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Bone Stress Injuries in the Military: Diagnosis, Management, and Prevention
Take-Home Points
- Stress injuries, specifically of the lower extremity, are very common in new military trainees.
- Stress injury can range from benign periosteal reaction to displaced fracture.
- Stress injury should be treated on a case-by-case basis, depending on the severity of injury, the location of the injury, and the likelihood of healing with nonoperative management.
- Modifiable risk factors such as nutritional status, training regiment, and even footwear should be investigated to determine potential causes of injury.
- Prevention is a crucial part of the treatment of these injuries, and early intervention such as careful pre-enrollment physicals and vitamin supplementation can be essential in lowering injury rates.
Bone stress injuries, which are common in military recruits, present in weight-bearing (WB) areas as indolent pain caused by repetitive stress and microtrauma. They were first reported in the metatarsals of Prussian soldiers in 1855.1 Today, stress injuries are increasingly common. One study estimated they account for 10% of patients seen by sports medicine practitioners.2 This injury most commonly affects military members, endurance athletes, and dancers.3-5 Specifically, the incidence of stress fractures in military members has been reported to range from 0.8% to 6.9% for men and from 3.4% to 21.0% for women.4 Because of repetitive vigorous lower extremity loading, stress fractures typically occur in the pelvis, femoral neck, tibial shaft, and metatarsals. Delayed diagnosis and the subsequent duration of treatment required for adequate healing can result in significant morbidity. In a 2009 to 2012 study of US military members, Waterman and colleagues6 found an incidence rate of 5.69 stress fractures per 1000 person-years. Fractures most frequently involved the tibia/fibula (2.26/1000), followed by the metatarsals (0.92/1000) and the femoral neck (0.49/1000).6 In addition, these injuries were most commonly encountered in new recruits, who were less accustomed to the high-volume, high-intensity training required during basic training.4,7 Enlisted junior service members have been reported to account for 77.5% of all stress fractures.6 Age under 20 years or over 40 years and white race have also been found to be risk factors for stress injury.6
The pathogenesis of stress injury is controversial. Stanitski and colleagues8 theorized that multiple submaximal mechanical insults create cumulative stress greater than bone capacity, eventually leading to fracture. Johnson9 conducted a biopsy study and postulated that an accelerated remodeling phase was responsible, whereas Friedenberg10 argued that stress injuries are a form of reduced healing, not an attempt to increase healing, caused by the absence of callous formation in the disease process.
Various other nonmodifiable and modifiable risk factors predispose military service members to stress injury. Nonmodifiable risk factors include sex, bone geometry, limb alignment, race, age, and anatomy. Lower extremity movement biomechanics resulting from dynamic limb alignment during activity may be important. Cameron and colleagues11 examined 1843 patients and found that those with knees in >5° of valgus or >5° of external rotation had higher injury rates. Although variables such as sex and limb alignment cannot be changed, proper identification of modifiable risk factors can assist with injury prevention, and nonmodifiable risk factors can help clinicians and researchers target injury prevention interventions to patients at highest risk.
Metabolic, hormonal, and nutritional status is crucial to overall bone health. Multiple studies have found that low body mass index (BMI) is a significant risk factor for stress fracture.7,12,13 Although low BMI is a concern, patients with abnormally high BMI may also be at increased risk for bone stress injury. In a recently released consensus statement on relative energy deficiency in sport (RED-S), the International Olympic Committee addressed the complex interplay of impairments in physiologic function—including metabolic rate, menstrual function, bone health, immunity, protein synthesis, and cardiovascular health—caused by relative energy deficiency.14 The committee stated that the cause of this syndrome is energy deficiency relative to the balance between dietary energy intake and energy expenditure required for health and activities of daily living, growth, and sporting activities. This finding reveals that conditions such as stress injury often may represent a much broader systemic deficit that may be influenced by a patient’s overall physiologic imbalance.
Diagnosis
History and Physical Examination
The onset of stress reaction typically is insidious, with the classic presentation being a new military recruit who is experiencing a sudden increase in pain during physical activity.15 Pain typically is initially present only during activity, and is relieved with rest, but with disease progression this evolves to pain at rest. It is crucial that the physician elicit the patient’s history of training and physical activity. Hsu and colleagues7 reported increased prevalence of overweight civilian recruits, indicating an increase in the number of new recruits having limited experience with the repetitive physical activity encountered in basic training. Stress injury should be suspected in the setting of worsening, indolent lower extremity pain that has been present for several days, especially in the higher-risk patient populations mentioned. Diet should be assessed, with specific attention given to the intake of fruits, vegetables, and foods high in vitamin D and calcium and, most important, the energy balance between intake and output.16 Special attention should also be given to female patients, who may experience the female athlete triad, a spectrum of low energy availability, menstrual dysfunction, and impaired bone turnover (high amount of resorption relative to formation). A key part of the RED-S consensus statement14 alerted healthcare providers that metabolic derangements do not solely affect female patients. These types of patients sustain a major insult to the homeostatic balance of the hormones that sustain adequate bone health. Beck and colleagues17 found that women with disrupted menstrual cycles are 2 to 4 times more likely to sustain a stress fracture than women without disrupted menstrual cycles, making this abnormality an important part of the history.
Examination should begin with careful evaluation of limb alignment and specific attention given to varus or valgus alignment of the knees.11 The feet should also be inspected, as pes planus or cavus foot may increase the risk of stress fracture.18 Identification of the area of maximal tenderness is important. The area in question may also be erythematous or warm secondary to the inflammatory response associated with attempted fracture healing. In chronic fractures in superficial areas such as the metatarsals, callus may be palpable. Although there are few specific tests for stress injury, pain may be reproducible with deep palpation and WB. 
Laboratory Testing
When a pathology is thought to have a nutritional or metabolic cause, particularly in a low-weight or underweight patient, a laboratory workup should be obtained. Specific laboratory tests that all patients should undergo are 25-hydroxyvitamin D3, complete blood cell count, and basic chemistry panel, including calcium and thyroid-stimulating hormone levels. Although not necessary for diagnosis, phosphate, parathyroid hormone, albumin, and prealbumin should also be considered. Females should undergo testing of follicle stimulating hormone, luteinizing hormone, estradiol, and testosterone and have a urine pregnancy test. In patients with signs of excessive cortisone, a dexamethasone suppression test can be administered.21 In males, low testosterone is a documented risk factor for stress injury.22
Imaging
Given their low cost and availability, plain radiographs typically are used for initial examination of a suspected stress injury. However, they often lack sensitivity, particularly in the early stages of stress fracture development (Figure 2). 
Management
Management of bone stress injury depends on many factors, including symptom duration, fracture location and severity, and risk of progression or nonunion (Table).13
Pelvis
Pelvic stress fractures are rare and represent only 1.6% to 7.1% of all stress fractures.13,27,28 Given the low frequency, physicians must have a high index of suspicion to make the correct diagnosis. These fractures typically occur in marathon runners and other patients who present with persistent pain and a history of high levels of activity. As pelvic stress fractures typically involve the superior or inferior pubic rami, or sacrum, and are at low risk for nonunion,13 most are managed with nonoperative treatment and activity modification for 8 to 12 weeks.27
Femur
Femoral stress fractures are also relatively uncommon, accounting for about 10% of all stress fractures. Depending on their location, these fractures can be at high risk for progression, nonunion, and significant morbidity.29 Especially concerning are femoral neck stress fractures, which can involve either the tension side (lateral cortex) or the compression side (medial cortex) of the bone. Suspicion of a femoral neck stress fracture should prompt immediate NWB.5 Early recognition of these injuries is crucial because once displacement occurs, their complication and morbidity rates become high.13 Patients with compression-side fractures should undergo NWB treatment for 4 to 6 weeks and then slow progression to WB activity. Most return to light-impact activity by 3 to 4 months. By contrast, tension-side fractures are less likely to heal without operative intervention.11 All tension-side fractures (and any compression-side fractures >50% of the width of the femoral neck) should be treated with percutaneous placement of cannulated screws (Figure 3). 
Stress fractures of the femoral shaft are less common than those of the femoral neck and represent as little as 3% of all stress fractures.32 However, femoral shaft stress fractures are more common in military populations. In French military recruits, Niva and colleagues33 found an 18% incidence. Similar to femoral neck fractures, femoral shaft fractures typically are diagnosed with advanced imaging, though the fulcrum test and pain on WB can aid in the diagnosis.19 These injuries are often managed nonoperatively with NWB for a period. Weishaar and colleagues34 described US military cadets treated with progressive rehabilitation who returned to full activity within 12 weeks. Displaced femoral shaft fractures associated with bone stress injury are even less common, and should be managed operatively. Salminen and colleagues35 found an incidence of 1.5 fractures per 100,000 years of military service. Over a 20-year period, they surgically treated 10 of these fractures. Average time from intramedullary nailing to union was 3.5 months.
Tibia
The tibia is one of the more common locations for stress injury and fracture. In a prospective study with members of the military, Giladi and colleagues36 found that 71% of stress fractures were tibia fractures. In addition, a large study of 320 athletes with stress fractures found 49.1% in the tibia.37 Fractures typically are diaphyseal and transverse, usually occurring along the posteromedial cortex, where the bone experiences maximal compressive forces (Figure 4).5,13
Compression-side fractures often heal with nonoperative management, though healing may take several months. Swenson and colleagues40 studied the effects of pneumatic bracing on conservative management and return to play in athletes with tibial stress fractures. Patients with bracing returned to light activity within 7 days and full activity within 21 days, whereas those without bracing returned to light activity within 21 days and full activity within 77 days. Pulsed electromagnetic therapy is of controversial benefit in the management of these injuries. Rettig
Metatarsals
Stress fractures were first discovered by Briethaupt1 in the painful swollen feet of Prussian army members in 1855 and were initially named march fractures. Waterman and colleagues6 reported that metatarsal stress fractures accounted for 16% of all stress fractures in the US military between 2009 and 2012. The second metatarsal neck is the most common location for stress fractures, followed by the third and fourth metatarsals, with the fifth metatarsal being the least common.5 The second metatarsal is thought to sustain these injuries more often than the other metatarsals because of its relative lack of immobility. Donahue and Sharkey43 found that the dorsal aspect of the second metatarsal experiences twice the amount of strain experienced by the fifth metatarsal during gait, and that peak strain in the second metatarsal was further increased by simulated muscle fatigue. The risk of stress fracture can be additionally increased with use of minimalist footwear, as shown by Giuliani and colleagues,44 particularly in the absence of a progressive transition in gait and training volume with a change toward minimalist footwear. In patients with a suspected or confirmed fracture of the second, third, or fourth metatarsal, treatment typically is NWB and immobilization for at least 4 weeks.5 Fifth metatarsal stress injuries (Figure 2) typically are treated differently because of their higher risk of nonunion. Patients with a fifth metatarsal stress fracture complain of lateral midfoot pain with running and jumping. For those who present with this fracture early, acceptable treatment consists of 6 weeks of casting and NWB.5 In cases of failed nonoperative therapy, or presentation with radiographic evidence of nonunion, treatment should be intramedullary screw fixation, with bone graft supplementation based on surgeon preference. DeLee and colleagues45 reported on the results of 10 athletes with fifth metatarsal stress fractures treated with intramedullary screw fixation without bone grafting. All 10 experienced fracture union, at a mean of 7.5 weeks, and returned to sport within 8.5 weeks. One complication with this procedure is pain at the screw insertion site, but this can be successfully managed with footwear modification.45
Prevention
Proper identification of patients at high risk for stress injuries has the potential of reducing the incidence of these injuries. Lappe and colleagues46 prospectively examined female army recruits before and after 8 weeks of basic training and found that those who developed a stress fracture were more likely to have a smoking history, to drink more than 10 alcoholic beverages a week, to have a history of corticosteroid or depot medroxyprogesterone use, and to have lower body weight. In addition, the authors found that a history of prolonged exercise before enrollment was protective against fracture. This finding identifies the importance of having new recruits undergo risk factor screening, which could result in adjusting training regimens to try to reduce injury. The RED-S consensus statement14 offers a comprehensive description of the physiologic factors that can contribute to such injury. Similar to proper risk factor identification, implementation of proper exercise progression programs is a simple, modifiable method of limiting stress injuries. For new recruits or athletes who are resuming activity, injury can be effectively prevented by adjusting the frequency, duration, and intensity of training and the training loads used.47
Vitamin D and calcium supplementation is a simple intervention that can be helpful in injury prevention, and its use has very little downside. A double-blind study found a 20% lower incidence of stress fracture in female navy recruits who took 2000 mg of calcium and 800 IU of vitamin D as daily supplemention.48 Of importance, a meta-analysis of more than 65,000 patients found vitamin D supplementation was effective in reducing fracture risk only when combined with calcium, irrespective of age, sex, or prior fracture.49 In female patients with the female athlete triad, psychological counseling and nutritional consultation are essential in bone health maintenance and long-term prevention.50 Other therapies have been evaluated as well. Use of bisphosphonates is controversial for both treatment and prevention of stress fractures. In a randomized, double-blind study of the potential prophylactic effects of risedronate in 324 new infantry recruits, Milgrom and colleagues51 found no statistically significant differences in tibial, femoral, metatarsal, or total stress fracture incidence between the treatment and placebo groups. Therefore, bisphosphonates are seldom recommended as prevention or in primary management of stress fracture.
In addition to nutritional and pharmacologic therapy, activity modification may have a role in injury prevention. Gait retraining has been identified as a potential intervention for reducing stress fractures in patients with poor biomechanics.47 Crowell and Davis52 investigated the effect of gait retraining on the forces operating in the tibia in runners. After 1 month of gait retraining, tibial acceleration while running decreased by 50%, vertical force loading rate by 30%, and peak vertical force impact by 20%. Such studies indicate the importance of proper mechanics during repetitive activity, especially in patients not as accustomed to the rigorous training methods used with new military recruits. However, whether these reduced loads translate into reduced risk of stress fracture remains unclear. In addition, biomechanical shoe orthoses may lower the stress fracture risk in military recruits by reducing peak tibial strain.53 Warden and colleagues54 found a mechanical loading program was effective in enchaining the structural properties of bone in rats, leading the authors to hypothesize that a similar program aimed at modifying bone structure in humans could help prevent stress fracture. Although there have been no studies of such a strategy in humans, pretraining may be an area for future research, especially for military recruits.
Conclusion
Compared with the general population, members of the military (new recruits in particular) are at increased risk for bone stress injuries. Most of these injuries occur during basic training, when recruits significantly increase their repetitive physical activity. Although the exact pathophysiology of stress injury is debated, nutritional and metabolic abnormalities are contributors. The indolent nature of these injuries, and their high rate of false-negative plain radiographs, may result in a significant delay in diagnosis in the absence of advanced imaging studies. Although a majority of injuries heal with nonoperative management and NWB, several patterns, especially those on the tension side of the bone, are at high risk for progression to fracture and nonunion. These include lateral femoral cortex stress injuries and anterior tibial cortex fractures. There should be a low threshold for operative management in the setting of delayed union or failed nonoperative therapy. Of equal importance to orthopedic management of these injuries is the management of underlying systemic deficits, which may have subjected the patient to injury in the first place. Supplementation with vitamin D and calcium can be an important prophylaxis against stress injury. In addition, military recruits and athletes with underlying metabolic or hormonal deficiencies should receive proper attention with a focus on balancing energy intake and energy expenditure. Stress injury leading to fracture—increasingly common in military populations—often requires a multimodal approach for treatment and subsequent prevention.
Am J Orthop. 2017;46(4):176-183. Copyright Frontline Medical Communications Inc. 2017. All rights reserved.
1. Briethaupt MD. Zur Pathologie des menschlichen Fusses [To the pathology of the human foot]. Med Zeitung. 1855;24:169-177.
2. Berger FH, de Jonge MC, Maas M. Stress fractures in the lower extremity. Eur J Radiol. 2007;62(1):16-26.
3. Almeida SA, Williams KM, Shaffer RA, Brodine SK. Epidemiological patterns of musculoskeletal injuries and physical training. Med Sci Sports Exerc. 1999;31(8):1176-1182.
4. Jones BH, Thacker SB, Gilchrist J, Kimsey CD, Sosin DM. Prevention of lower extremity stress fractures in athletes and soldiers: a systematic review. Epidemiol Rev. 2002;24(2):228-247.
5. Jacobs JM, Cameron KL, Bojescul JA. Lower extremity stress fractures in the military. Clin Sports Med. 2014;33(4):591-613.
6. Waterman BR, Gun B, Bader JO, Orr JD, Belmont PJ. Epidemiology of lower extremity stress fractures in the United States military. Mil Med. 2016;181(10):1308-1313.
7. Hsu LL, Nevin RL, Tobler SK, Rubertone MV. Trends in overweight and obesity among 18-year-old applicants to the United States military, 1993–2006. J Adolesc Health. 2007;41(6):610-612.
8. Stanitski CL, McMaster JH, Scranton PE. On the nature of stress fractures. Am J Sports Med. 1978;6(6):391-396.
9. Johnson LC. Histogenesis of stress fractures [annual lecture]. Washington, DC: Armed Forces Institute of Pathology; 1963.
10. Friedenberg ZB. Fatigue fractures of the tibia. Clin Orthop Relat Res. 1971;(76):111-115.
11. Cameron KL, Peck KY, Owens BD, et al. Biomechanical risk factors for lower extremity stress fracture. Orthop J Sports Med. 2013;1(4 suppl).
12. Knapik J, Montain S, McGraw S, Grier T, Ely M, Jones B. Stress fracture risk factors in basic combat training. Int J Sports Med. 2012;33(11):940-946.
13. Behrens SB, Deren ME, Matson A, Fadale PD, Monchik KO. Stress fractures of the pelvis and legs in athletes. Sports Health. 2013;5(2):165-174.
14. Mountjoy M, Sundgot-Borgen J, Burke L, et al. The IOC consensus statement: beyond the female athlete triad—relative energy deficiency in sport (RED-S). Br J Sports Med. 2014;48(7):491-497.
15. Maitra RS, Johnson DL. Stress fractures. Clinical history and physical examination. Clin Sports Med. 1997;16(2):259-274.
16. Nieves JW, Melsop K, Curtis M, et al. Nutritional factors that influence change in bone density and stress fracture risk among young female cross-country runners. PM R. 2010;2(8):740-750.
17. Beck BR, Matheson GO, Bergman G, et al. Do capacitively coupled electric fields accelerate tibial stress fracture healing? Am J Sports Med. 2008;36(3):545-553.
18. Simkin A, Leichter I, Giladi M, Stein M, Milgrom C. Combined effect of foot arch structure and an orthotic device on stress fractures. Foot Ankle. 1989;10(1):25-29.
19. 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(2):248-256.
20. Clement D, Ammann W, Taunton J, et al. Exercise-induced stress injuries to the femur. Int J Sports Med. 1993;14(6):347-352.
21. Wood PJ, Barth JH, Freedman DB, Perry L, Sheridan B. Evidence for the low dose dexamethasone suppression test to screen for Cushing’s syndrome—recommendations for a protocol for biochemistry laboratories. Ann Clin Biochem. 1997;34(pt 3):222-229.
22. Bennell K, Matheson G, Meeuwisse W, Brukner P. Risk factors for stress fractures. Sports Med. 1999;28(2):91-122.
23. Prather JL, Nusynowitz ML, Snowdy HA, Hughes AD, McCartney WH, Bagg RJ. Scintigraphic findings in stress fractures. J Bone Joint Surg Am. 1977;59(7):869-874.
24. 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(2):291-306.
25. Boden BP, Osbahr DC. High-risk stress fractures: evaluation and treatment. J Am Acad Orthop Surg. 2000;8(6):344-353.
26. Gaeta M, Minutoli F, Scribano E, et al. CT and MR imaging findings in athletes with early tibial stress injuries: comparison with bone scintigraphy findings and emphasis on cortical abnormalities. Radiology. 2005;235(2):553-561.
27. Matheson GO, Clement DB, Mckenzie DC, Taunton JE, Lloyd-Smith DR, Macintyre JG. Stress fractures in athletes. Am J Sports Med. 1987;15(1):46-58.
28. Iwamoto J, Takeda T. Stress fractures in athletes: review of 196 cases. J Orthop Sci. 2003;8(3):273-278.
29. Noakes TD, Smith JA, Lindenberg G, Wills CE. Pelvic stress fractures in long distance runners. Am J Sports Med. 1985;13(2):120-123.
30. Neubauer T, Brand J, Lidder S, Krawany M. Stress fractures of the femoral neck in runners: a review. Res Sports Med. 2016;24(3):283-297.
31. Evans JT, Guyver PM, Kassam AM, Hubble MJW. Displaced femoral neck stress fractures in Royal Marine recruits—management and results of operative treatment. J R Nav Med Serv. 2012;98(2):3-5.
32. Orava S. Stress fractures. Br J Sports Med. 1980;14(1):40-44.
33. Niva MH, Kiuru MJ, Haataja R, Pihlajamäki HK. Fatigue injuries of the femur. J Bone Joint Surg Br. 2005;87(10):1385-1390.
34. Weishaar MD, McMillian DJ, Moore JH. Identification and management of 2 femoral shaft stress injuries. J Orthop Sports Phys Ther. 2005;35(10):665-673.
35. Salminen ST, Pihlajamäki HK, Visuri TI, Böstman OM. Displaced fatigue fractures of the femoral shaft. Clin Orthop Relat Res. 2003;(409):250-259.
36. Giladi M, Ahronson Z, Stein M, Danon YL, Milgrom C. Unusual distribution and onset of stress fractures in soldiers. Clin Orthop Relat Res. 1985;(192):142-146.
37. Matheson GO, Clement DB, Mckenzie DC, Taunton JE, Lloyd-Smith DR, Macintyre JG. Stress fractures in athletes. Am J Sports Med. 1987;15(1):46-58.
38. Green NE, Rogers RA, Lipscomb AB. Nonunions of stress fractures of the tibia. Am J Sports Med. 1985;13(3):171-176.
39. Orava S, Hulkko A. Stress fracture of the mid-tibial shaft. Acta Orthop Scand. 1984;55(1):35-37.
40. Swenson EJ Jr, DeHaven KE, Sebastianelli WJ, Hanks G, Kalenak A, Lynch JM. The effect of a pneumatic leg brace on return to play in athletes with tibial stress fractures. Am J Sports Med. 1997;25(3):322-328.
41. Rettig AC, Shelbourne KD, McCarroll JR, Bisesi M, Watts J. The natural history and treatment of delayed union stress fractures of the anterior cortex of the tibia. Am J Sports Med. 1988;16(3):250-255.
42. Varner KE, Younas SA, Lintner DM, Marymont JV. Chronic anterior midtibial stress fractures in athletes treated with reamed intramedullary nailing. Am J Sports Med. 2005;33(7):1071-1076.
43. Donahue SW, Sharkey NA. Strains in the metatarsals during the stance phase of gait: implications for stress fractures. J Bone Joint Surg Am. 1999;81(9):1236-1244.
44. Giuliani J, Masini B, Alitz C, Owens BD. Barefoot-simulating footwear associated with metatarsal stress injury in 2 runners. Orthopedics. 2011;34(7):e320-e323.
45. DeLee JC, Evans JP, Julian J. Stress fracture of the fifth metatarsal. Am J Sports Med. 1983;11(5):349-353.
46. 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.
47. Friedl KE, Evans RK, Moran DS. Stress fracture and military medical readiness: bridging basic and applied research. Med Sci Sports Exerc. 2008;40(11 suppl):S609-S622.
48. Lappe J, Cullen D, Haynatzki G, Recker R, Ahlf R, Thompson K. Calcium and vitamin D supplementation decreases incidence of stress fractures in female navy recruits. J Bone Miner Res. 2008;23(5):741-749.
49. DIPART (Vitamin D Individual Patient Analysis of Randomized Trials) Group. Patient level pooled analysis of 68 500 patients from seven major vitamin D fracture trials in US and Europe. BMJ. 2010;340:b5463.
50. Duckham RL, Peirce N, Meyer C, Summers GD, Cameron N, Brooke-Wavell K. Risk factors for stress fracture in female endurance athletes: a cross-sectional study. BMJ Open. 2012;2(6).
51. 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):418-424.
52. Crowell HP, Davis IS. Gait retraining to reduce lower extremity loading in runners. Clin Biomech. 2011;26(1):78-83.
53. 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):866-870.
54. Warden SJ, Hurst JA, Sanders MS, Turner CH, Burr DB, Li J. Bone adaptation to a mechanical loading program significantly increases skeletal fatigue resistance. J Bone Miner Res. 2005;20(5):809-816.
Take-Home Points
- Stress injuries, specifically of the lower extremity, are very common in new military trainees.
- Stress injury can range from benign periosteal reaction to displaced fracture.
- Stress injury should be treated on a case-by-case basis, depending on the severity of injury, the location of the injury, and the likelihood of healing with nonoperative management.
- Modifiable risk factors such as nutritional status, training regiment, and even footwear should be investigated to determine potential causes of injury.
- Prevention is a crucial part of the treatment of these injuries, and early intervention such as careful pre-enrollment physicals and vitamin supplementation can be essential in lowering injury rates.
Bone stress injuries, which are common in military recruits, present in weight-bearing (WB) areas as indolent pain caused by repetitive stress and microtrauma. They were first reported in the metatarsals of Prussian soldiers in 1855.1 Today, stress injuries are increasingly common. One study estimated they account for 10% of patients seen by sports medicine practitioners.2 This injury most commonly affects military members, endurance athletes, and dancers.3-5 Specifically, the incidence of stress fractures in military members has been reported to range from 0.8% to 6.9% for men and from 3.4% to 21.0% for women.4 Because of repetitive vigorous lower extremity loading, stress fractures typically occur in the pelvis, femoral neck, tibial shaft, and metatarsals. Delayed diagnosis and the subsequent duration of treatment required for adequate healing can result in significant morbidity. In a 2009 to 2012 study of US military members, Waterman and colleagues6 found an incidence rate of 5.69 stress fractures per 1000 person-years. Fractures most frequently involved the tibia/fibula (2.26/1000), followed by the metatarsals (0.92/1000) and the femoral neck (0.49/1000).6 In addition, these injuries were most commonly encountered in new recruits, who were less accustomed to the high-volume, high-intensity training required during basic training.4,7 Enlisted junior service members have been reported to account for 77.5% of all stress fractures.6 Age under 20 years or over 40 years and white race have also been found to be risk factors for stress injury.6
The pathogenesis of stress injury is controversial. Stanitski and colleagues8 theorized that multiple submaximal mechanical insults create cumulative stress greater than bone capacity, eventually leading to fracture. Johnson9 conducted a biopsy study and postulated that an accelerated remodeling phase was responsible, whereas Friedenberg10 argued that stress injuries are a form of reduced healing, not an attempt to increase healing, caused by the absence of callous formation in the disease process.
Various other nonmodifiable and modifiable risk factors predispose military service members to stress injury. Nonmodifiable risk factors include sex, bone geometry, limb alignment, race, age, and anatomy. Lower extremity movement biomechanics resulting from dynamic limb alignment during activity may be important. Cameron and colleagues11 examined 1843 patients and found that those with knees in >5° of valgus or >5° of external rotation had higher injury rates. Although variables such as sex and limb alignment cannot be changed, proper identification of modifiable risk factors can assist with injury prevention, and nonmodifiable risk factors can help clinicians and researchers target injury prevention interventions to patients at highest risk.
Metabolic, hormonal, and nutritional status is crucial to overall bone health. Multiple studies have found that low body mass index (BMI) is a significant risk factor for stress fracture.7,12,13 Although low BMI is a concern, patients with abnormally high BMI may also be at increased risk for bone stress injury. In a recently released consensus statement on relative energy deficiency in sport (RED-S), the International Olympic Committee addressed the complex interplay of impairments in physiologic function—including metabolic rate, menstrual function, bone health, immunity, protein synthesis, and cardiovascular health—caused by relative energy deficiency.14 The committee stated that the cause of this syndrome is energy deficiency relative to the balance between dietary energy intake and energy expenditure required for health and activities of daily living, growth, and sporting activities. This finding reveals that conditions such as stress injury often may represent a much broader systemic deficit that may be influenced by a patient’s overall physiologic imbalance.
Diagnosis
History and Physical Examination
The onset of stress reaction typically is insidious, with the classic presentation being a new military recruit who is experiencing a sudden increase in pain during physical activity.15 Pain typically is initially present only during activity, and is relieved with rest, but with disease progression this evolves to pain at rest. It is crucial that the physician elicit the patient’s history of training and physical activity. Hsu and colleagues7 reported increased prevalence of overweight civilian recruits, indicating an increase in the number of new recruits having limited experience with the repetitive physical activity encountered in basic training. Stress injury should be suspected in the setting of worsening, indolent lower extremity pain that has been present for several days, especially in the higher-risk patient populations mentioned. Diet should be assessed, with specific attention given to the intake of fruits, vegetables, and foods high in vitamin D and calcium and, most important, the energy balance between intake and output.16 Special attention should also be given to female patients, who may experience the female athlete triad, a spectrum of low energy availability, menstrual dysfunction, and impaired bone turnover (high amount of resorption relative to formation). A key part of the RED-S consensus statement14 alerted healthcare providers that metabolic derangements do not solely affect female patients. These types of patients sustain a major insult to the homeostatic balance of the hormones that sustain adequate bone health. Beck and colleagues17 found that women with disrupted menstrual cycles are 2 to 4 times more likely to sustain a stress fracture than women without disrupted menstrual cycles, making this abnormality an important part of the history.
Examination should begin with careful evaluation of limb alignment and specific attention given to varus or valgus alignment of the knees.11 The feet should also be inspected, as pes planus or cavus foot may increase the risk of stress fracture.18 Identification of the area of maximal tenderness is important. The area in question may also be erythematous or warm secondary to the inflammatory response associated with attempted fracture healing. In chronic fractures in superficial areas such as the metatarsals, callus may be palpable. Although there are few specific tests for stress injury, pain may be reproducible with deep palpation and WB.
Laboratory Testing
When a pathology is thought to have a nutritional or metabolic cause, particularly in a low-weight or underweight patient, a laboratory workup should be obtained. Specific laboratory tests that all patients should undergo are 25-hydroxyvitamin D3, complete blood cell count, and basic chemistry panel, including calcium and thyroid-stimulating hormone levels. Although not necessary for diagnosis, phosphate, parathyroid hormone, albumin, and prealbumin should also be considered. Females should undergo testing of follicle stimulating hormone, luteinizing hormone, estradiol, and testosterone and have a urine pregnancy test. In patients with signs of excessive cortisone, a dexamethasone suppression test can be administered.21 In males, low testosterone is a documented risk factor for stress injury.22
Imaging
Given their low cost and availability, plain radiographs typically are used for initial examination of a suspected stress injury. However, they often lack sensitivity, particularly in the early stages of stress fracture development (Figure 2).
Management
Management of bone stress injury depends on many factors, including symptom duration, fracture location and severity, and risk of progression or nonunion (Table).13
Pelvis
Pelvic stress fractures are rare and represent only 1.6% to 7.1% of all stress fractures.13,27,28 Given the low frequency, physicians must have a high index of suspicion to make the correct diagnosis. These fractures typically occur in marathon runners and other patients who present with persistent pain and a history of high levels of activity. As pelvic stress fractures typically involve the superior or inferior pubic rami, or sacrum, and are at low risk for nonunion,13 most are managed with nonoperative treatment and activity modification for 8 to 12 weeks.27
Femur
Femoral stress fractures are also relatively uncommon, accounting for about 10% of all stress fractures. Depending on their location, these fractures can be at high risk for progression, nonunion, and significant morbidity.29 Especially concerning are femoral neck stress fractures, which can involve either the tension side (lateral cortex) or the compression side (medial cortex) of the bone. Suspicion of a femoral neck stress fracture should prompt immediate NWB.5 Early recognition of these injuries is crucial because once displacement occurs, their complication and morbidity rates become high.13 Patients with compression-side fractures should undergo NWB treatment for 4 to 6 weeks and then slow progression to WB activity. Most return to light-impact activity by 3 to 4 months. By contrast, tension-side fractures are less likely to heal without operative intervention.11 All tension-side fractures (and any compression-side fractures >50% of the width of the femoral neck) should be treated with percutaneous placement of cannulated screws (Figure 3).
Stress fractures of the femoral shaft are less common than those of the femoral neck and represent as little as 3% of all stress fractures.32 However, femoral shaft stress fractures are more common in military populations. In French military recruits, Niva and colleagues33 found an 18% incidence. Similar to femoral neck fractures, femoral shaft fractures typically are diagnosed with advanced imaging, though the fulcrum test and pain on WB can aid in the diagnosis.19 These injuries are often managed nonoperatively with NWB for a period. Weishaar and colleagues34 described US military cadets treated with progressive rehabilitation who returned to full activity within 12 weeks. Displaced femoral shaft fractures associated with bone stress injury are even less common, and should be managed operatively. Salminen and colleagues35 found an incidence of 1.5 fractures per 100,000 years of military service. Over a 20-year period, they surgically treated 10 of these fractures. Average time from intramedullary nailing to union was 3.5 months.
Tibia
The tibia is one of the more common locations for stress injury and fracture. In a prospective study with members of the military, Giladi and colleagues36 found that 71% of stress fractures were tibia fractures. In addition, a large study of 320 athletes with stress fractures found 49.1% in the tibia.37 Fractures typically are diaphyseal and transverse, usually occurring along the posteromedial cortex, where the bone experiences maximal compressive forces (Figure 4).5,13
Compression-side fractures often heal with nonoperative management, though healing may take several months. Swenson and colleagues40 studied the effects of pneumatic bracing on conservative management and return to play in athletes with tibial stress fractures. Patients with bracing returned to light activity within 7 days and full activity within 21 days, whereas those without bracing returned to light activity within 21 days and full activity within 77 days. Pulsed electromagnetic therapy is of controversial benefit in the management of these injuries. Rettig
Metatarsals
Stress fractures were first discovered by Briethaupt1 in the painful swollen feet of Prussian army members in 1855 and were initially named march fractures. Waterman and colleagues6 reported that metatarsal stress fractures accounted for 16% of all stress fractures in the US military between 2009 and 2012. The second metatarsal neck is the most common location for stress fractures, followed by the third and fourth metatarsals, with the fifth metatarsal being the least common.5 The second metatarsal is thought to sustain these injuries more often than the other metatarsals because of its relative lack of immobility. Donahue and Sharkey43 found that the dorsal aspect of the second metatarsal experiences twice the amount of strain experienced by the fifth metatarsal during gait, and that peak strain in the second metatarsal was further increased by simulated muscle fatigue. The risk of stress fracture can be additionally increased with use of minimalist footwear, as shown by Giuliani and colleagues,44 particularly in the absence of a progressive transition in gait and training volume with a change toward minimalist footwear. In patients with a suspected or confirmed fracture of the second, third, or fourth metatarsal, treatment typically is NWB and immobilization for at least 4 weeks.5 Fifth metatarsal stress injuries (Figure 2) typically are treated differently because of their higher risk of nonunion. Patients with a fifth metatarsal stress fracture complain of lateral midfoot pain with running and jumping. For those who present with this fracture early, acceptable treatment consists of 6 weeks of casting and NWB.5 In cases of failed nonoperative therapy, or presentation with radiographic evidence of nonunion, treatment should be intramedullary screw fixation, with bone graft supplementation based on surgeon preference. DeLee and colleagues45 reported on the results of 10 athletes with fifth metatarsal stress fractures treated with intramedullary screw fixation without bone grafting. All 10 experienced fracture union, at a mean of 7.5 weeks, and returned to sport within 8.5 weeks. One complication with this procedure is pain at the screw insertion site, but this can be successfully managed with footwear modification.45
Prevention
Proper identification of patients at high risk for stress injuries has the potential of reducing the incidence of these injuries. Lappe and colleagues46 prospectively examined female army recruits before and after 8 weeks of basic training and found that those who developed a stress fracture were more likely to have a smoking history, to drink more than 10 alcoholic beverages a week, to have a history of corticosteroid or depot medroxyprogesterone use, and to have lower body weight. In addition, the authors found that a history of prolonged exercise before enrollment was protective against fracture. This finding identifies the importance of having new recruits undergo risk factor screening, which could result in adjusting training regimens to try to reduce injury. The RED-S consensus statement14 offers a comprehensive description of the physiologic factors that can contribute to such injury. Similar to proper risk factor identification, implementation of proper exercise progression programs is a simple, modifiable method of limiting stress injuries. For new recruits or athletes who are resuming activity, injury can be effectively prevented by adjusting the frequency, duration, and intensity of training and the training loads used.47
Vitamin D and calcium supplementation is a simple intervention that can be helpful in injury prevention, and its use has very little downside. A double-blind study found a 20% lower incidence of stress fracture in female navy recruits who took 2000 mg of calcium and 800 IU of vitamin D as daily supplemention.48 Of importance, a meta-analysis of more than 65,000 patients found vitamin D supplementation was effective in reducing fracture risk only when combined with calcium, irrespective of age, sex, or prior fracture.49 In female patients with the female athlete triad, psychological counseling and nutritional consultation are essential in bone health maintenance and long-term prevention.50 Other therapies have been evaluated as well. Use of bisphosphonates is controversial for both treatment and prevention of stress fractures. In a randomized, double-blind study of the potential prophylactic effects of risedronate in 324 new infantry recruits, Milgrom and colleagues51 found no statistically significant differences in tibial, femoral, metatarsal, or total stress fracture incidence between the treatment and placebo groups. Therefore, bisphosphonates are seldom recommended as prevention or in primary management of stress fracture.
In addition to nutritional and pharmacologic therapy, activity modification may have a role in injury prevention. Gait retraining has been identified as a potential intervention for reducing stress fractures in patients with poor biomechanics.47 Crowell and Davis52 investigated the effect of gait retraining on the forces operating in the tibia in runners. After 1 month of gait retraining, tibial acceleration while running decreased by 50%, vertical force loading rate by 30%, and peak vertical force impact by 20%. Such studies indicate the importance of proper mechanics during repetitive activity, especially in patients not as accustomed to the rigorous training methods used with new military recruits. However, whether these reduced loads translate into reduced risk of stress fracture remains unclear. In addition, biomechanical shoe orthoses may lower the stress fracture risk in military recruits by reducing peak tibial strain.53 Warden and colleagues54 found a mechanical loading program was effective in enchaining the structural properties of bone in rats, leading the authors to hypothesize that a similar program aimed at modifying bone structure in humans could help prevent stress fracture. Although there have been no studies of such a strategy in humans, pretraining may be an area for future research, especially for military recruits.
Conclusion
Compared with the general population, members of the military (new recruits in particular) are at increased risk for bone stress injuries. Most of these injuries occur during basic training, when recruits significantly increase their repetitive physical activity. Although the exact pathophysiology of stress injury is debated, nutritional and metabolic abnormalities are contributors. The indolent nature of these injuries, and their high rate of false-negative plain radiographs, may result in a significant delay in diagnosis in the absence of advanced imaging studies. Although a majority of injuries heal with nonoperative management and NWB, several patterns, especially those on the tension side of the bone, are at high risk for progression to fracture and nonunion. These include lateral femoral cortex stress injuries and anterior tibial cortex fractures. There should be a low threshold for operative management in the setting of delayed union or failed nonoperative therapy. Of equal importance to orthopedic management of these injuries is the management of underlying systemic deficits, which may have subjected the patient to injury in the first place. Supplementation with vitamin D and calcium can be an important prophylaxis against stress injury. In addition, military recruits and athletes with underlying metabolic or hormonal deficiencies should receive proper attention with a focus on balancing energy intake and energy expenditure. Stress injury leading to fracture—increasingly common in military populations—often requires a multimodal approach for treatment and subsequent prevention.
Am J Orthop. 2017;46(4):176-183. Copyright Frontline Medical Communications Inc. 2017. All rights reserved.
Take-Home Points
- Stress injuries, specifically of the lower extremity, are very common in new military trainees.
- Stress injury can range from benign periosteal reaction to displaced fracture.
- Stress injury should be treated on a case-by-case basis, depending on the severity of injury, the location of the injury, and the likelihood of healing with nonoperative management.
- Modifiable risk factors such as nutritional status, training regiment, and even footwear should be investigated to determine potential causes of injury.
- Prevention is a crucial part of the treatment of these injuries, and early intervention such as careful pre-enrollment physicals and vitamin supplementation can be essential in lowering injury rates.
Bone stress injuries, which are common in military recruits, present in weight-bearing (WB) areas as indolent pain caused by repetitive stress and microtrauma. They were first reported in the metatarsals of Prussian soldiers in 1855.1 Today, stress injuries are increasingly common. One study estimated they account for 10% of patients seen by sports medicine practitioners.2 This injury most commonly affects military members, endurance athletes, and dancers.3-5 Specifically, the incidence of stress fractures in military members has been reported to range from 0.8% to 6.9% for men and from 3.4% to 21.0% for women.4 Because of repetitive vigorous lower extremity loading, stress fractures typically occur in the pelvis, femoral neck, tibial shaft, and metatarsals. Delayed diagnosis and the subsequent duration of treatment required for adequate healing can result in significant morbidity. In a 2009 to 2012 study of US military members, Waterman and colleagues6 found an incidence rate of 5.69 stress fractures per 1000 person-years. Fractures most frequently involved the tibia/fibula (2.26/1000), followed by the metatarsals (0.92/1000) and the femoral neck (0.49/1000).6 In addition, these injuries were most commonly encountered in new recruits, who were less accustomed to the high-volume, high-intensity training required during basic training.4,7 Enlisted junior service members have been reported to account for 77.5% of all stress fractures.6 Age under 20 years or over 40 years and white race have also been found to be risk factors for stress injury.6
The pathogenesis of stress injury is controversial. Stanitski and colleagues8 theorized that multiple submaximal mechanical insults create cumulative stress greater than bone capacity, eventually leading to fracture. Johnson9 conducted a biopsy study and postulated that an accelerated remodeling phase was responsible, whereas Friedenberg10 argued that stress injuries are a form of reduced healing, not an attempt to increase healing, caused by the absence of callous formation in the disease process.
Various other nonmodifiable and modifiable risk factors predispose military service members to stress injury. Nonmodifiable risk factors include sex, bone geometry, limb alignment, race, age, and anatomy. Lower extremity movement biomechanics resulting from dynamic limb alignment during activity may be important. Cameron and colleagues11 examined 1843 patients and found that those with knees in >5° of valgus or >5° of external rotation had higher injury rates. Although variables such as sex and limb alignment cannot be changed, proper identification of modifiable risk factors can assist with injury prevention, and nonmodifiable risk factors can help clinicians and researchers target injury prevention interventions to patients at highest risk.
Metabolic, hormonal, and nutritional status is crucial to overall bone health. Multiple studies have found that low body mass index (BMI) is a significant risk factor for stress fracture.7,12,13 Although low BMI is a concern, patients with abnormally high BMI may also be at increased risk for bone stress injury. In a recently released consensus statement on relative energy deficiency in sport (RED-S), the International Olympic Committee addressed the complex interplay of impairments in physiologic function—including metabolic rate, menstrual function, bone health, immunity, protein synthesis, and cardiovascular health—caused by relative energy deficiency.14 The committee stated that the cause of this syndrome is energy deficiency relative to the balance between dietary energy intake and energy expenditure required for health and activities of daily living, growth, and sporting activities. This finding reveals that conditions such as stress injury often may represent a much broader systemic deficit that may be influenced by a patient’s overall physiologic imbalance.
Diagnosis
History and Physical Examination
The onset of stress reaction typically is insidious, with the classic presentation being a new military recruit who is experiencing a sudden increase in pain during physical activity.15 Pain typically is initially present only during activity, and is relieved with rest, but with disease progression this evolves to pain at rest. It is crucial that the physician elicit the patient’s history of training and physical activity. Hsu and colleagues7 reported increased prevalence of overweight civilian recruits, indicating an increase in the number of new recruits having limited experience with the repetitive physical activity encountered in basic training. Stress injury should be suspected in the setting of worsening, indolent lower extremity pain that has been present for several days, especially in the higher-risk patient populations mentioned. Diet should be assessed, with specific attention given to the intake of fruits, vegetables, and foods high in vitamin D and calcium and, most important, the energy balance between intake and output.16 Special attention should also be given to female patients, who may experience the female athlete triad, a spectrum of low energy availability, menstrual dysfunction, and impaired bone turnover (high amount of resorption relative to formation). A key part of the RED-S consensus statement14 alerted healthcare providers that metabolic derangements do not solely affect female patients. These types of patients sustain a major insult to the homeostatic balance of the hormones that sustain adequate bone health. Beck and colleagues17 found that women with disrupted menstrual cycles are 2 to 4 times more likely to sustain a stress fracture than women without disrupted menstrual cycles, making this abnormality an important part of the history.
Examination should begin with careful evaluation of limb alignment and specific attention given to varus or valgus alignment of the knees.11 The feet should also be inspected, as pes planus or cavus foot may increase the risk of stress fracture.18 Identification of the area of maximal tenderness is important. The area in question may also be erythematous or warm secondary to the inflammatory response associated with attempted fracture healing. In chronic fractures in superficial areas such as the metatarsals, callus may be palpable. Although there are few specific tests for stress injury, pain may be reproducible with deep palpation and WB.
Laboratory Testing
When a pathology is thought to have a nutritional or metabolic cause, particularly in a low-weight or underweight patient, a laboratory workup should be obtained. Specific laboratory tests that all patients should undergo are 25-hydroxyvitamin D3, complete blood cell count, and basic chemistry panel, including calcium and thyroid-stimulating hormone levels. Although not necessary for diagnosis, phosphate, parathyroid hormone, albumin, and prealbumin should also be considered. Females should undergo testing of follicle stimulating hormone, luteinizing hormone, estradiol, and testosterone and have a urine pregnancy test. In patients with signs of excessive cortisone, a dexamethasone suppression test can be administered.21 In males, low testosterone is a documented risk factor for stress injury.22
Imaging
Given their low cost and availability, plain radiographs typically are used for initial examination of a suspected stress injury. However, they often lack sensitivity, particularly in the early stages of stress fracture development (Figure 2).
Management
Management of bone stress injury depends on many factors, including symptom duration, fracture location and severity, and risk of progression or nonunion (Table).13
Pelvis
Pelvic stress fractures are rare and represent only 1.6% to 7.1% of all stress fractures.13,27,28 Given the low frequency, physicians must have a high index of suspicion to make the correct diagnosis. These fractures typically occur in marathon runners and other patients who present with persistent pain and a history of high levels of activity. As pelvic stress fractures typically involve the superior or inferior pubic rami, or sacrum, and are at low risk for nonunion,13 most are managed with nonoperative treatment and activity modification for 8 to 12 weeks.27
Femur
Femoral stress fractures are also relatively uncommon, accounting for about 10% of all stress fractures. Depending on their location, these fractures can be at high risk for progression, nonunion, and significant morbidity.29 Especially concerning are femoral neck stress fractures, which can involve either the tension side (lateral cortex) or the compression side (medial cortex) of the bone. Suspicion of a femoral neck stress fracture should prompt immediate NWB.5 Early recognition of these injuries is crucial because once displacement occurs, their complication and morbidity rates become high.13 Patients with compression-side fractures should undergo NWB treatment for 4 to 6 weeks and then slow progression to WB activity. Most return to light-impact activity by 3 to 4 months. By contrast, tension-side fractures are less likely to heal without operative intervention.11 All tension-side fractures (and any compression-side fractures >50% of the width of the femoral neck) should be treated with percutaneous placement of cannulated screws (Figure 3).
Stress fractures of the femoral shaft are less common than those of the femoral neck and represent as little as 3% of all stress fractures.32 However, femoral shaft stress fractures are more common in military populations. In French military recruits, Niva and colleagues33 found an 18% incidence. Similar to femoral neck fractures, femoral shaft fractures typically are diagnosed with advanced imaging, though the fulcrum test and pain on WB can aid in the diagnosis.19 These injuries are often managed nonoperatively with NWB for a period. Weishaar and colleagues34 described US military cadets treated with progressive rehabilitation who returned to full activity within 12 weeks. Displaced femoral shaft fractures associated with bone stress injury are even less common, and should be managed operatively. Salminen and colleagues35 found an incidence of 1.5 fractures per 100,000 years of military service. Over a 20-year period, they surgically treated 10 of these fractures. Average time from intramedullary nailing to union was 3.5 months.
Tibia
The tibia is one of the more common locations for stress injury and fracture. In a prospective study with members of the military, Giladi and colleagues36 found that 71% of stress fractures were tibia fractures. In addition, a large study of 320 athletes with stress fractures found 49.1% in the tibia.37 Fractures typically are diaphyseal and transverse, usually occurring along the posteromedial cortex, where the bone experiences maximal compressive forces (Figure 4).5,13
Compression-side fractures often heal with nonoperative management, though healing may take several months. Swenson and colleagues40 studied the effects of pneumatic bracing on conservative management and return to play in athletes with tibial stress fractures. Patients with bracing returned to light activity within 7 days and full activity within 21 days, whereas those without bracing returned to light activity within 21 days and full activity within 77 days. Pulsed electromagnetic therapy is of controversial benefit in the management of these injuries. Rettig
Metatarsals
Stress fractures were first discovered by Briethaupt1 in the painful swollen feet of Prussian army members in 1855 and were initially named march fractures. Waterman and colleagues6 reported that metatarsal stress fractures accounted for 16% of all stress fractures in the US military between 2009 and 2012. The second metatarsal neck is the most common location for stress fractures, followed by the third and fourth metatarsals, with the fifth metatarsal being the least common.5 The second metatarsal is thought to sustain these injuries more often than the other metatarsals because of its relative lack of immobility. Donahue and Sharkey43 found that the dorsal aspect of the second metatarsal experiences twice the amount of strain experienced by the fifth metatarsal during gait, and that peak strain in the second metatarsal was further increased by simulated muscle fatigue. The risk of stress fracture can be additionally increased with use of minimalist footwear, as shown by Giuliani and colleagues,44 particularly in the absence of a progressive transition in gait and training volume with a change toward minimalist footwear. In patients with a suspected or confirmed fracture of the second, third, or fourth metatarsal, treatment typically is NWB and immobilization for at least 4 weeks.5 Fifth metatarsal stress injuries (Figure 2) typically are treated differently because of their higher risk of nonunion. Patients with a fifth metatarsal stress fracture complain of lateral midfoot pain with running and jumping. For those who present with this fracture early, acceptable treatment consists of 6 weeks of casting and NWB.5 In cases of failed nonoperative therapy, or presentation with radiographic evidence of nonunion, treatment should be intramedullary screw fixation, with bone graft supplementation based on surgeon preference. DeLee and colleagues45 reported on the results of 10 athletes with fifth metatarsal stress fractures treated with intramedullary screw fixation without bone grafting. All 10 experienced fracture union, at a mean of 7.5 weeks, and returned to sport within 8.5 weeks. One complication with this procedure is pain at the screw insertion site, but this can be successfully managed with footwear modification.45
Prevention
Proper identification of patients at high risk for stress injuries has the potential of reducing the incidence of these injuries. Lappe and colleagues46 prospectively examined female army recruits before and after 8 weeks of basic training and found that those who developed a stress fracture were more likely to have a smoking history, to drink more than 10 alcoholic beverages a week, to have a history of corticosteroid or depot medroxyprogesterone use, and to have lower body weight. In addition, the authors found that a history of prolonged exercise before enrollment was protective against fracture. This finding identifies the importance of having new recruits undergo risk factor screening, which could result in adjusting training regimens to try to reduce injury. The RED-S consensus statement14 offers a comprehensive description of the physiologic factors that can contribute to such injury. Similar to proper risk factor identification, implementation of proper exercise progression programs is a simple, modifiable method of limiting stress injuries. For new recruits or athletes who are resuming activity, injury can be effectively prevented by adjusting the frequency, duration, and intensity of training and the training loads used.47
Vitamin D and calcium supplementation is a simple intervention that can be helpful in injury prevention, and its use has very little downside. A double-blind study found a 20% lower incidence of stress fracture in female navy recruits who took 2000 mg of calcium and 800 IU of vitamin D as daily supplemention.48 Of importance, a meta-analysis of more than 65,000 patients found vitamin D supplementation was effective in reducing fracture risk only when combined with calcium, irrespective of age, sex, or prior fracture.49 In female patients with the female athlete triad, psychological counseling and nutritional consultation are essential in bone health maintenance and long-term prevention.50 Other therapies have been evaluated as well. Use of bisphosphonates is controversial for both treatment and prevention of stress fractures. In a randomized, double-blind study of the potential prophylactic effects of risedronate in 324 new infantry recruits, Milgrom and colleagues51 found no statistically significant differences in tibial, femoral, metatarsal, or total stress fracture incidence between the treatment and placebo groups. Therefore, bisphosphonates are seldom recommended as prevention or in primary management of stress fracture.
In addition to nutritional and pharmacologic therapy, activity modification may have a role in injury prevention. Gait retraining has been identified as a potential intervention for reducing stress fractures in patients with poor biomechanics.47 Crowell and Davis52 investigated the effect of gait retraining on the forces operating in the tibia in runners. After 1 month of gait retraining, tibial acceleration while running decreased by 50%, vertical force loading rate by 30%, and peak vertical force impact by 20%. Such studies indicate the importance of proper mechanics during repetitive activity, especially in patients not as accustomed to the rigorous training methods used with new military recruits. However, whether these reduced loads translate into reduced risk of stress fracture remains unclear. In addition, biomechanical shoe orthoses may lower the stress fracture risk in military recruits by reducing peak tibial strain.53 Warden and colleagues54 found a mechanical loading program was effective in enchaining the structural properties of bone in rats, leading the authors to hypothesize that a similar program aimed at modifying bone structure in humans could help prevent stress fracture. Although there have been no studies of such a strategy in humans, pretraining may be an area for future research, especially for military recruits.
Conclusion
Compared with the general population, members of the military (new recruits in particular) are at increased risk for bone stress injuries. Most of these injuries occur during basic training, when recruits significantly increase their repetitive physical activity. Although the exact pathophysiology of stress injury is debated, nutritional and metabolic abnormalities are contributors. The indolent nature of these injuries, and their high rate of false-negative plain radiographs, may result in a significant delay in diagnosis in the absence of advanced imaging studies. Although a majority of injuries heal with nonoperative management and NWB, several patterns, especially those on the tension side of the bone, are at high risk for progression to fracture and nonunion. These include lateral femoral cortex stress injuries and anterior tibial cortex fractures. There should be a low threshold for operative management in the setting of delayed union or failed nonoperative therapy. Of equal importance to orthopedic management of these injuries is the management of underlying systemic deficits, which may have subjected the patient to injury in the first place. Supplementation with vitamin D and calcium can be an important prophylaxis against stress injury. In addition, military recruits and athletes with underlying metabolic or hormonal deficiencies should receive proper attention with a focus on balancing energy intake and energy expenditure. Stress injury leading to fracture—increasingly common in military populations—often requires a multimodal approach for treatment and subsequent prevention.
Am J Orthop. 2017;46(4):176-183. Copyright Frontline Medical Communications Inc. 2017. All rights reserved.
1. Briethaupt MD. Zur Pathologie des menschlichen Fusses [To the pathology of the human foot]. Med Zeitung. 1855;24:169-177.
2. Berger FH, de Jonge MC, Maas M. Stress fractures in the lower extremity. Eur J Radiol. 2007;62(1):16-26.
3. Almeida SA, Williams KM, Shaffer RA, Brodine SK. Epidemiological patterns of musculoskeletal injuries and physical training. Med Sci Sports Exerc. 1999;31(8):1176-1182.
4. Jones BH, Thacker SB, Gilchrist J, Kimsey CD, Sosin DM. Prevention of lower extremity stress fractures in athletes and soldiers: a systematic review. Epidemiol Rev. 2002;24(2):228-247.
5. Jacobs JM, Cameron KL, Bojescul JA. Lower extremity stress fractures in the military. Clin Sports Med. 2014;33(4):591-613.
6. Waterman BR, Gun B, Bader JO, Orr JD, Belmont PJ. Epidemiology of lower extremity stress fractures in the United States military. Mil Med. 2016;181(10):1308-1313.
7. Hsu LL, Nevin RL, Tobler SK, Rubertone MV. Trends in overweight and obesity among 18-year-old applicants to the United States military, 1993–2006. J Adolesc Health. 2007;41(6):610-612.
8. Stanitski CL, McMaster JH, Scranton PE. On the nature of stress fractures. Am J Sports Med. 1978;6(6):391-396.
9. Johnson LC. Histogenesis of stress fractures [annual lecture]. Washington, DC: Armed Forces Institute of Pathology; 1963.
10. Friedenberg ZB. Fatigue fractures of the tibia. Clin Orthop Relat Res. 1971;(76):111-115.
11. Cameron KL, Peck KY, Owens BD, et al. Biomechanical risk factors for lower extremity stress fracture. Orthop J Sports Med. 2013;1(4 suppl).
12. Knapik J, Montain S, McGraw S, Grier T, Ely M, Jones B. Stress fracture risk factors in basic combat training. Int J Sports Med. 2012;33(11):940-946.
13. Behrens SB, Deren ME, Matson A, Fadale PD, Monchik KO. Stress fractures of the pelvis and legs in athletes. Sports Health. 2013;5(2):165-174.
14. Mountjoy M, Sundgot-Borgen J, Burke L, et al. The IOC consensus statement: beyond the female athlete triad—relative energy deficiency in sport (RED-S). Br J Sports Med. 2014;48(7):491-497.
15. Maitra RS, Johnson DL. Stress fractures. Clinical history and physical examination. Clin Sports Med. 1997;16(2):259-274.
16. Nieves JW, Melsop K, Curtis M, et al. Nutritional factors that influence change in bone density and stress fracture risk among young female cross-country runners. PM R. 2010;2(8):740-750.
17. Beck BR, Matheson GO, Bergman G, et al. Do capacitively coupled electric fields accelerate tibial stress fracture healing? Am J Sports Med. 2008;36(3):545-553.
18. Simkin A, Leichter I, Giladi M, Stein M, Milgrom C. Combined effect of foot arch structure and an orthotic device on stress fractures. Foot Ankle. 1989;10(1):25-29.
19. 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(2):248-256.
20. Clement D, Ammann W, Taunton J, et al. Exercise-induced stress injuries to the femur. Int J Sports Med. 1993;14(6):347-352.
21. Wood PJ, Barth JH, Freedman DB, Perry L, Sheridan B. Evidence for the low dose dexamethasone suppression test to screen for Cushing’s syndrome—recommendations for a protocol for biochemistry laboratories. Ann Clin Biochem. 1997;34(pt 3):222-229.
22. Bennell K, Matheson G, Meeuwisse W, Brukner P. Risk factors for stress fractures. Sports Med. 1999;28(2):91-122.
23. Prather JL, Nusynowitz ML, Snowdy HA, Hughes AD, McCartney WH, Bagg RJ. Scintigraphic findings in stress fractures. J Bone Joint Surg Am. 1977;59(7):869-874.
24. 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(2):291-306.
25. Boden BP, Osbahr DC. High-risk stress fractures: evaluation and treatment. J Am Acad Orthop Surg. 2000;8(6):344-353.
26. Gaeta M, Minutoli F, Scribano E, et al. CT and MR imaging findings in athletes with early tibial stress injuries: comparison with bone scintigraphy findings and emphasis on cortical abnormalities. Radiology. 2005;235(2):553-561.
27. Matheson GO, Clement DB, Mckenzie DC, Taunton JE, Lloyd-Smith DR, Macintyre JG. Stress fractures in athletes. Am J Sports Med. 1987;15(1):46-58.
28. Iwamoto J, Takeda T. Stress fractures in athletes: review of 196 cases. J Orthop Sci. 2003;8(3):273-278.
29. Noakes TD, Smith JA, Lindenberg G, Wills CE. Pelvic stress fractures in long distance runners. Am J Sports Med. 1985;13(2):120-123.
30. Neubauer T, Brand J, Lidder S, Krawany M. Stress fractures of the femoral neck in runners: a review. Res Sports Med. 2016;24(3):283-297.
31. Evans JT, Guyver PM, Kassam AM, Hubble MJW. Displaced femoral neck stress fractures in Royal Marine recruits—management and results of operative treatment. J R Nav Med Serv. 2012;98(2):3-5.
32. Orava S. Stress fractures. Br J Sports Med. 1980;14(1):40-44.
33. Niva MH, Kiuru MJ, Haataja R, Pihlajamäki HK. Fatigue injuries of the femur. J Bone Joint Surg Br. 2005;87(10):1385-1390.
34. Weishaar MD, McMillian DJ, Moore JH. Identification and management of 2 femoral shaft stress injuries. J Orthop Sports Phys Ther. 2005;35(10):665-673.
35. Salminen ST, Pihlajamäki HK, Visuri TI, Böstman OM. Displaced fatigue fractures of the femoral shaft. Clin Orthop Relat Res. 2003;(409):250-259.
36. Giladi M, Ahronson Z, Stein M, Danon YL, Milgrom C. Unusual distribution and onset of stress fractures in soldiers. Clin Orthop Relat Res. 1985;(192):142-146.
37. Matheson GO, Clement DB, Mckenzie DC, Taunton JE, Lloyd-Smith DR, Macintyre JG. Stress fractures in athletes. Am J Sports Med. 1987;15(1):46-58.
38. Green NE, Rogers RA, Lipscomb AB. Nonunions of stress fractures of the tibia. Am J Sports Med. 1985;13(3):171-176.
39. Orava S, Hulkko A. Stress fracture of the mid-tibial shaft. Acta Orthop Scand. 1984;55(1):35-37.
40. Swenson EJ Jr, DeHaven KE, Sebastianelli WJ, Hanks G, Kalenak A, Lynch JM. The effect of a pneumatic leg brace on return to play in athletes with tibial stress fractures. Am J Sports Med. 1997;25(3):322-328.
41. Rettig AC, Shelbourne KD, McCarroll JR, Bisesi M, Watts J. The natural history and treatment of delayed union stress fractures of the anterior cortex of the tibia. Am J Sports Med. 1988;16(3):250-255.
42. Varner KE, Younas SA, Lintner DM, Marymont JV. Chronic anterior midtibial stress fractures in athletes treated with reamed intramedullary nailing. Am J Sports Med. 2005;33(7):1071-1076.
43. Donahue SW, Sharkey NA. Strains in the metatarsals during the stance phase of gait: implications for stress fractures. J Bone Joint Surg Am. 1999;81(9):1236-1244.
44. Giuliani J, Masini B, Alitz C, Owens BD. Barefoot-simulating footwear associated with metatarsal stress injury in 2 runners. Orthopedics. 2011;34(7):e320-e323.
45. DeLee JC, Evans JP, Julian J. Stress fracture of the fifth metatarsal. Am J Sports Med. 1983;11(5):349-353.
46. 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.
47. Friedl KE, Evans RK, Moran DS. Stress fracture and military medical readiness: bridging basic and applied research. Med Sci Sports Exerc. 2008;40(11 suppl):S609-S622.
48. Lappe J, Cullen D, Haynatzki G, Recker R, Ahlf R, Thompson K. Calcium and vitamin D supplementation decreases incidence of stress fractures in female navy recruits. J Bone Miner Res. 2008;23(5):741-749.
49. DIPART (Vitamin D Individual Patient Analysis of Randomized Trials) Group. Patient level pooled analysis of 68 500 patients from seven major vitamin D fracture trials in US and Europe. BMJ. 2010;340:b5463.
50. Duckham RL, Peirce N, Meyer C, Summers GD, Cameron N, Brooke-Wavell K. Risk factors for stress fracture in female endurance athletes: a cross-sectional study. BMJ Open. 2012;2(6).
51. 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):418-424.
52. Crowell HP, Davis IS. Gait retraining to reduce lower extremity loading in runners. Clin Biomech. 2011;26(1):78-83.
53. 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):866-870.
54. Warden SJ, Hurst JA, Sanders MS, Turner CH, Burr DB, Li J. Bone adaptation to a mechanical loading program significantly increases skeletal fatigue resistance. J Bone Miner Res. 2005;20(5):809-816.
1. Briethaupt MD. Zur Pathologie des menschlichen Fusses [To the pathology of the human foot]. Med Zeitung. 1855;24:169-177.
2. Berger FH, de Jonge MC, Maas M. Stress fractures in the lower extremity. Eur J Radiol. 2007;62(1):16-26.
3. Almeida SA, Williams KM, Shaffer RA, Brodine SK. Epidemiological patterns of musculoskeletal injuries and physical training. Med Sci Sports Exerc. 1999;31(8):1176-1182.
4. Jones BH, Thacker SB, Gilchrist J, Kimsey CD, Sosin DM. Prevention of lower extremity stress fractures in athletes and soldiers: a systematic review. Epidemiol Rev. 2002;24(2):228-247.
5. Jacobs JM, Cameron KL, Bojescul JA. Lower extremity stress fractures in the military. Clin Sports Med. 2014;33(4):591-613.
6. Waterman BR, Gun B, Bader JO, Orr JD, Belmont PJ. Epidemiology of lower extremity stress fractures in the United States military. Mil Med. 2016;181(10):1308-1313.
7. Hsu LL, Nevin RL, Tobler SK, Rubertone MV. Trends in overweight and obesity among 18-year-old applicants to the United States military, 1993–2006. J Adolesc Health. 2007;41(6):610-612.
8. Stanitski CL, McMaster JH, Scranton PE. On the nature of stress fractures. Am J Sports Med. 1978;6(6):391-396.
9. Johnson LC. Histogenesis of stress fractures [annual lecture]. Washington, DC: Armed Forces Institute of Pathology; 1963.
10. Friedenberg ZB. Fatigue fractures of the tibia. Clin Orthop Relat Res. 1971;(76):111-115.
11. Cameron KL, Peck KY, Owens BD, et al. Biomechanical risk factors for lower extremity stress fracture. Orthop J Sports Med. 2013;1(4 suppl).
12. Knapik J, Montain S, McGraw S, Grier T, Ely M, Jones B. Stress fracture risk factors in basic combat training. Int J Sports Med. 2012;33(11):940-946.
13. Behrens SB, Deren ME, Matson A, Fadale PD, Monchik KO. Stress fractures of the pelvis and legs in athletes. Sports Health. 2013;5(2):165-174.
14. Mountjoy M, Sundgot-Borgen J, Burke L, et al. The IOC consensus statement: beyond the female athlete triad—relative energy deficiency in sport (RED-S). Br J Sports Med. 2014;48(7):491-497.
15. Maitra RS, Johnson DL. Stress fractures. Clinical history and physical examination. Clin Sports Med. 1997;16(2):259-274.
16. Nieves JW, Melsop K, Curtis M, et al. Nutritional factors that influence change in bone density and stress fracture risk among young female cross-country runners. PM R. 2010;2(8):740-750.
17. Beck BR, Matheson GO, Bergman G, et al. Do capacitively coupled electric fields accelerate tibial stress fracture healing? Am J Sports Med. 2008;36(3):545-553.
18. Simkin A, Leichter I, Giladi M, Stein M, Milgrom C. Combined effect of foot arch structure and an orthotic device on stress fractures. Foot Ankle. 1989;10(1):25-29.
19. 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(2):248-256.
20. Clement D, Ammann W, Taunton J, et al. Exercise-induced stress injuries to the femur. Int J Sports Med. 1993;14(6):347-352.
21. Wood PJ, Barth JH, Freedman DB, Perry L, Sheridan B. Evidence for the low dose dexamethasone suppression test to screen for Cushing’s syndrome—recommendations for a protocol for biochemistry laboratories. Ann Clin Biochem. 1997;34(pt 3):222-229.
22. Bennell K, Matheson G, Meeuwisse W, Brukner P. Risk factors for stress fractures. Sports Med. 1999;28(2):91-122.
23. Prather JL, Nusynowitz ML, Snowdy HA, Hughes AD, McCartney WH, Bagg RJ. Scintigraphic findings in stress fractures. J Bone Joint Surg Am. 1977;59(7):869-874.
24. 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(2):291-306.
25. Boden BP, Osbahr DC. High-risk stress fractures: evaluation and treatment. J Am Acad Orthop Surg. 2000;8(6):344-353.
26. Gaeta M, Minutoli F, Scribano E, et al. CT and MR imaging findings in athletes with early tibial stress injuries: comparison with bone scintigraphy findings and emphasis on cortical abnormalities. Radiology. 2005;235(2):553-561.
27. Matheson GO, Clement DB, Mckenzie DC, Taunton JE, Lloyd-Smith DR, Macintyre JG. Stress fractures in athletes. Am J Sports Med. 1987;15(1):46-58.
28. Iwamoto J, Takeda T. Stress fractures in athletes: review of 196 cases. J Orthop Sci. 2003;8(3):273-278.
29. Noakes TD, Smith JA, Lindenberg G, Wills CE. Pelvic stress fractures in long distance runners. Am J Sports Med. 1985;13(2):120-123.
30. Neubauer T, Brand J, Lidder S, Krawany M. Stress fractures of the femoral neck in runners: a review. Res Sports Med. 2016;24(3):283-297.
31. Evans JT, Guyver PM, Kassam AM, Hubble MJW. Displaced femoral neck stress fractures in Royal Marine recruits—management and results of operative treatment. J R Nav Med Serv. 2012;98(2):3-5.
32. Orava S. Stress fractures. Br J Sports Med. 1980;14(1):40-44.
33. Niva MH, Kiuru MJ, Haataja R, Pihlajamäki HK. Fatigue injuries of the femur. J Bone Joint Surg Br. 2005;87(10):1385-1390.
34. Weishaar MD, McMillian DJ, Moore JH. Identification and management of 2 femoral shaft stress injuries. J Orthop Sports Phys Ther. 2005;35(10):665-673.
35. Salminen ST, Pihlajamäki HK, Visuri TI, Böstman OM. Displaced fatigue fractures of the femoral shaft. Clin Orthop Relat Res. 2003;(409):250-259.
36. Giladi M, Ahronson Z, Stein M, Danon YL, Milgrom C. Unusual distribution and onset of stress fractures in soldiers. Clin Orthop Relat Res. 1985;(192):142-146.
37. Matheson GO, Clement DB, Mckenzie DC, Taunton JE, Lloyd-Smith DR, Macintyre JG. Stress fractures in athletes. Am J Sports Med. 1987;15(1):46-58.
38. Green NE, Rogers RA, Lipscomb AB. Nonunions of stress fractures of the tibia. Am J Sports Med. 1985;13(3):171-176.
39. Orava S, Hulkko A. Stress fracture of the mid-tibial shaft. Acta Orthop Scand. 1984;55(1):35-37.
40. Swenson EJ Jr, DeHaven KE, Sebastianelli WJ, Hanks G, Kalenak A, Lynch JM. The effect of a pneumatic leg brace on return to play in athletes with tibial stress fractures. Am J Sports Med. 1997;25(3):322-328.
41. Rettig AC, Shelbourne KD, McCarroll JR, Bisesi M, Watts J. The natural history and treatment of delayed union stress fractures of the anterior cortex of the tibia. Am J Sports Med. 1988;16(3):250-255.
42. Varner KE, Younas SA, Lintner DM, Marymont JV. Chronic anterior midtibial stress fractures in athletes treated with reamed intramedullary nailing. Am J Sports Med. 2005;33(7):1071-1076.
43. Donahue SW, Sharkey NA. Strains in the metatarsals during the stance phase of gait: implications for stress fractures. J Bone Joint Surg Am. 1999;81(9):1236-1244.
44. Giuliani J, Masini B, Alitz C, Owens BD. Barefoot-simulating footwear associated with metatarsal stress injury in 2 runners. Orthopedics. 2011;34(7):e320-e323.
45. DeLee JC, Evans JP, Julian J. Stress fracture of the fifth metatarsal. Am J Sports Med. 1983;11(5):349-353.
46. 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.
47. Friedl KE, Evans RK, Moran DS. Stress fracture and military medical readiness: bridging basic and applied research. Med Sci Sports Exerc. 2008;40(11 suppl):S609-S622.
48. Lappe J, Cullen D, Haynatzki G, Recker R, Ahlf R, Thompson K. Calcium and vitamin D supplementation decreases incidence of stress fractures in female navy recruits. J Bone Miner Res. 2008;23(5):741-749.
49. DIPART (Vitamin D Individual Patient Analysis of Randomized Trials) Group. Patient level pooled analysis of 68 500 patients from seven major vitamin D fracture trials in US and Europe. BMJ. 2010;340:b5463.
50. Duckham RL, Peirce N, Meyer C, Summers GD, Cameron N, Brooke-Wavell K. Risk factors for stress fracture in female endurance athletes: a cross-sectional study. BMJ Open. 2012;2(6).
51. 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):418-424.
52. Crowell HP, Davis IS. Gait retraining to reduce lower extremity loading in runners. Clin Biomech. 2011;26(1):78-83.
53. 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):866-870.
54. Warden SJ, Hurst JA, Sanders MS, Turner CH, Burr DB, Li J. Bone adaptation to a mechanical loading program significantly increases skeletal fatigue resistance. J Bone Miner Res. 2005;20(5):809-816.
