A stress fracture can be a season-ending, even a career-ending, injury for the female athlete. It is essential that clinicians caring for athletes at risk of injury are knowledgeable about the appropriate evaluation and treatment of injuries, and are aware of the factors that contribute to injury. Athletes who participate in weight-bearing impact exercise such as running are at greatest risk. The presence of the female athlete triad, or any of its components, increases the athlete's risk of stress fracture. Any female athlete with a stress fracture should be evaluated with respect to dietary intake, menstrual function, and previous history of boney injury. Treatment should focus on altering identified risk factors for injury to promote healing, in addition to efforts at maintaining fitness. The vast majority of stress fractures will heal without complication. This article provides an overview of the etiology and epidemiology of stress fractures in athletes, followed by a discussion of evaluation and treatment principles that should be considered when caring for the female athlete with stress fracture.
Etiology of Stress Fractures
Stress fractures result from an imbalance in the bone remodeling process. With repetitive stress to a bone over time, new bone deposition cannot keep up with the damage from the stress and bone resorption. This dynamic process often takes place insidiously. Stress fractures differ from acute fracture, in which bone gives way suddenly when an applied force exceeds the composite strength of the bone at that moment in time. Bone homeostasis includes a process of continual remodeling. When a particular bone is stressed, the bony architecture is changed to add strength against the stress. Wolff's law states that every change in form and function of a bone, or in its function alone, is followed by certain definite changes in the bone's internal architecture and equally definite secondary alteration in its mathematic laws . Thus, bone deposition and resorption are governed by stress placed upon it. This process of remodeling, however, takes time, and a stress fracture can occur if the cumulative stress exceeds the strength of the bony architecture. A stress fracture then is a maladaptive response to abnormal doses of stress .
Stress fractures have been classically been divided into two categories: fatigue fractures or insufficiency fractures. The difference between the two involves both the underlying bone quality and the nature of the stress applied. Fatigue fractures are a result of an abnormal stress applied to a normal bone. Insufficiency fractures are a result of normal stress applied to abnormal bone [3••].
Many theories attempt to explain the physiologic process that regulates bone adaptation to physiologic stress. Though they differ in describing the triggers of osteoclastic and osteoblastic activity, they seem to agree that with a stress fracture, over time, these two processes become imbalanced. Stress fractures are the end result of a process. Knapp and Garrett  stress that stress fractures must be considered as an injury spectrum (from stress response to stress fracture) because all do not progress to the point of actual disruption of bony cortices and intramedullary changes that are detectable on radiographs .
Though the exact mechanisms that regulate bone homeostasis may not be completely understood, many risk factors have been defined as predisposing individuals for developing a stress fracture. These risk factors can be separated into two general categories, intrinsic and extrinsic. Both play a role in the injury spectrum of a stress fracture. Intrinsic factors may include bone size and density, nutrition and hormonal influences, anatomy and biomechanics, age, and overall conditioning . Extrinsic factors may include training errors, sport-specific repetitive forces, training surface, or equipment failure.
Patients can present with any combination of these risk factors. The female athlete triad is a well-described example in which a patient with a group of risk factors (amenorrhea, eating disorders, and premature osteoporosis/stress fractures) has shown an increased rate stress fractures . Identification of these risk factors is important, in that an intervention may stop or reverse the injury spectrum of stress fractures. Knapp and Garrett  state that by modulating the application of stress in a judicial manner, the injury is preventable. Adequate adaptive response requires that stress be applied in a cyclic fashion, alternating with periods of rest .
Epidemiology of Stress Fractures
Stress fractures were first described in 1855 by Breihaupt, who reported march fractures in the metatarsals of Prussian army recruits after long marches. In addition, stress fractures have been reported in men and women and in most sports such as running, gymnastics, basketball, rowing, and dancing. The incidence of stress fractures has been stratified by sex, age, race, risk factors, and specific anatomic fracture sites. Intuitively, the weight-bearing bones exposed to the repetitive forces that occur in sports should have the highest incidence of stress fractures. And in fact, about 95% of stress fractures occur in the lower extremities [3••]. In a study of 320 cases of stress fractures confirmed by bone scan and stratified by location, Matheson et al. [6•] revealed the following results: 49.1% tibia, 25.3% tarsals, 8.8% metatarsals, 7.2% femur, 6.6% fibula, 1.6% pelvis, and 0.9% sesamoids.
Currently, running generates the highest reported incidence of stress fractures, accounting for 4.4% to 15.6% of all injuries to runners [6•]. Prior to the popularity of running, however, metatarsals were the most common location of stress fracture [3••].
Stress fractures are not exclusive in weight-bearing bones. Any bone with a repetitive force applied is susceptible. Stress fractures have been noted in case reports in non–weight-bearing bones, including the ribs in rowers or the first rib in throwing athletes [7,8].
When stratified by sex, women are more likely to develop a stress fracture than men. After following a group of 310 army basic trainees, Jones et al.  reported that women had a significantly higher incidence of injuries including stress fracture resulting in time loss than men (44.6% compared with 29.0%). In an earlier study on lower extremity injuries, Shaffer et al.  found that 12.3% of the women had a stress fracture compared with 2.4% of the men. Women with menstrual abnormalities have shown a strong association with stress fracture occurrence. In a 1988 study of a group of 240 college runners, Jones and James  found that stress fractures occurred in 49% of the women with very irregular menses (0–5 menses/year), 39% of the women with irregular menses (6–9 menses/year), and 29% of the women with regular menses (10–13 menses/year). It was also noted that runners who had never used oral contraceptives were more than twice as likely to have had a stress fracture when compared with runners who had used oral contraceptives for more than 1 year.
In both men and women, overall conditioning is a major factor in the occurrence of stress fractures. Unconditioned persons are more likely to suffer a stress fracture when undertaking a new exercise program. In a group of 1286 US Marine Corps recruits, Barrow and Saha  tried to develop a screening tool to separate persons at high risk for training injuries and showed 21.6% of high-risk subjects suffered more than three times as many stress fractures as low-risk subjects. Beck et al.  evaluated a group of 693 female Marine recruits and compared their findings with an earlier study with 626 male recruits. They found that in both sexes, the fracture cases were less physically fit compared with controls.
The overall fitness level and fitness education of persons participating in sporting activities is also a factor in stress fracture occurrence. However, the most important risk factor for stress fractures may be training errors. In his 1987 survey of athletes, Matheson et al. [6•] found 22.4% of stress fractures occurred as a result of training errors.
Evaluation and Treatment of Stress Fractures in the Female Athlete
The clinician's responsibility in evaluating the female athlete with a presumed stress fracture is to assess the situation like a detective. Diagnosis can be challenging, especially early on in the course of injury, and in the athlete presenting with vague symptoms. Furthermore, it is essential to determine why the athlete developed the injury. Thus, evaluation of the female athlete presenting with a presumed stress fracture should focus not only on diagnosis, but on the various etiologies as discussed earlier.
Diagnosis is generally accomplished through a combination of clinical history, with physical and radiologic evaluations. The history should focus on identifying the various etiologies of injury—the intrinsic and extrinsic factors. In many athletes, a number of factors may be contributing to the development of a stress fracture. For example, the athlete presented by Cooper and Joy  (elsewhere in this issue), whose contributing factors included weight loss (negative energy balance), menstrual dysfunction, and diminished bone mineral density.
Intrinsic abnormalities may play a greater role in the development of stress fractures in female athletes compared with male athletes . The female athlete triad describes the relationship between disordered eating, menstrual dysfunction, and negative bone mineral balance. These three conditions combined with repetitive weight-bearing exercise can result in stress fractures. Many studies have examined the relationship between the triad and subsequent development of stress fracture [16••,17]. It is essential that the clinician evaluating the female athlete with a suspected stress fracture enquire about her body weight, eating habits, current and past menstrual function, and bone health. Table 1 lists a series of questions that allow the clinician to initially evaluate the athlete for the presence of the female athlete triad.
Research has found that low body mass index (BMI) , menstrual irregularity [16••,18••], and diminished bone mineral density (BMD) , all increase a woman's risk of suffering a stress fracture.
Biomechanical abnormalities represent another group of intrinsic factors that can impact an athlete's risk of stress fracture. Pes cavus, leg length inequality, and excessive forefoot varus were found to increase the risk of multiple stress fractures in an analysis of injuries in 31 athletes [18••]. In a study that retrospectively evaluated 2002 running injuries, 30% of runners with a tibial stress fracture had varus knee alignment, compared with only 17% with valgus knee alignment. In the same study, foot type (pes planus or pes cavus), patellar squinting, high Q angle, and leg length discrepancy had no influence on the incidence of tibial stress fractures .
Athletes presenting with presumed stress fracture (especially of the low back, hip, pelvis, and lower extremity) should undergo an evaluation of their kinetic chain to identify potentially contributing biomechanical factors. Extrinsic factors are another contributor to the development of stress fracture. Training errors, such as the “too much, too soon” scenario, loom large. This has been especially true in the military, where unconditioned recruits undergo a period of basic training, and women recruits seem to be especially vulnerable . In running athletes, stress fracture incidence increases with increasing mileage [18••]. Worn or poorly fitting footwear may contribute as well, especially in running athletes. Runners should have their shoes fit by an experienced salesperson that can help determine the right shoe for their foot type. It is generally recommended that runners change out their training shoes every 300 to 400 miles. Larger athletes may need to change more quickly.
Physical and radiologic examination
On physical examination, the athlete may have tenderness to palpation and localized swelling depending on the location of injury. Other tests of bone stress such as a single leg hop for lower extremity injuries, oblique spinal hyperextension for stress fractures of the pars intra-articularis, and the tuning fork test, among others, can be helpful clinically.
The radiologic evaluation provides a definitive diagnosis. Early in the natural course of the injury, plain film radiographs are typically normal. Depending on the location of injury, plain films may not be revealing regardless of the duration of symptoms. Various studies have looked at other imaging modalities including nuclear medicine bone scans, CT scans, and MRI. Bone scans are highly sensitive for acute boney injury, but have low specificity. CT scans can be helpful in visualizing the anatomy of a known injury especially if surgical intervention is being considered . More recently, MRI has been used to detect injuries early, and to guide prognosis. However, a recent study found that 43% of 21 aymptomatic runners had abnormal MRI images of their lower extremity, suggesting that the use of this technology in the absence of a thorough clinical evaluation may be misleading .
A reasonable approach to imaging the patient with suspected stress fracture depends on the location and duration of symptoms. Stress fractures of the hip and pelvis can be difficult to visualize on plain films as well, and typically will require further radiologic testing to identify them. With respect to duration, in patients whose symptoms have been present for less than 2 weeks, plain film radiographs are not likely to demonstrate evidence of a stress fracture. If the clinical history, physical examination and plain film radiographs are consistent with stress fracture, no further imaging is likely necessary. Exceptions to this recommendation would include injuries that might require surgical intervention such as anterior tibial stress fractures or tension-side fractures of the femoral neck, in which an evaluation of the injury/anatomy is essential.
Patients with negative plain film images where the location of injury (eg, tibia, fibula, metatarsal) is fairly certain, should undergo MRI to further evaluate their injury. Patients whose pain is not as well localized, may benefit from a bone scan to localize the source of pain. MRI may then be utilized to image the lesion for greater detail.
Treating athletes with stress fractures usually calls for rest from the aggravating activity. Most injuries will heal in 6 to 8 weeks, but athletes with a less severe fracture may be able to return to sports sooner. Depending on symptoms, certain stress fractures with low risk of complication, such as fibular stress fractures, may not even be a contraindication to further participation during an athlete's competitive season. High-risk injuries, such as anterior tibial stress fractures, femoral neck stress fractures, and fractures to the base of the fifth metatarsal, are at greater risk of complication. Healthcare providers who lack expertise in the management of these injuries should refer patients to a sports medicine or orthopedic specialist.
Athletes can continue with alternative exercise programs during the recovery phase. Depending on the location of injury and level of pain, alternative activities may include swimming, water running, cycling, elliptical trainer, and weight training. Competitive athletes can reproduce their regular workouts in the alternative setting. For example, a track athlete whose Monday workout should consist of 12 400-meter repeats at 75% effort, can do a similar workout in the pool using time, heart rate, and perceived exertion as a guide.
An essential component of treatment is to address predisposing factors. Biomechanical abnormalities should be addressed and corrected. If the athlete has been identified as having features of the female athlete triad, she should begin treatment for this with an experienced treatment team. This team should consist of a physician, mental health professional, and sports nutritionist. Previous articles have addressed the team treatment of disordered eating in detail [23•].
The treatment of associated menstrual disturbance remains controversial. The key to the normalization of menses is to restore normal body weight and achieve positive energy balance. This is a challenge to accomplish in this population. The question remains, “What to do in the meantime?” Although studies have not definitively shown a benefit from hormone replacement in this population, it is reasonable to consider the use of oral contraceptives (OCPs) as a way to replace estrogen and progesterone. However, given the other hormonal abnormalities associated with negative energy balance, OCPs cannot restore all of the deficient hormones.
Some women with prolonged amenorrhea can exhibit significant bone loss, whereas others have very little. Stress fracture is an obvious consequence of bone loss combined with weight-bearing impact exercise. Athletes who have been amenorrheic for 6 months or more should undergo an evaluation of their bone mineral density. Dual-energy x-ray absorptiometry (DEXA) is the current gold standard for measuring bone mineral density. Diagnostic criteria for premenopausal women with bone loss were recently revised by the International Society for Clinical Densitometry (ISCD) . Terms such as “low BMD for chronologic age” should be used rather than osteoporosis or osteopenia. That being said, athletes with low BMD and stress fracture clearly have a clinically significant loss of bone mineral density.
Restoration of normal bone mass can be difficult, even impossible, to achieve in athletes who have sustained a significant loss. Keen and Drinkwater  has repeatedly found that the bone loss that occurs within the setting of the female athlete triad is largely irreversible. With restoration of positive energy balance, normal body weight, and normal menstruation, women do see an increase in their BMD. Long-term follow-up of these women as they age and go through menopause will be helpful in determining how aggressive the clinician should be in attempting to restore BMD.
A recent report by Stewart et al.  evaluated the treatment of stress fractures in athletes with intravenous pamidronate. Five intercollegiate female athletes with tibial stress fractures were administered intravenous pamidronate weekly for five treatments. Their main outcome variable was the athletes' ability to continue playing without restrictions. Four of the five athletes were able to continue training and competition within 1 week of treatment. The fifth patient missed only 3 weeks of training. Although this limited case series is not enough to suggest that all athletes should be treated with this regimen, this treatment modality certainly deserves further study. Athletes should also be encouraged to increase their calcium intake to achieve 1500 mg/d through diet and/or supplements.
Immobilization has a limited role in stress fracture treatment. A recent study examining the role of pneumatic leg brace in the treatment of tibial stress fractures in military recruits found no added benefit when comparing braced with nonbraced (control) athletes . Given their increased risk of nonunion, stress fractures of the proximal fifth metatarsal require immobilization for 6 to 12 weeks, and in some cases, surgery. One can also consider immobilization in high-risk patients who have underlying medical conditions that could negatively impact fracture healing, and in those athletes who may struggle with compliance regarding relative rest.
Stress fractures are a common injury, seen most often in runners and military recruits. Both intrinsic and extrinsic factors play a role in their occurrence. It is essential that women presenting with stress fracture undergo evaluation for the female athlete triad, keeping in mind that all three components of the triad do not need to be present to increase a woman's risk of fracture. Advanced imaging techniques such as MRI, bone scan, and CT scan are often needed to further evaluate the injury after a thorough clinical evaluation. It is important to keep in mind that MRI results can be misleading due to its high sensitivity.
Treatment largely consists of relative rest, maintenance of fitness, and addressing those intrinsic and extrinsic factors that contributed to the development of injury. Providers who lack experience in the management of high-risk fractures should refer those patients to a more experienced practitioner.
Preventive measures are really the key in protecting against stress fractures. Gradual increases in training, appropriate footwear for an athlete's foot type and sport activity, and appropriate energy balance will likely prevent the majority of stress fractures. Athletes, their parents, coaches, and athletic trainers, all need to be aware of the risk of stress fracture associated with weight-bearing impact activities, especially running. Earlier diagnosis will lead to earlier intervention, which in turn can reduce morbidity associated with these injuries.
The authors wish to thank Steve Thiese, MS, University of Utah, Department of Family and Preventive Medicine, for his assistance in the preparation of this manuscript.
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