Bone stress injuries (BSIs) are common running injuries and may occur at a rate of 20% annually. Both biological and biomechanical risk factors contribute to BSI. Evaluation of a runner with suspected BSI includes completing an appropriate history and physical examination. MRI grading classification for BSI has been proposed and may guide return to play. Management includes activity modification, optimizing nutrition, and addressing risk factors, including the female athlete triad. BSI prevention strategies include screening for risk factors during preparticipation evaluations, optimizing nutrition (including adequate caloric intake, calcium, and vitamin D), and promoting ball sports during childhood and adolescence.
Key points
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Bone stress injuries (BSIs) are a common form of injury in runners of both sexes.
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Both biological and biomechanical risk factors may contribute to BSI.
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History and physical examination are helpful to diagnose BSI, and MRI may be useful for radiographic confirmation and grading BSI.
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Prevention strategies include screening for risk factors during preparticipation evaluation, promoting optimal nutrition, and encouraging appropriate bone loading activities, including ball sports.
Introduction
Bone stress injuries (BSIs) in runners result from the failure of skeleton to withstand repetitive, submaximal forces from running. BSI can range in severity, with early injuries showing radiographic findings of periosteal edema with varying degrees of marrow edema and more advanced stress fractures showing evidence of a fracture line. Stress fractures account for up to 20% of injuries seen in sports medicine clinic.
Studies suggest the annual incidence of BSI may be greater than 20% in runners and that BSI is a common cause of injury in track and field athletes. Early identification of a BSI is important in management, because delay in diagnosis or continued running may result in a higher-grade BSI that requires longer healing time. This article discusses the incidence and distribution of BSI in runners. It reviews biological and biomechanical risk factors for BSI, with a focus on risk factors that can be efficiently evaluated in the clinic setting. It discusses evaluation and management of BSI by anatomic location and grade of injury by MRI. In addition, it reviews evidence for prevention of BSI in runners.
Introduction
Bone stress injuries (BSIs) in runners result from the failure of skeleton to withstand repetitive, submaximal forces from running. BSI can range in severity, with early injuries showing radiographic findings of periosteal edema with varying degrees of marrow edema and more advanced stress fractures showing evidence of a fracture line. Stress fractures account for up to 20% of injuries seen in sports medicine clinic.
Studies suggest the annual incidence of BSI may be greater than 20% in runners and that BSI is a common cause of injury in track and field athletes. Early identification of a BSI is important in management, because delay in diagnosis or continued running may result in a higher-grade BSI that requires longer healing time. This article discusses the incidence and distribution of BSI in runners. It reviews biological and biomechanical risk factors for BSI, with a focus on risk factors that can be efficiently evaluated in the clinic setting. It discusses evaluation and management of BSI by anatomic location and grade of injury by MRI. In addition, it reviews evidence for prevention of BSI in runners.
Summary/discussion
Incidence and Distribution
The incidence of BSI varies by age and sex. In a study comparing high school sports, female and male athletes participating in cross-country had the first and third highest incidences of injuries at 10.62 and 5.42 per 100,000 athletic exposures, respectively. In a separate investigation, adolescent runners of both sexes sustained stress fractures at a similar rate of approximately 4% to 5% annually. Elite collegiate runners may sustain BSIs at a rate exceeding 20% per year. Common sites for BSI include the tibia, fibula, metatarsals, tarsals, calcaneus, and femur.
Risk factors
Risk factors for BSI can be divided into biological and biomechanical risk factors ( Table 1 ). Genetics are reported to modulate fracture risk. Medications, including steroids, anticonvulsants, antidepressants, and antacids, may impair bone health. Nutritional deficiencies in calcium and vitamin D increase risk for BSI. Female athletes seem to be at greater risk for BSI than male athletes. Sex-specific differences include the female athlete triad (hereafter referred to as the triad), defined as the interrelationship of energy availability, menstrual function, and bone mineral density (BMD). Each aspect occurs on a continuum of health with the most severe form of the triad represented by low energy availability with an eating disorder, functional hypothalamic amenorrhea, and osteoporosis. A female runner may have 1 or more components of the triad, and greater number of triad risk factors has been associated with increased risk for BSI in female athletes.
| Biological Factors | Biomechanical Factors |
|---|---|
| Female sex | Training patterns, including volume or changes in intensity |
| Genetics | Bone characteristics (thinner cortex, lower bone mineral density) |
| Medications (including anticonvulsants, steroids, antidepressants, antacids) | Anatomic considerations (leg length discrepancy, lean mass, foot type, smaller calf cross-sectional area) |
| Female athlete triad (low energy availability, menstrual dysfunction, and low bone mineral density) | |
| Other dietary contributors (insufficient calcium and vitamin D) | — |
In both sexes, prior fracture has been found to be a risk factor for development of BSI in runners. Lower whole body bone mineral content values increase risk for BSI in female runners aged 18 to 26 years. In adolescent female runners, the combination of menstrual irregularities with fracture history was associated with low bone density. The largest study to date in male runners identified lower BMD as an independent risk factor for increased time for healing from a BSI. In addition, athletes with trabecular sites of fracture, including the sacrum, pelvis, and femoral neck, had lower BMDs in the lumbar spine and proximal femur than runners with fractures in cortical sites. In addition to bone density, bone geometric properties may predispose to BSIs, including a thinner cortex of tibia in triathletes and smaller tibial cross-sectional area in runners.
Biomechanical factors can also contribute to BSI. Static alignment and anatomic issues may contribute, including leg length discrepancy, smaller calf girth, and cavus or planus type foot. Dynamic biomechanical loading patterns experienced during running may also contribute to injury. These characteristics have been evaluated primarily in female patients who sustain BSI in the tibia and include greater average vertical loading, higher peak acceleration, and greater peak free mass. Higher peak hip adduction, knee internal rotation, knee abduction, tibial internal rotation, and rear foot eversion may also contribute. Running volumes greater than 32 km (20 miles) per week increase risk for BSI.
Evaluation
Clinical Evaluation
Clinicians should complete a full history and physical examination in runners who present for evaluation of a BSI. A complete running history should be obtained (including changes in running volume, shoe type and duration of use, frequency of racing, and change in foot strike pattern strategy). In female runners, screening for triad risk factors is important, including dietary restriction behaviors, daily servings of foods rich in calcium and vitamin D, menstrual dysfunction, history of fractures, and personal/family history of low BMD. Medications including hormones (oral contraceptive pills, estrogen, progesterone) and historical or current use of medications that influence bone health, including steroids and antacids, should be recorded.
During physical examination, the characteristics of a BSI include focal bony tenderness and pain with direct and/or indirect percussion. Single-leg hop test may be attempted to elicit pain depending on the clinical context. In more advanced cases, local swelling or skin color changes may be noted.
Specific forms of BSI may require additional aspects of the physical examination. In our clinical experience, and based on available research, we recommend clinicians consider the following for specific examination findings based on location of pain.
Sacral/pelvic location
In addition to focal tenderness, sacroiliac joint provocative maneuvers may elicit pain, including thigh thrust; pelvic distraction; pelvic compression; and flexion, abduction, and external rotation of hip (FABER maneuver). Evaluation for a leg length discrepancy may be valuable to correct for biomechanical risk factors contributing to injury.
Femoral neck
Pain may be provoked with hip internal rotation. In addition, evaluate for the presence of femoral acetabular impingement with flexion adduction and internal rotation (FADIR maneuver) because this has been associated with femoral neck BSI.
Lesser trochanter
The clinical evaluation is similar to evaluation for a femoral neck BSI. This injury is typically associated with iliopsoas tendinopathy and is a potentially high-risk injury because it can progress to full fracture.
Femoral shaft
Fulcrum test may localize pain at the site of injury.
Calcaneus
Calcaneal squeeze test may elicit pain and help differentiate from other causes of heel pain, including retrocalcaneal bursitis.
Anatomy and imaging
The anatomic locations for BSI can be divided into high-risk, moderate-risk, and low-risk locations based on time to heal and risk for nonunion ( Table 2 ). Table 2 is based on a modified version of previously published high-risk and low-risk classifications, including a moderate-risk category that may be more challenging to address given biological and biomechanical forces that can contribute to risk for impaired bone healing.
| Low Risk | Medium Risk | High Risk |
|---|---|---|
| Posteromedial tibia Fibula/lateral malleolus Calcaneus Diaphysis of second to fourth metatarsals | Pelvis (sacrum and pubic rami) ∗ Femoral shaft Proximal tibia Cuboid Cuneiform | Femoral neck Patella Anterior tibial diaphysis Medial malleolus Talus (lateral process) |
∗ The pelvis is a controversial anatomical location for determining risk for bone stress injury, but recent research by Nattiv and colleagues showed that time to full return to play is longer in trabecular BSIs.
MRI is commonly used to evaluate BSI because of the value in grading severity of injury and use of nonionizing radiation. Multiple grading systems have been developed. Two MRI imaging grades are shown in Table 3 , including the initial proposed criteria by Fredericson and colleagues that have been most recently updated by Nattiv and colleagues.
| MRI Grade | MRI Grading Scales for BSIs | |
|---|---|---|
| Nattiv et al, 2013 | Fredericson et al, 1995 | |
| 1 | Mild marrow or periosteal edema on T2; T1 normal | Mild to moderate periosteal edema on T2; normal marrow on T2 and T1 |
| 2 | Moderate marrow or periosteal edema plus positive T2 | Moderate to severe periosteal edema on T2; marrow edema on T2 but not T1 |
| 3 | Severe marrow or periosteal edema on T2 and T1 | Moderate to severe periosteal edema on T2; marrow edema on T2 and T1 |
| 4 | Severe marrow or periosteal edema on T2 and T1 plus fracture line on T2 or T1 | Moderate to severe periosteal edema on T2; marrow edema on T2 and T1; fracture line present |
Management
Activity Modification and Aerobic Activity
After the initial healing phase to achieve pain-free ambulation and no pain with provocative maneuvers on physical examination, most athletes initiate a nonimpact loading activity to maintain fitness and strength, including deep water running. Athletes should be counseled to maintain good caloric intake to meet the metabolic demands of cross-training and not inadvertently restrict caloric intake, which may risk delayed healing response. Use of an antigravity treadmill may allow for progressive impact loading to maintain fitness while allowing healing of lower extremity BSIs. We outlined a protocol used at Stanford University for athletes recovering from BSIs using an antigravity treadmill that can modulate forces encountered in the lower extremities to allow for progressive weight bearing.
Ensure Adequate Intake of Calcium and Vitamin D
All athletes with BSIs should be assessed to ensure adequate calcium and vitamin D intake, preferably through diet. Target values published by the Institute of Medicine based on age and sex in 2010 are as follows :
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600 IU of vitamin D daily is recommended for ages 9 to 70 years
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800 IU of vitamin D daily is recommended for ages 71 years or older
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1300 mg of calcium daily for ages 9 to 18 years
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1000 mg of calcium daily for women aged 19 to 50 years and men aged 19 to 70 years
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1200 mg of calcium daily for women aged 51 years and older and for men 71 years and older
Clinicians who suspect low energy availability should refer the runner for a complete nutritional assessment with a registered dietitian. This assessment is best accomplished with a dietician who has sports nutrition background and takes into account sports participation demands, caloric intake, and energy availability, in addition to other important nutrients of bone health. Given the prevalence of vitamin D deficiency, we recommend screening athletes who sustain a BSI by measuring 25-OH vitamin D level and providing supplemental vitamin D if needed to ensure that the runner is not vitamin D deficient. Further studies are needed to assess the relationship with BSIs and vitamin D.
Female Runners: Screening and Management of the Triad
In female runners, screening for the triad is critical for addressing risk factors for BSI and identifying health risks in this population. The Female Athlete Triad Coalition statement in 2014 outlined a risk factor assessment score that can be used to help in treatment and return-to-play guidelines in female athletes. The key component to management of the triad is to ensure adequate energy availability, allow for ovulatory menstrual cycles, and maintain bone mass. In addition to preventing disruptions to training from management of BSIs, female athletes may be motivated by research that suggests that performance improves in athletes who maintain ovulatory function with adequate nutrition. A full description of the evaluation and management of the female athlete triad is described elsewhere. One important consideration is to ensure that female runners understand that adequate energy availability (defined as the difference between energy intake and estimated energy expenditure standardized to fat-free mass per day ) should be maintained both during the healing process and on return to full running. Inadvertent low energy availability may occur if a female runner does not consume adequate calories to meet the metabolic demands of aerobic cross-training activities.
Evaluation of Bone Health in Male Runners
For male runners with diagnosed BSIs in trabecular sites, including the pelvis, sacrum, and femoral neck, practitioners should consider work-up for impaired bone health, including dual-energy X-ray absorptiometry (DXA) to measure BMD and initial endocrine work-up. Athletes with higher-grade BSI assessed by MRI and lower BMD values may have a longer healing time before return to sports. BMD values from DXA in athletes less than 50 years of age should be interpreted using age, ethnicity, and male-sex reference values (Z-scores). The American College of Sports Medicine defines Z-score less than −1 as low bone mass in female athletes participating in weight-bearing sports, although criteria have not been defined for male athletes. The International Society for Clinical Densitometry defines Z-scores less than −2 as low bone mass for age in both sexes.
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