that 41% of their patients who had proximal fifth metatarsal fractures had prodromal symptoms. Zelko and coworkers [31] identified a fracture line with periosteal reaction at initial presentation in 67% of patients. Torg and colleagues [27] suggested a classification system to distinguish the healing potential of proximal diaphyseal fifth metatarsal fractures: (1) acute, (2) delayed union, and (3) nonunion (Table 1). Acute (type I) fractures are described as clinically acute (although prodromal pain may have been present) and defined radiographically by sharp fracture margins, minimal or no periosteal reaction, and minimal cortical hypertrophy. Delayed-union (type II) fractures are characterized by history of previous injury or fracture and characterized radiographically by some periosteal reaction, widened fracture margins, and some intramedullary sclerosis. Nonunion (type III) fractures are characterized by a clinical history of repetitive trauma or recurrent symptoms and characterized radiographically by sclerosis obliterating the medullary canal and blunted fracture edges.

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Table 1 Classification of proximal diaphyseal fifth metatarsal fractures Classification

Clinical

Acute (type I)

Acute injury New onset pain

Radiographic

Sharp fracture margins without widening Minimal cortical hypertrophy Minimal periosteal reaction Delayed union (type II) History of previous injury Slight fracture widening Persistent pain New periosteal bone formation Some intramedullary canal sclerosis Nonunion (type III) Repetitive injury Definite fracture widening with blunted edges Recurrent symptoms Abundant periosteal bone formation Complete obliteration of intramedullary canal

Data from Torg JS, Balduini FC, Zelko RR, et al. Fractures of the base of the fifth metatarsal distal to the tuberosity. J Bone Joint Surg Am 1984;66(2):209–14.

Treatment Treatment of avulsion fractures (zone 1) is generally straightforward. The recommended treatment of these injuries is symptomatic care [1–3,22,36]. There has been little difficulty reported in obtaining successful healing of these injuries regardless of fragment size or degree of displacement, or for nondisplaced intraarticular fractures [30,34,37]. Weight bearing as tolerated in a hard-sole postoperative shoe with ice, elevation, and a compressive elastic wrap for swelling control is usually adequate. A functional brace (walker boot) or short-leg walking cast may be useful for increased comfort but is generally not necessary. Most fractures heal by bony union or by an asymptomatic fibrous union within 6 to 8 weeks [33,34,37]. Quill [3] reported clinical union at an average of 6.1 weeks in 14 patients who had nonoperative treatment of avulsion fracture. Occasionally, operative management is required in the event of significant articular step-off (greater than 2–3 mm), fragments involving greater than 30% of the articular surface, or a symptomatic nonunion [1,2,30,33,34]. In these situations, excision of the small fragment, open reduction and internal fixation with an interfragmentary screw, closed reduction and Kirschner wire fixation, or tension band wiring can be performed [3,30,33,34]. The suggested treatment of acute nondisplaced Jones fracture and Torg type 1 (acute) diaphyseal stress fractures is non–weight-bearing ambulation in a short-leg cast for 6 to 8 weeks [3,22,33,34]. Exceptions to this include the highperformance athlete or the informed patient who refuses nonoperative management [3,22,33,34]. Two published series have documented the nonoperative treatment outcomes of acute true Jones fractures [27,38]. Torg and colleagues [27] reported on 15 acute Jones fractures treated nonoperatively with protected weight bearing and cast immobilization. Ninety-three percent healed at an average of 6.5 weeks. One patient had a symptomatic nonunion that required operative management before union was obtained. Clapper and coworkers [38] reported on 235 true acute Jones fractures. In their series, union occurred in only

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72% of patients, whereas 28% had clinical and radiographic evidence of nonunion at 25 weeks after injury. These 7 patients were treated with intramedullary screw fixation, and 100% union was achieved in all patients at an average of 12.1 weeks. High incidence of delayed union and nonunion has led many surgeons to consider more aggressive treatment for these fractures. Operative management has been suggested for patients who have acute displaced fractures, who have failed or refuse nonoperative management, and who have Torg type II and III diaphyseal stress fractures. Early surgical intervention may also be a reasonable option in high-performance athletes and even some recreational athletes who have acute Jones fractures [3,27,33,34].

Fig. 3. A 30-year-old professional athlete who had an acute proximal fifth metatarsal fracture. Operative management with intramedullary screw fixation resulted in clinical and radiographic union. (A,B) Preoperative radiographs demonstrating acute fracture. (C,D) Postoperative radiographs demonstrating a healed fracture with a cannulated intramedullary screw.

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Fig. 3 (continued ).

The goal of early operative management is to minimize risk of nonunion, delayed union, and possible refracture and to decrease the return time to athletic activity. Options for surgical intervention include closed reduction with intramedullary screw, intercalated corticocancellous bone graft, open reduction and internal fixation with minifragment plate and screws, tension band construct, or closed reduction and Kirschner wire fixation [1,2,10,25,26,28,29,33,34,36]. Bone grafting can also be added for biologic supplementation. Internal fixation with intramedullary screw fixation has become a popular method of surgical management of these fractures, with reports of increased union rates and rapid recovery (Fig. 3) [10,25,26,28,36]. Intramedullary screws offer the benefits of compression across the fracture site without the need to open the fracture site or strip the periosteum. Kavanaugh and colleagues [36] reported on 13 proximal fifth metatarsal fractures treated with a 4.5-mm malleolar screw and demonstrated a 100% union rate with no refractures. DeLee and coworkers [10] reported a 100% union rate with no complications after intramedullary screw fixation with a 4.5-mm malleolar screw in 11 athletes. Mean times to clinical and radiographic union were 4.5 weeks and 7.5 weeks, respectively. The use of cannulated screws has also been reported [25,26,28]. Reese and coworkers [28] reported on 15 patients treated with cannulated screws ranging in diameter from 4.0 to 6.5 mm. Mean times to healing clinically and radiographically were 7.9 weeks and 7.3 weeks, respectively. There were no refractures or nonunions. These investigators concluded that cannulated screw fixation was a reliable method of internal fixation and allowed quick return to activity. Their biomechanical analysis comparing cannulated and solid stainless steel

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and titanium screws demonstrated that all screws with a diameter less than 4.0 mm did poorly with fatigue testing; it was recommended that the largest screw possible be used for surgical fixation. Porter and colleagues [26] followed 23 patients treated with a 4.5-mm cannulated intramedullary screw for proximal fifth metatarsal fractures (Jones fractures). They reported no refractures and a 100% clinical healing rate. All patients returned to sports at a mean time of 7.5 weeks; however, 2 patients suffered re-injury but did not need operative treatment. Although intramedullary screw fixation has demonstrated excellent outcomes and early return to full activity, there are reports in the literature of complications after intramedullary screw fixation [25,29]. Wright and colleagues [29] reported on six refractures after cannulated screw fixation of Jones fractures in athletes (screw size ranged from 4.0 to 5.0 mm). Despite clinical and radiographic union, 3 patients sustained a refracture the day after return to full activity, and 3 other patients experienced refracture 2.5 to 4.5 months after return to activity. These investigators recommended use of a larger-diameter screw in athletes who have a larger body mass index and use of an orthosis upon return to activity. Larson and coworkers [25] followed 15 patients who underwent cannulated screw fixation of a Jones fracture. They reported six treatment failures: four refractures and two symptomatic nonunions. Only 1 of the 6 patients who failed initial operative management had complete radiographic union upon return to full activity. These researchers concluded that return to full activity before complete radiographic union, especially among elite athletes, was predictive of failure. Plain radiographs may be difficult to interpret for complete radiographic healing. In the patient who desires early return to high-level activities, further testing may be necessary. Currently, the authors obtain a CT scan of the foot and, in consultation with radiologists, use artifact subtraction software to remove the signal of the fixation devices to allow circumferential assessment of bony healing. SUMMARY Metatarsal fractures represent a relatively common injury, especially in athletes. Treatment remains relatively straightforward for the traumatic metatarsal injury. Traditional stress fractures typically heal with decreased activity. The problematic proximal fifth metatarsal fracture (Jones fracture) frequently requires surgical intervention in the patient who wants to avoid , non–weight-bearing cast immobilization. The authors current treatment for this fracture includes the option of intramedullary fixation versus cast immobilization. If surgical treatment is chosen, then the largest-diameter cannulated screw is used for intramedullary fixation. Patients are immobilized for 7 to 10 days until the wounds are healed. Weight bearing is instituted, as tolerated, with biking and swimming also allowed. Light jogging is typically begun at 6 weeks if early healing is noted and the patient is asymptomatic. In the high-

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performance athlete, a CT scan is obtained before release to full sports activity, which usually occurs at 8 to 12 weeks. References [1] Early JS. Fractures and dislocations of the midfoot and forefoot. In: Buckholz RW, Heckman JD, editors. Fractures in adults. 5th edition. Philadelphia: Lippincott Williams and Wilkins; 2001. p. 2215–28. [2] Hansen ST. Foot injuries. In: Browner BD, editor. Skeletal trauma. 2nd edition. Philadelphia: WB Saunders; 1992. p. 1984–6. [3] Quill GE. Fractures of the proximal fifth metatarsal. Orthop Clin North Am 1995;26(2): 353–61. [4] Dameron TB. Fractures and anatomic variations of the proximal portion of the fifth metatarsal. J Bone Joint Surg Am 1972;57(6):788–92. [5] Shereff MJ. Complex fractures of the metatarsals. Orthopaedics 1990;13:875–82. [6] Schenck RC, Heckman JD. Fractures and dislocations of the forefoot: operative and nonoperative treatment. J Am Assoc Ortho Surg 1995;3(2):70–8. [7] Armagon OE, Shereff MJ. Injuries to the toes and metatarsals. Orthop Clin North Am 2001;32(1):1–10. [8] Bernstein A, Stone JR. March fracture: a report of three hundred and seven cases and a new method of treatment. J Bone Joint Surg Am 1944;26(4):743–50. [9] Boden BP, Osbahr DC, Jimenez C. Low-risk stress fractures. Am J Sports Med 2001; 29(1):100–11. [10] DeLee JC, Evans JP, Julian J. Stress fracture of the fifth metatarsal. Am J Sports Med 1983; 11:349–53. [11] McBryde AM. Stress fractures in athletes. J Sports Med 1975;3:212–7. [12] Meyer SA, Saltzman CL, Albright JP. Stress fractures of the foot and leg. Clin Sports Med 1993;12:395–413. [13] Kaufman KR, Brodine SK, Shaffer RA, et al. The effect of foot structure and range of motion on musculoskeletal overuse injuries. Am J Sports Med 1999;27(5):585–93. [14] Donahue SW, Sharkey NA. Strains in the metatarsals during stance phase of gait: implications for stress fractures. J Bone Joint Surg Am 1999;81(9):1236–44. [15] McBryde AM, Barfield WR. Stress fractures of the foot and ankle. Foot Ankle Clin 1999; 4(4):881–909. [16] Matheson DO, Clement DB. Stress fractures in athletes: a study of 320 cases. Am J Sports Med 1987;15:46–58. [17] Muscolo L, Migues A, Slullitel G, et al. Stress fracture nonunion at base of the second metatarsal in a ballet dancer. A case report. Am J Sports Med 2004;32(6):1535–7. [18] Sullivan D, Warren RF, Pavlov H. Stress fractures in 51 runners. Clin Orthop 1984;187: 188–92. [19] Orava S. Stress fractures. Br J Sports Med 1980;14:40–4. [20] Heim U, Pfeiffer KM. Internal fixation of small fractures: techniques recommended by the AO group. Berlin: Springer-Verlag; 1987. [21] Jones R. Fracture of the base of the fifth metatarsal bone by indirect violence. Ann Surg 1902;35:697–700. , [22] Lawrence SJ, Botte MJ. Jones fractures and related fractures of the proximal fifth metatarsal. Foot Ankle 1993;14:358–65. [23] Carp L. Fracture of the fifth metatarsal bone with special reference to delayed union. Ann Surg 1927;86:308–20. [24] Smith JW, Arnoczky SP, Hersh A. The interosseous blood supply of the fifth metatarsal: implications for proximal fracture healing. Foot Ankle 1992;13(3):143–52. [25] Larson CM, Almekinders LC, Taft TN, et al. Intramedullary screw fixation of Jones fractures. Analysis of failure. Am J Sports Med 2002;30(1):55–60. [26] Porter DA, Duncan M, Meyer SJ. Fifth metatarsal Jones fracture fixation with a 4.5-mm

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[30]

[31]

[32]

[33] [34] [35] [36] [37]

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cannulated stainless steel screw in the competitive and recreational athlete. A clinical and radiographic evaluation. Am J Sports Med 2005;33(5):1–8. Torg JS, Balduini FC, Zelko RR, et al. Fractures of the base of the fifth metatarsal distal to the tuberosity. J Bone Joint Surg Am 1984;66(2):209–14. Reese K, Litsky A, Kaeding C, et al. Cannulated screw fixation of Jones fractures. A clinical and biomechanical study. Am J Sports Med 2004;32(7):1736–42. Wright RW, Fischer DA, Shively RA, et al. Refracture of proximal fifth metatarsal (Jones) fracture after intramedullary screw fixation in athletes. Am J Sports Med 2000;28(5): 732–6. Rettig AC, Shelbourne KD, Wilckens J. The surgical treatment of symptomatic nonunions of the proximal (metaphyseal) fifth metatarsal in athletes. Am J Sports Med 1992;20(1): 50–4. Zelko RR, Torg JS, Rachun A. Proximal diaphyseal fracture of the fifth metatarsal— treatment of the fractures and their complications in athletes. Am J Sports Med 1979;7: 95–101. Theodorou DJ, Theodorou SJ, Kakitsubata Y, et al. Fractures of proximal portion of fifth metatarsal bone: anatomic and imaging evidence of a pathogenesis of avulsion of the plantar aponeurosis and short peroneal muscle tendon. Radiology 2003;226(3): 857–65. Rosenberg GA, Sferra JJ. Treatment strategies for acute fractures and nonunions of the proximal fifth metatarsal. J Am Assoc Ortho Surg 2000;8(5):332–8. Dameron TB. Fractures of the proximal fifth metatarsal: selecting the best treatment option. J Am Assoc Ortho Surg 1995;3(2):110–4. Stewart IM. Jones fracture: fracture of the base of fifth metatarsal. Clin Orthop 1960; 16:190–8. Kavanaugh JH, Brower TD, Mann RV. The Jones fracture revisited. J Bone Joint Surg Am 1978;60:776–82. DeLee JC. Fractures and dislocations of the foot. In: Mann RA, Coughlin MJ, editors. Surgery of the foot and ankle. 6th edition. St. Louis (MO): Mosby-Year Book; 1992. p. 1627–40. , Clapper MF, O Brien TJ, Lyons PM. Fractures of the fifth metatarsal: analysis of a fracture registry. Clin Orthop 1995;315:238–41.

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CLINICS IN SPORTS MEDICINE Navicular Stress Fractures Morgan H. Jones, MDa, Annunziato S. Amendola, MDb,* a Department of Orthopaedic Surgery, Cleveland Clinic Foundation, A41, 9500 Euclid Avenue, Cleveland, OH 44195, USA b Department of Orthopaedic Surgery, University of Iowa Hospitals and Clinics, 01018 JPP, 200 Hawkins Drive, Iowa City, IA 52242, USA

T

he stress fracture of the tarsal navicular was first described by Towne and colleagues in 1970. It was considered initially to be a rare injury, representing 0.7% to 2.4% of stress fractures, in early reports [1–3]. Since then, the awareness of the injury has increased, and navicular stress fractures represent up to 35% of stress fractures in recent series. However, these injuries remain difficult to diagnose and treat because of their often vague clinical presentation and the poor correlation between radiographic and clinical findings. ANATOMY AND BIOMECHANICS The tarsal navicular is a pear-shaped bone, which is part of the medial column of the foot. The proximal and distal surfaces of the bone as well as a portion of the lateral surface are covered with articular cartilage, whereas the remaining surfaces provide attachment sites for ligamentous and tendinous structures. The proximal surface is concave and articulates with the talus. The distal surface has three facets that articulate with the cuneiform bones. The largest of these is the convex medial surface, which articulates with the medial cuneiform. The inferior segment of the lateral surface articulates with the cuboid bone, and the dorsal segment of the lateral surface serves as an attachment site for the lateral calcaneonavicular ligament. The plantar aspect of the bone often has a prominence called the navicular beak and provides the attachment site for the calcaneonavicular or spring ligament. The navicular tuberosity is the attachment site of the posterior tibial tendon and is located on the medial aspect of the bone [4]. Both the kinematics of the tarsal joints and the blood supply to the navicular bone contribute to the characteristic location of stress fractures in this bone. During heel strike, the navicular is compressed between the talus and cuneiforms, and this force is focused on the central third of the bone [5]. The blood supply to the navicular comes dorsally from branches of the dorsalis pedis artery, plantarly from branches of the medial plantar artery, and medially to

* Corresponding author. E-mail address: [email protected] (A.S. Amendola). 0278-5919/06/$ – see front matter doi:10.1016/j.csm.2005.08.007

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the navicular tuberosity from an anastomosis between the dorsalis pedis and medial plantar arteries. This pattern of vascular supply causes the central portion of the bone to have decreased vascularity compared with the medial and lateral portions [4]. Because of the concentration of force and decreased vascularity of the central portion of the navicular bone, this area is the most susceptible to stress fractures. Numerous predisposing factors have been implicated in the development of navicular stress fractures, including pes cavus, short first metatarsal, metatarsus adductus, limited subtalar or ankle motion, and medial narrowing of the talonavicular joint. However, no study has yet demonstrated the statistical significance of any of these factors [6–8]. INCIDENCE Early studies reported that navicular stress fractures represented only 2.4% of all stress fractures because of the limited recognition of the injury. In fact, some authors did not even distinguish between the navicular and the other tarsal bones in their work [9,10]. As awareness of this injury has increased, more recent studies have reported an incidence as high as 35% [11]. Bennell and colleagues [12] followed 111 track and field athletes in Australia over a 12-month period. Twenty percent of all musculoskeletal injuries sustained were stress fractures, and 15% of stress fractures (four injuries) were navicular fractures. Brukner and colleagues [11] reviewed 180 consecutive stress fractures that presented to a sports medicine clinic in Australia over a 2-year period. Twentysix injuries (14%) were navicular fractures. Nineteen of these fractures occurred in track athletes and two in Australian football players, and one each occurred in a distance runner, a triathlete, a tennis player, a canoer, and a basketball player. CLINICAL EVALUATION A high index of suspicion for navicular stress fracture is necessary in the approach to treating an active patient who complains of foot pain. In other words, if a weight-bearing athlete experiences an insidious onset of midfoot pain, a stress fracture must be ruled out, even if radiographs are normal. Torg and colleagues [8] have noted an average period of 7 months between the onset of symptoms and the diagnosis, in their series. A thorough medical history should be taken to discern the onset of symptoms and any aggravating factors. Patients often complain of pain with an insidious onset that is worse during and following physical activity. Sprinting, jumping, and pushing off are movements that particularly aggravate the condition. A vague pain along the longitudinal arch on the dorsolateral aspect of the foot may be the initial complaint, but as the condition progresses, the pain is often localized to the dorsum of the navicular bone. Patients also may report a recent increase in the intensity or duration of physical activity or a change in equipment or technique. Training errors are often implicated in the development of navicular stress fractures. Although this

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injury is more common in males, female athletes should be questioned to be certain that their injury does not represent part of the female athlete triad. Physical examination should include palpation of the foot to identify areas of tenderness and swelling. Navicular stress fractures typically are tender over the “N” spot on the dorsal aspect of the navicular bone [13]. Symptoms may also be reproduced by hopping on the affected leg with the foot in an equinus position [14]. IMAGING Conventional radiographs of the weight-bearing foot should be the initial imaging study obtained for patients in whom navicular stress fractures are suspected. Wilson and Katz [15] have classified radiographic changes in navicular stress fractures into four types. Type-I fractures have a linear lucency; type-II fractures have sclerosis of the fracture edges and callus formation; type-III fractures have a periosteal reaction and external callus; and type-IV fractures have a mixed pattern. The fracture is usually in the middle third of the bone and oriented in the sagittal plane. However, radiographic results may be normal in the acute phase and not demonstrate changes until 3 to 6 weeks after the injury [16]. If the initial radiographic evidence is normal, additional studies may include CT, MRI, or bone scanning. Kiss and colleagues [17] retrospectively reviewed CT findings in 55 navicular stress fractures in athletes. Fifty-three of the fractures were incomplete, and six small fractures (11%) were not identified on the initial examination. In addition, follow-up studies showed inconsistent findings in fractures that were clinically healed, although all 12 clinical nonunions were confirmed by CT evidence of a persistent fracture gap. Saxena and colleagues [18] have classified CT-scan characteristics of navicular stress fractures into three types. Type I is a break in the dorsal cortex; type II is a break in the dorsal cortex and navicular body; and type III is a fracture

Fig. 1. Bone scan demonstrating increased uptake of the navicular bone.

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into another cortex. Subclassification characterizes avascular, cystic, and sclerotic changes. Bone scanning is a sensitive modality for evaluating a possible navicular stress fracture and provides the additional advantage of screening the entire skeleton (Fig. 1). A negative result reliably rules out a stress fracture; however, a positive result is nonspecific and requires clinical correlation. MRI evaluation provides a sensitive method of evaluation with more specificity that bone scan and the advantage of more anatomic detail [16]. TREATMENT These are high-risk fractures; therefore, aggressive operative and nonoperative treatments are necessary. Aggressive nonoperative treatment means the patient must wear a non-weight-bearing cast until the fracture is healed. Both operative and nonoperative treatments of navicular stress fractures are appropriate depending on fracture characteristics and patient expectations for return to activity. Nonoperative treatment should begin with a non-weight-bearing cast for a period of at least 6 weeks. If tenderness has resolved after the period of casting, then weight bearing can resume, and functional rehabilitation can be started. If pain persists, then the patient can be allowed to bear weight in a boot until the pain resolves. Patients may require up to 8 months to return to full activity [19]. Operative treatment consists of percutaneous screw fixation with or without exposure of the fracture site. Generally, bone grafting is reserved for chronic fractures and delayed unions or nonunions. In their report on 21 navicular stress fractures in 19 patients, Torg and colleagues [8] reported a 100% success rate in the 10 patients whom they treated with non-weight-bearing cast immobilization for 6 to 8 weeks, with an average return to activity at 3.8 months.

Fig. 2. Imaging studies of type-I injury (stress reaction). (A) MRI demonstrating bone edema. (B) CT scan demonstrating sclerosis of dorsal central portion of navicular without fracture.

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Fig. 3. CT scan demonstrating type-II injury (incomplete fracture).

Khan and colleagues [20] reported on the time to return to full activity in 55 patients with navicular stress fractures. All patients were initially treated nonoperatively. Treatment with 6 weeks in a non-weight-bearing cast allowed 86% of patients to return to full activity in an average period of 5.6 months after the injury. This form of treatment was also successful for 9 of 10 patients whose first treatment failed. When patients were placed in a cast for 2 to 5 weeks, 69% of them returned to full activity. When activity restriction without casting was ordered, 50% returned to full activity. When no activity restrictions were ordered, only 20% returned to full activity [20]. Saxena and colleagues [18] reported the time to return to full activity for 19 patients with navicular stress fractures. According to their classification sys-

Fig. 4. CT scan demonstrating type-III injury (complete fracture).

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tem, patients with type-I fractures (break in the dorsal cortex only) (Fig. 2) returned to activity at an average of 3.0 months after injury; patients with type-II fractures (break in dorsal cortex and navicular body) (Fig. 3) returned at an average of 3.6 months after injury; and those with type-III fractures (break into another cortex) (Fig. 4) returned at an average of 6.8 months after injury. The authors advocate early surgical treatment of type-II and -III injuries to allow a faster functional recovery. Pulsed low-intensity ultrasound and an electrical bone stimulator have both been described in the treatment of navicular stress fractures, but no evidence is available on the effectiveness of these treatments [21].

Fig. 5. Surgical technique. (A) Guide pin is placed from lateral to medial in navicular. (B) Cannulated screw is advanced over guide pin. (C ) Guide pin is removed after insertion of screw. (D) An additional screw may be placed from medial to lateral if additional fixation is required.

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Based on these data, the present authors recommend aggressive treatment of navicular stress fractures in athletes, including early surgical intervention. This approach can minimize the time lost from practice and competition without adversely affecting the success of treatment. Patients’ incomplete fractures will undergo percutaneous fixation with cannulated screws (Fig. 5). The fracture site will be opened in cases of displaced fractures or in cases that have progressed to nonunion. Patients with partial fractures that do not extend into the navicular body (Saxena type I) will undergo a trial of non-weight-bearing cast immobilization before surgical intervention. SUMMARY Navicular stress fractures affect athletes and active individuals and can be a difficult condition to diagnose and treat. A high index of suspicion should be maintained to allow early diagnosis and appropriate treatment to minimize disability from this significant injury. References [1] Hulkko A, Orava S, Peltokallio P, et al. Stress fracture of the navicular bone: nine cases in athletes. Acta Orthop Scand 1985;56:503–5. [2] Orava S, Hulkko A. Delayed unions and nonunions of stress fractures in athletes. Am J Sports Med 1988;16:378–82. [3] Smith LS. 300 stress fractures in runners. Med Sci Sports Exerc 1982;14:140. [4] Golano P, Farinas O, Saenz I. The anatomy of the navicular and periarticular structures. Foot Ankle Clin 2004;9:1–23. [5] Van Langelaan EJ. A kinematic analysis of the tarsal joints: an x-ray photogrammetric study. Acta Orthop Scand Suppl 1983;204:1–269. [6] Pavlov H, Torg JS, Freiberger RH. Tarsal navicular stress fractures: radiographic evaluation. Radiology 1983;148:641–5. [7] Ting A, King W, Yocum L, et al. Stress fractures of the tarsal navicular in long-distance runners. Clin Sports Med 1988;7:89–101. [8] Torg JS, Pavlov H, Cooley LH, et al. Stress fractures of the tarsal navicular: a retrospective review of twenty-one cases. J Bone Joint Surg Am 1982;64A:700–12. [9] Goldberg B, Pecora C. Stress fractures: a risk of increased training in freshman. Phys Sportsmed 1994;22:68–78. [10] Matheson GO, Clement DB, McKenzie DC, et al. Stress fractures in athletes: a study of 320 cases. Am J Sports Med 1987;15:46–58. [11] Brukner P, Bradshaw C, Khan KM, et al. Stress fractures: a review of 180 cases. Clin J Sport Med 1996;6:85–9. [12] Bennell KL, Malcolm SA, Thomas SA, et al. The incidence and distribution of stress fractures in competitive track and field athletes: a twelve-month prospective study. Am J Sports Med 1996;24:211–7. [13] Khan KM, Brukner PD, Kearney C, et al. Tarsal navicular stress fracture in athletes. Sports Med 1994;17:65–76. [14] Fitch KD, Blackwell JB, Gilmour WN. Operation for non-union of stress fracture of the tarsal navicular. J Bone Joint Surg Br 1989;71B:105–10. [15] Wilson Jr ES, Katz FN. Stress fractures: an analysis of 250 consecutive cases. Radiology 1969;92:481–6. [16] Sizensky JA, Marks RM. Imaging of the navicular. Foot Ankle Clin 2004;9:181–209. [17] Kiss ZS, Khan KM, Fuller PJ. Stress fractures of the tarsal navicular bone: CT findings in 55 cases. AJR Am J Roentgenol 1993;160:111–5.

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[18] Saxena A, Fullem B, Hannaford D. Results of treatment of 22 navicular stress fractures and a new proposed radiographic classification system. J Foot Ankle Surg 2000;39:96–103. [19] Lee S, Anderson RB. Stress fractures of the tarsal navicular. Foot Ankle Clin 2004;9: 85–104. [20] Khan KM, Fuller PJ, Brukner PD, et al. Outcome of conservative and surgical management of navicular stress fracture in athletes: eighty-six cases proven with computerized tomography. Am J Sports Med 1992;20:657–66. [21] Brand Jr JC, Brindle T, Nyland J, et al. Does pulsed low intensity ultrasound allow early return to normal activities when treating stress fractures? a review of one tarsal navicular and eight tibial stress fractures. Iowa Orthop J 1999;19:26–30.

Clin Sports Med 25 (2006) 159–174

CLINICS IN SPORTS MEDICINE Upper Extremity Stress Fractures Grant Lloyd Jones, MD The Ohio State University Sports Medicine Center, 2050 Kenny Road, Columbus, OH 43221, USA

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tress fractures occur typically in the lower extremity, caused by impact loading from running, walking, or jumping. In one large series, Matheson and colleagues [1] reported on 320 stress fractures, in which 90% occurred in the lower extremity. However, upper-extremity stress fractures are now being recognized more frequently. These fractures occur either as a result of repetitive loading at the point of muscular attachments to bone or as a result of impact loading, as seen in upper-extremity weight-bearing athletes [2]. In a recent review of 196 stress fractures [3], rib stress fractures were second only to tibia fractures in frequency, and ulnar olecranon fractures were fourth in occurrence. In this study [3], rib fractures were the most common type of stress fracture in rowing athletes, whereas olecranon fractures were most common among baseball players. Sinha and colleagues [4] reported on 44 cases of upper-extremity stress fractures in athletes, including rib fractures but excluding spine and physeal fractures. The authors divided the patients into four categories based on the predominant type of upper-extremity activity required for participation in their sport: (1) weight lifting (eg, football, weight lifting, and wrestling); (2) upperextremity weight bearing (eg, gymnastics, diving, and cheerleading); (3) throwing (eg, pitcher, soccer goalie, and javelin); and (4) swinging (eg, golf and tennis). The authors noted that all fractures in the weight bearers were distal to the elbow, whereas most fractures in the throwers affected the shoulder girdle. In the swingers, lower-rib fractures predominated. The weight lifters, on the other hand, had stress fractures throughout the upper extremity but none in the ribs. Overall, the ulnar shaft stress fracture was the most frequently reported stress fracture in their series and occurred in all four groups. The present article reviews the different types of upper extremity and torso stress fractures seen in athletes, starting with the sternum and extending outward to the fingers. The presentation, diagnosis, mechanism of injury, treatment, prevention, and prognosis for each of these injuries will be discussed.

E-mail address: [email protected] 0278-5919/06/$ – see front matter doi:10.1016/j.csm.2005.08.008

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STERNUM Although they are rare, stress fractures of the sternum have been reported in a wrestler [5], a golfer [6], and an athlete performing strenuous abdominal exercises [7]. In the case of the wrestler [5], the patient had pain after weeks of modified training in preparation for a competition. The pain then suddenly increased during activity. Results of a standard radiograph were normal, but a technetium bone scan revealed an increased uptake in the sternum, exactly where his pain was located. The golfer [6] noticed pain and swelling over the sternum at the level of the fourth rib 2 days before a tournament, and the pain increased significantly by the third day of the event. The patient revealed that he had purchased a new set of clubs before the tournament and was training intensively with this new equipment in preparation for the competition. Again, plain radiographic results were normal, but a bone scan revealed a “hot spot” located on the sternum, consistent with a stress fracture. To rule out a neoplastic or infectious cause, exploratory surgery was performed and biopsies were taken, which were negative. The patient followed up with an orthopedic surgeon 9 weeks after surgery and was asymptomatic and beginning to train again. The athlete who was performing strenuous abdominal exercises developed sharp, anterior chest pain and heard a “loud, sharp” sound during a training session [7]. He was tender to palpation over the sternum, and sternal radiographs revealed a transverse fracture of the manubrium sternum. A CT scan of the chest revealed no other pathology. The patient was treated subsequently with analgesics and rest from the offending activity, and his symptoms resolved after 8 weeks. The authors proposed that hyperflexion of the spine in conjunction with contraction of the thoracic and abdominal muscles during a situp exercise were the mechanism of injury. Hyperflexion of the spine presses the manubrium anteriorly, and the pull of the abdominal and thoracic muscles adds to this moment. RIBS Rib stress fractures have been reported in several sports, including rowing, rugby, golf, weightlifting, volleyball, gymnastics, judo, tennis, table tennis, baseball, basketball, soccer, javelin throwing, backpacking, and wind surfing [8–23]. Muscular forces are predominately responsible for these stress fractures [24]. Muscles that attach to ribs are used during upper-extremity movements, trunk rotation, bending, and breathing. The stress placed on the ribs by the muscles during repetitive contraction is accentuated during training because, as in other bones such as the sternum, muscles strengthen more rapidly than bone. In addition, muscle fatigue during prolonged activity lessens the ability of a muscle to absorb and dissipate energy, which then places a bone at risk for fracture [25]. Stress fractures can occur in any portion of any rib depending on the sporting activity and the forces placed on the ribs. The most common sites of fracture

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include the first rib anterolaterally, the fourth through ninth ribs posterolaterally, and the upper ribs posteromedially [24]. First-rib stress fractures occur most commonly in athletes whose sports involve repetitive overhead positioning of the arm such as baseball pitching, basketball, lacrosse, weightlifting, ballet, javelin throwing, and tennis [18,21,23]. One case has been reported in a soccer player who developed the fracture after repetitively heading the ball [20]. These fractures occur at or near the subclavian groove, between the insertions of the scalenus anterior and scalenus medius muscles, where the bone is thinnest [21]. Repetitive contractions of these muscles along with the serratus anterior in overhead activities can cause a fatigue fracture. The scalene muscles stress the first rib with superiorly directed forces, while the serratus anterior and intercostals muscles cause inferiorly directed forces [18]. Patients with first-rib fractures present with an insidious onset of a dull, vague pain in the anterior cervical triangle and clavicular region, with occasional radiation to the sternum and pectoral region [23]. Initially, results of plain radiographs are commonly negative but may demonstrate the stress fracture once osseous callous appears during the healing phase. Technetium bone scanning is a very sensitive technique for the early diagnosis of these fractures and frequently will be positive when radiographs are normal [19]. The treatment of all rib stress fractures is nonoperative, and the initial goal is to provide symptomatic relief [23]. Treatment includes relative rest by avoiding throwing sports or carrying backpacks. Rib fractures usually heal with this type of management, although, there has been one reported case of a baseball pitcher who developed a nonunion of a first rib fracture [21]. The pitcher eventually became asymptomatic despite the nonunion. Stress fractures of the middle and lower ribs occur predominantly in athletes involved in rowing and swinging sports (eg, golf and tennis) [4,17–19]. Other athletic activities associated with these stress fractures include gymnastics, throwing sports, and swimming [4,18,22]. Rib fractures in rowers are found most commonly on the antero- and posterolateral aspects of ribs five through nine and are associated most often with long-distance training and heavy load per stroke [19]. Contractions of the serratus anterior and external oblique muscles during the rowing stroke cause a repetitive bending force to the lateral aspect of the rib [19]. The serratus anterior stabilizes the scapula and draws a rib laterally and superiorly while the external oblique muscle draws a rib medially and inferiorly [18,19]. When the elastic limit of the rib is exceeded, microfractures occur that can progress to complete fractures [18]. When a stress fracture occurs, the rower experiences pain that is greatest at the finish of a stroke and is exacerbated by coughing [19]. There was an apparent increase in the incidence of rib stress fractures in the mid to late 1990s [19]. This has been attributed to several factors, including a new oar shape that was introduced in 1992 [19]. The new shape involved a bigger blade, which yielded faster speeds at the price of increased load per rowing stroke. At the same time, training volumes increased, particularly long-

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distance rows at low stroke rates, and along with these lower stroke rates came an increased load per stroke. This combination of factors results in increased tension required by the serratus anterior to stabilize the scapula and increased force of its eccentric contraction at the end of the stroke, which lead to increased force across the muscle’s rib attachments. Therefore, the incidence of rib factors might be reduced by modification of the equipment and stroke during long-distance rows in the training phase when stress fractures are most likely to occur [19]. The faster stroke rates during competition result in less load per stroke, less muscle force per stroke, and a decreased incidence of stress fracture. The posterolateral aspects of the fourth through sixth ribs are most commonly injured in golfers [17]. This is because compression and tension stresses of the serratus anterior are maximal on the posterolateral segment of the ribs, as demonstrated by a two-dimensional finite analysis of the muscle [26]. The ribs on the leading arm side are most commonly involved, most likely because of constant moderate activity of the serratus muscle through all phases of the golf swing on the leading side compared with the trailing side where the muscle is primarily activated only during the acceleration and early follow-through phase of the swing, as shown in an electromyographic study [27]. The constant activity of the serratus anterior muscle on the leading side may make it more susceptible to fatigue and decrease its ability to protect the ribs from stress fractures [27]. Therefore, these authors recommend a strengthening and endurance training program to prevent fatigue of this muscle [27]. Overall, rib fractures usually heal uneventfully with reduction or elimination of the inciting activity for 4 to 6 weeks [18]. Sport-specific training and endurance programs as well as correction of faulty mechanics should be included in the rehabilitation once the fracture has healed. SCAPULA Stress fractures of the scapula in athletes are rare. There have been four reported cases in the literature: a gymnast, a jogger using hand-held weights, a professional American football player with a stress fracture at the base of the acromial process, and a trap shooter with a fracture in the coracoid process [4,28–31]. The jogger had been jogging with weights for an 8-week period when he presented with a 2-week history of shoulder pain [29]. A bone scan revealed a linear band of increased uptake in the superomedial portion of the scapula, which was later present on plain radiographs. The authors theorized that the likely cause was overuse of the supraspinatus muscle in stabilizing the humeral head while the patient was jogging with weights. The football player was an offensive lineman with no history of trauma, who developed pain in his shoulder during a game [30]. The patient had point tenderness over the acromion, and plain radiographs revealed an incomplete transverse radiolucent line in an area of sclerotic bone at the underside of the acromion near its origin from the scapular spine. A bone scan also revealed increased activity in this area. Weightlifting and football activities were subsequently discontinued for 6 weeks, followed by a gradual resumption of

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weightlifting and contact activities. Within 2 months, the patient had returned to football without any pain. The authors suggest that an intense weightlifting program contributed to the development of the stress fracture. The professional trapshooter was shooting trap regularly at the rate of 200 to 1000 rounds per week when she noticed an aching sensation in her shoulder where the butt of the rifle rests [31]. The patient had pinpoint tenderness over the coracoid process and had pain in this area with resisted adduction and flexion of the shoulder. A plain radiograph axillary view revealed a fracture through the mid portion of the base of the coracoid process. The patient was then treated with rest from trap shooting, followed by a gradual resumption of shooting when she was asymptomatic. CLAVICLE Clavicular stress fractures have been reported in a javelin thrower, a rower, a gymnast, a diver, a weight lifter, a human tower stuntman, and a baseball player [32–38]. The fractures in the rower and gymnast involved the medial third of the clavicle [33,34]. The lightweight rower presented with increasing pain in her medial clavicular area after rapidly increasing her training intensity over a 3- to 4-week period, after a 5-month period of rest [33]. Plain radiographs demonstrated a right medial clavicular fracture, just lateral to the sternoclavicular joint. The patient was treated with cessation from rowing activity and a short course of physical therapy to improve posture, scapulothoracic mechanics, and rotator cuff strength until she was pain free, followed by a progressive increase in rowing. After 2 months from the time of diagnosis of the fracture, the rower returned to full competition. The authors suggest that the fracture was a result of the resumption of high-energy cyclic loading without prior strengthening and stabilization of the torso and upper extremity, leading to muscular imbalance and subsequent stress fracture. Muscular forces working on the clavicle include the pectoralis major and deltoid muscles that produce primarily a downward force, which is counteracted by the forces produced by the sternocleidomastoid and trapezius muscles. During the drive phase of the rowing stroke, the clavicle is elevated, rotated, and drawn posteriorly. Significant bending, shear, and torsional forces can develop across the bone, particularly if there is any imbalance in muscular contraction. The motion of the sternoclavicular and acromioclavicular joints helps dissipate this energy, but if these forces exceed the ultimate tensile strength of the bone or cause fatigue through repeated loading, a fracture can occur. The gymnast was a 10-year-old female who presented with a 6-week history of medial clavicular pain [34]. Radiographs revealed a nondisplaced medial third clavicular fracture. The patient was treated with rest, and, after 4 weeks, she was asymptomatic, with plain radiographs revealing a bridging callus across the fracture site. Again, the authors attribute the fracture to the forces of the sternocleidomastoid and pectoralis major muscles on the medial third of the clavicle.

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The diver was a collegiate platform diver who presented with a several-month history of clavicular pain [35]. Radiographs and bone scans revealed a fracture of the mid clavicle, which eventually healed with rest. The authors partially attribute the fracture to an open-hand entry diving technique, which is more traumatic on the wrist than a closed-hand technique. Theoretically, these repetitive increased forces radiate up the arm to the mid portion of the clavicle, which bears the greatest load of the clavicle, resulting in a fatigue fracture. The fracture in the female weight lifter involved the distal clavicle [36]. The symptoms occurred after several months of lifting but, unlike the above fractures, did not heal with conservative management. A distal clavicle excision was eventually performed, and the patient’s symptoms resolved. The authors propose a mechanism similar to that of distal clavicle osteolysis, in which repetitive weight lifting caused subchondral structural fatigue of the distal clavicle, resulting in a fracture. HUMERUS Stress fractures have been described in baseball pitchers, a tennis player, a javelin thrower, a body-builder, weight lifters, a softball player, and a cricket player [39–49]. Humeral stress fractures in throwing athletes such as baseball pitchers most commonly are spiral fractures that involve the middle and distal third of the humerus [40,43–46]. These fractures predominate in two main age groups: adolescent Little League pitchers and healthy middle-aged pitchers [44–46], although, Polu and colleagues [40] reported a nondisplaced fracture in a collegiate pitcher. The most likely explanation for stress fractures in the adolescent age group is a high level of activity, which places a high degree of stress on immature bone, aggravated by growth spurts and inadequate muscular development [4,47]. The authors in one study believe that in the middle-aged pitchers, the most probable reason for these fractures was muscle fatigue caused by a prolonged layoff from pitching and a lack of a preseason conditioning and a regular exercise program [46]. The axial loads applied to the humerus generated by the biceps and triceps muscles during pitching serve as stress protection against torsional forces placed on the humerus [50]. Therefore, when these muscles are fatigued by overuse and lack of conditioning, more torsional stress is placed on the humerus, predisposing it to stress fracture. These athletes present with either an acute onset of pain or a “pop” sound after a period of prodromal throwing arm pain or with an insidious onset of increasing arm pain if the fracture is incomplete or nondisplaced [40,43–46]. Plain radiographs most commonly reveal the fracture, especially if it is complete and displaced (Fig. 1). In incomplete fractures, plain radiographs may reveal only subtle cortical hypertrophy [40]. In these cases, radionuclide imaging or MRI may be needed to aid in the diagnosis. MRI will show a linear zone of decreased signal intensity within the cortex or medullary cavity or both on T1-weighted scans and increased signal in the medullary cavity on T2-weighted images. MRI also can help in determining the stage of the injury, with more recent injuries having increased signal on the T2-weighted views.

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Fig. 1. Plain radiograph of a minimally displaced spiral stress fracture of the humeral shaft in a baseball pitcher.

Treatment is determined by many factors, including the age of the patient and degree of fracture displacement. Adolescent patients and those with nondisplaced fractures often can be treated nonsurgically with a cuff and collar for 1 week, followed by a fracture brace until the fracture heals clinically and radiographically. Patients with displaced fractures often require open reduction and internal fixation. Preventive measures include a well-structured preseason strengthening and conditioning program. The stress fractures seen in the weight lifters were transverse and involved the proximal humeral shaft [41,42]. Both patients complained of proximal arm and anterior shoulder pain, which occurred during bench press exercises for a period of time before presentation. One patient presented with a transversely oriented radiolucency in the proximal humerus, suggestive of cortical lysis with surrounding periosteal reaction, whereas the other patient presented with a transverse fracture of the proximal diaphysis with greater than 50% displacement. The former patient was treated with cessation of weight lifting for 8 weeks, followed by a gradually progressive supervised training program. The latter patient was treated with surgical fixation with an intramedullary nail. In terms of the mechanism of injury, these fractures were transverse in nature, suggesting a bending force rather than a rotational force, and occurred anatomically between the insertions of the pectoralis major and deltoid muscles. During bench pressing, the humerus is exposed to mechanical forces generated by the supporting musculature of the shoulder girdle and the weight being lifted [41]. The muscles are able to dynamically redistribute these forces across the bone, allowing the bone to endure more stress and load. However, with muscle fatigue, the “stress shielding” effect of the muscles is diminished, which predisposes the bone to fracture. OLECRANON Four distinct types of olecranon stress fractures have been reported in the literature. Two fracture types occur in skeletally mature athletes, fractures of the olecranon tip and oblique fractures through the midportion of the olecranon; and two types occur in skeletally immature athletes, transverse fractures and osteochondroses [4,51–53]. Tip fractures occur in the proximal third of the olecranon and are seen typically in throwers [54]. Slocum [55] theorizes that the

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fractures could result from either impingement of the olecranon in its fossa, caused by hypertrophy of the osseous structures in the pitching arm, or from repeated stresses exerted on the olecranon by the pull of the triceps. These fractures are prone to nonunion and may be treated best with surgery, either by open reduction and internal fixation or by tip excision, depending on the size of the fragment [53,54]. Stress fractures involving the middle third of the olecranon have been reported in baseball pitchers, javelin throwers, and weight lifters [53,54,56–62]. These fractures result from the impaction of the medial olecranon onto the medial wall of the olecranon fossa from valgus forces [63]. Repetitive valgus stresses to the elbow may result in the tensile failure of the trabecular bone of the posteromedial olecranon [58,63]. With continued throwing or lifting, this failure may progress to a stress fracture. These patients usually present with posteromedial elbow pain during the acceleration and follow-through phases of the throwing motion. On physical examination, there is tenderness over the posteromedial elbow, and the pain is reproduced with valgus stress testing or forced hyperextension of the elbow. Plain radiographs are often negative or show very subtle findings such as periosteal reaction over the medial olecranon [58,59]. MRI findings range from poorly defined, patchy areas of low signal intensity on T1-weighted images and areas of high signal intensity on T2-weighted images if an acute stress reaction is present to more focal linear areas of intermediate signal throughout the cortex and subjacent cancellous bone of the articular surface of the proximal ulna in patients with more discrete macroscopic incomplete stress fracture lines (Fig. 2) [58]. Treatment consists of a period of rest and avoidance of throwing and other forms of valgus stress for at least 6 weeks. Schickendantz and colleagues [58] also suggest using a custom-fabricated, hinged elbow orthosis set from 20°

Fig. 2. (A) T2-weighted sagittal view MRI of an incomplete valgus stress-induced olecranon stress fracture in a collegiate baseball pitcher, indicated by the black box. (B) T2-weighted coronal MRI view of the same olecranon stress fracture.

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short of extension to full flexion for the first 4 weeks to protect the elbow from full extension. At 6 weeks, sport-specific functional rehabilitation is started, followed by an interval-throwing program at 8 weeks. After completion of the throwing program, which requires approximately 4 to 6 weeks, the patient is allowed to return to play. Most of these fractures heal with nonsurgical management, but occasionally, open reduction and internal fixation is required [57–59]. There are two types of adolescent olecranon stress injuries, transverse growth plate fractures and osteochondroses [51]. Transverse physeal fractures and osteochondroses may be caused by an extensor overload of the triceps at the weak area of the olecranon, the physis [55]. The physis is injured by repeated forceful contractions of the triceps, resulting in transient localized ischemia in the olecranon physis and apophysis, which leads to disturbed ossification and fragmentation, a condition known as olecranon apophysitis or olecranon osteochondritis [4,55]. When the apophysis is more mature but not yet fused, the same forces may result in a transverse stress fracture through the growth plate. These injuries have been reported in young gymnasts, adolescent baseball pitchers, and an adolescent wrestler [51,52,64–66]. These patients present commonly with chronic, dull elbow pain and have tenderness over the olecranon. Plain radiographs reveal a widened olecranon epiphyseal plate, often with fragmentation of the olecranon apophysis. Treatment is initially nonsurgical with rest from the offending activity until the patient is asymptomatic. Rarely, the patient remains symptomatic, and a nonunion of the growth plate develops [52,64,66]. These patients are treated with open reduction and internal fixation, with bone grafting of the growth plate to promote fusion. ULNA Stress fractures of the ulna have been described in baseball and softball pitchers, tennis players, volleyball players, weight lifters, bowlers, riflemen, a golfer, a polo player, a kendo player, and a baton twirler [67–82]. These athletes present with pain in the region of the ulnar shaft during and after activities and, on physical examination, have tenderness over the ulnar shaft. Radiographs demonstrate either a small crack in the cortex or subtle periosteal reaction at the site of the fracture. Radionuclide imaging or MRI is used to confirm the diagnosis. All of the reported cases have healed with nonsurgical management, which includes rest from the offending activity for a period of 6 to 8 weeks. Mutoh and colleagues [71] have reported two ulnar stress fractures, one in a fast-pitch softball pitcher and one in volleyball player, both of whom experienced pain with underhand maneuvers. Both actions involved repetitive movements of the limb, with a light load following contraction of the wrist flexors. The authors state that the fracture was more proximal in the volleyball player, in which the wrist flexion was more prominent. Tanabe and colleagues [72] have presented three cases of ulnar stress fractures in fast-pitch softball pitchers. The authors state that the windmill softball delivery results in a strongly pronated forearm. Because of the relatively restricted rotatory motion at the distal radioulnar joint and proximal ulnohumeral joint, the ulnar rotation is restricted,

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allowing a strong revolving force of the radius to possibly act on the ulna. Morphologically, the middle third of the ulna has the thinnest cortex and smallest cross-sectional area compared with the proximal and distal ulna and has a triangular shape, which is less resistant to torsional stress. Therefore, large repetitive pronation torsional forces act on the weakest portion of the ulna shaft, which can result in a stress fracture of the middle third. Bollen and colleagues [67] have reported two cases of stress fracture in the nondominant-sided ulna in tennis players who use a double-handed backhand stroke. These authors describe a similar mechanism of repetitive excessive pronation as reported by Tanabe and colleagues [72] in their softball pitchers. In other case reports of nondominant ulnar stress fractures in tennis players, Rettig [83] and Young and colleagues [68] theorize that the mechanism of injury is repetitive impact loading of the forearm during the ball strike. Bell and Hawkins [69] have described a tennis player who developed a nondominant-sided distal ulnar stress fracture after using a double-handed backhand technique. The authors propose a hyperdorsiflexion mechanism of injury, which stresses the ulnocarpal joint and distal ulnar diaphysis. To obtain top spin, the racket head is dropped and brought backward, which results in a maximally dorsiflexed wrist position at the point of ball impact, which stresses the distal ulna. To help counteract this force, the authors used a dorsally applied wrist extension block splint on a temporary basis to prevent additional stress on the ulna. Escher [73] has presented a bowler who developed an ulnar stress fracture while using a heavy, fingertip ball. The author states that, with the fingertip grip, the distal interphalangeal joints of the third and fourth digits are flexed to hold the bowling ball along with the thumb. Therefore, the flexor digitorum profundus muscle is activated repetitively, which results in repetitive stress on the ulnar origin of the muscle and predisposes this area of the bone to stress fracture. Koskinen and colleagues [74] have reported a case of a golfer who had an ulnar stress fracture. The authors theorize that excessive supination together with overuse of the hand flexor muscles resulted in the fracture. After return to play, the patient’s golf instructor changed the patient’s grip so that the hand and forearm were in less supination. RADIUS Stress fractures of the radius have been described in gymnasts, a tennis player, a pool player, a cyclist, and a badminton player [83–91]. Stress fractures of the distal radial growth plate are seen frequently in young gymnasts [83,84,87,89]. Ahluwalia and colleagues [88] have reported a skeletally mature female gymnast who presented with bilateral radial stress fractures, which were diagnosed by radionuclide imaging. Loosli and Leslie [85] have described a female tennis player in her 20s who developed increasing dominant-sided wrist pain. Plain radiograph results were normal; however, a bone scan revealed a distal radius stress fracture. The patient was subsequently placed in a short arm cast for 3 weeks, followed by a posterior splint for 3 more weeks. After the

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immobilization period, the subject began a strengthening program using latex tubing. The patient began hitting the tennis ball at 8 weeks and had returned to full competition by 3 months. Orloff and Resnick [90] have presented a pool player who developed a distal third radial shaft fracture after playing multiple rounds of pool over an extended period of time. Radiographs revealed a periosteal reaction over the distal radius. After 16 weeks, the patient’s pain subsided, and radiographs revealed a healed fracture. Caine and colleagues [83] studied growth plate changes in young competitive gymnasts. They noted that widening and irregularities of the distal radial physis were the first changes to appear in a spectrum of abnormal changes secondary to overuse and probably represented a stress fracture of the distal radial growth plate. These changes were associated with injury and were not normal adaptive changes seen in asymptomatic gymnasts. The fractures, seen radiographically, may appear to be only Salter-Harris type I or II fractures; however, they actually may involve more significant growth plate injury. Long-term complications may include symmetrical and asymmetrical growth plate retardation, positive ulnar variance, and associated pathoanatomic sequelae. SCAPHOID Two cases of scaphoid stress fractures have been reported in the literature: one in an adolescent badminton player, associated with an ipsilateral distal radial epiphysiolysis, and one in a young gymnast who actually developed bilateral scaphoid stress fractures [86,92]. In the case of the gymnast, repetitive abduction and dorsiflexion movement of the wrist was implicated as a possible mechanism of injury [92]. In the badminton player, the authors propose that repeated shearing and torsional forces by excessive wrist movement from hitting the shuttle caused the stress injury [86]. METACARPALS Metacarpal stress fractures are rare but have been reported in a softball pitcher, tennis players, and a rower [93–96]. The second metacarpal was affected in both of the tennis players [94,96]. The authors in both of these tennis case studies suggest that increased training intensity combined with changes in stroke biomechanics and racket grip predisposed the second metacarpals to fracture. The movement of the second carpometacarpal joint is relatively limited, except for flexion and extension. This, in turn, may result in more stress being placed on the second metacarpal compared with the more mobile lateral metacarpals [4]. The softball pitcher developed a fifth metacarpal stress fracture [93]. The authors postulate that the abduction forces involved in the grip and release of the softball along with the muscle pull exerted by the extensor carpi ulnaris in gripping a softball may have played a role in overloading the normal dynamic balance of bony resorption and formation in the fifth metacarpal, resulting in a fracture.

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The collegiate rower had a fourth metacarpal stress fracture [95]. The authors state that the pathogenesis of this fracture was related to the large mechanical forces transmitted from a gripped object. This may have been accentuated by poor grip and rowing mechanics. All of the fractures healed with a period of relative rest followed by a gradual rehabilitation program. In addition, changes in techniques, equipment, and grip facilitated the return to competition. PHALANGES Chell and colleagues [97] have reported bilateral Salter-Harris type III stress fractures at the bases of the middle phalanges of the middle fingers, occurring in an adolescent climber. The avid climber presented with a 1-week history of pain and swelling in his middle fingers, which was spontaneous in onset and without any direct trauma. Plain radiographs revealed each of these fractures; one fracture was nondisplaced, whereas the other was minimally displaced. MRI confirmed the diagnosis. The patient was treated conservatively, with relative rest from offending activities, and eventually became asymptomatic at 12 months. The proposed mechanism of injury was the prolonged gripping action required in rock climbing, with the metacarpophalangeal joint in extension and the interphalangeal joints in flexion. The prolonged activation of the finger extensors in this position resulted in the fractures. SUMMARY Although they are less common than lower-extremity stress fractures, upperextremity stress fractures are becoming recognized much more frequently. A majority of these fractures are caused by overuse and fatigue of the surrounding musculature and, as a result, may be prevented by appropriate training and conditioning. The diagnosis is made by obtaining a medical history and a physical examination with the aid of plain radiographs, bone scans, and MRI. Most of these fractures heal with a period of relative rest followed by a structured rehabilitation program. A small percentage of these fractures, however, may require surgical fixation. References [1] Matheson GO, Clement DB, McKenzie DC, et al. Stress fractures in athletes: a study of 320 cases. Am J Sports Med 1987;15:46–58. [2] Brukner P. Stress fractures of the upper limb. Sports Med 1998;26:415–24. [3] Iwamoto J, Takeda T. Stress fractures in athletes: review of 196 cases. J Orthop Sci 2003; 8:273–8. [4] Sinha AK, Kaeding CC, Wadley GM. Upper extremity stress fractures in athletes: clinical features of 44 cases. Clin J Sports Med 1999;9:199–202. [5] Keating TM. Stress fracture of the sternum in a wrestler. Am J Sports Med 1987;15:92–3. [6] Barbaix EJ. Stress fracture of the sternum in a golf player. Int J Sports Med 1996;17:303–4. [7] Robertson K, Kristensen O, Vejen L. Manubrium sterni stress fracture: an unusual complication of non-contact sport. Br J Sports Med 1996;30:176–7. [8] Holden DL, Jackson DW. Stress fractures of the ribs in female rowers. Am J Sports Med 1985;13:342–8.

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