Stress Fractures in Military Men and Bone Quality Related Factors

Abstract

The aetiology of stress fractures is multifactorial, and many risk factors have been implicated. The aim of this study was to explore the relationship between stress fractures, factors and biochemical markers related to bone metabolism, and calcaneal stiffness index measured by quantitative ultrasound in a case control study including male military personnel beyond basic training. Thirty-two male patients with stress fractures were matched with 32 uninjured-healthy volunteers by age, height, body weight and level of physical performance. A questionnaire concerning the calcium intake, alcohol consumption and smoking was completed, the values of several biochemical markers were measured from blood samples, and calcaneal quantitative ultrasound was measured by heel ultrasound for all participants. Statistically significant higher levels of albumin (4.59 ± 0.28 vs. 4.40 ± 0.25, p = 0.006) and lower levels of serum osteocalcin (6.26 ± 1.74 vs. 7.40 ± 1.80, p = 0.012), mean values of T-scores (− 0.21 ± 0.95 vs. 0.33 ± 0.82, p = 0.018) and Z-scores (− 0.14 ± 0.81 vs. 0.33 ± 0.71, p = 0.016) were found among patients compared to controls. Based on the results, it seems that a decreased bone turnover and a low calcaneal stiffness index may be related to the incidence of stress fractures amongst male military personnel.

Key words

bone metabolism - bone density - calcaneal quantitative ultrasound - stress fracture

References

• 1 Altarac M, Gardner J W, Popovich R M, Potter R, Knapik J J, Jones B H. Cigarette smoking and exercise-related injuries among young men and women.  Am J Prev Med. 2000;  18 96-102
• 2 Armstrong D WIII, Rue J P, Wilckens J H, Frassica F J. Stress fracture injury in young military men and women.  Bone. 2004;  35 806-816
• 3 Beck T J, Ruff C B, Mourtada F A, Shaffer R A, Maxwell-Williams K, Kao G L, Sartoris D J, Brodine S. Dual-energy X‐ray absorptiometry derived structural geometry for stress fracture prediction in male U.S. Marine Corps recruits.  J Bone Miner Res. 1996;  11 645-653
• 4 Beck T J, Ruff C B, Shaffer R A, Betsinger K, Trone D W, Brodine S K. Stress fracture in military recruits: gender differences in muscle and bone susceptibility factors.  Bone. 2000;  27 43-44
• 5 Bennell K, Matheson G, Meeuwisse W, Brukner P. Risk factors for stress fractures.  Sports Med. 1999;  28 91-122
• 6 Bikle D, Genant H, Cann C, Recker R, Halloran B, Strewler G. Bone disease in alcohol abuse.  Ann Intern Med. 1985;  103 42-48
• 7 Black J R. Stress fractures of the foot in female soldiers: a two-year survey.  Mil Med. 1982;  147 861-862
• 8 Brown J P, Delmas P D, Malaval L, Edouard C, Chapuy M C, Meunier P J. Serum bone Gla-protein: a specific marker for bone formation in postmenopausal osteoporosis.  Lancet. 1984;  1 1091-1093
• 9 Burr D B. Bone, exercise, and stress fractures.  Exerc Sport Sci Rev. 1997;  25 171-194
• 10 Cline A D, Jansen G R, Melby C L. Stress fractures in female army recruits: implications of bone density, calcium intake, and exercise.  J Am Coll Nutr. 1998;  17 128-135
• 11 Court-Brown C, McQeen M, Tornetta P III. Stress fractures. Schepsis AA, Busconi BD, Tornetta P, Einhorn TA Orthopaedic Surgery Essentials: Trauma. Philadelphia; Lippincott Williams & Wilkins 2006: 32-42
• 12 Cummings S, Nevitt M, Browner W, Stone K, Fox K, Ensrud K, Cauley J, Black D, Vogt T. Risk factors for hip fractures in white women.  N Engl J Med. 1995;  332 767-773
• 13 Delmas P D, Christiansen C, Mann K G, Price P A. Bone Gla protein (osteocalcin) assay standardization report.  J Bone Miner Res. 1990;  5 5-11
• 14 Dressendorfer R, Wade C, Claybaugh S, Cucinell S, Timmis G. Effects of 7 successive days of unaccustomed prolonged exercise on aerobic performance and tissue damage in fitness joggers.  Int J Sports Med. 1991;  12 55-61
• 15 Feitelberg S, Epstein S, Ismail F, D'Amanda C. Deranged bone mineral metabolism in chronic alcoholism.  Metabolism. 1987;  36 322-326
• 16 Felson D, Kiel D, Anderson J, Kannel W. Alcohol consumption and hip fractures.  Am J Epidemiol. 1988;  128 1102-1110
• 17 Forsen L, Bjorndal A, Bjartveit K, Edna T, Holmen J, Jessen V, Westberg G. Interaction between current smoking, leanness, and physical inactivity in the prediction of hip fracture.  J Bone Miner Res. 1994;  9 1671-1678
• 18 Friedl K E, Nuovo J A, Patience T H, Dettori J R. Factors associated with stress fracture in young Army women: indications for further research.  Mil Med. 1992;  157 334-338
• 19 Gardner L, Dziados J, Jones B, Brundage J, Harris J, Sullivan R, Gill P. Prevention of lower extremity stress fractures: a controlled trial of a shock absorbent insole.  Am J Public Health. 1988;  78 1563-1567
• 20 Garnero P, Sornay-Rendu E, Chapuy M C, Delmas P D. Increased bone turnover in late postmenopausal women is a major determinant of osteoporosis.  J Bone Miner Res. 1996;  11 337-349
• 21 Gefen A. Biomechanical analysis of fatigue-related foot injury mechanisms in athletes and recruits during intensive marching.  Med Biol Eng Comput. 2002;  40 302-310
• 22 Giladi M, Milgrom C, Simkin A, Danon Y. Stress fractures. Identifiable risk factors.  Am J Sports Med. 1991;  19 647-652
• 23 Givon U, Friedman E, Reiner A, Vered I, Finestone A, Shemer J. Stress fractures in the Israeli defense forces from 1995 to 1996.  Clin Orthop. 2000;  373 227-232
• 24 Hansen M, Overgaard K, Riis B, Christiansen C. Potential risk factors for development of postmenopausal osteoporosis – examined over a 12-year period.  Osteoporos Int. 1991;  1 95-102
• 25 Hemenway D, Colditz G, Willett W, Stampfer M, Speizer F. Fractures and lifestyle: effect of cigarette smoking, alcohol intake, and relative weight on the risk of hip and forearm fractures in middle-aged women.  Am J Public Health. 1998;  78 1554-1558
• 26 Hershman E, Mailly T. Stress fractures.  Clin Sports Med. 1990;  9 183-214
• 27 Hoffman J R, Chapnik L, Shamis A, Givon U, Davidson B. The effect of leg strength on the incidence of lower extremity overuse injuries during military training.  Mil Med. 1999;  164 153-156
• 28 Honkanen R, Tuppurainen M, Kroger H, Alhava E, Saarikoski S. Relationships between risk factors and fractures differ by type of fracture: a population-based study of 12 192 perimenopausal women.  Osteoporos Int. 1998;  8 25-31
• 29 Ivaska K K, Hentunen T A, Vaaraniemi J, Ylipahkala H, Pettersson K, Vaananen H K. Release of intact and fragmented osteocalcin molecules from bone matrix during bone resorption in vitro.  J Biol Chem. 2004;  279 18361-18369
• 30 Johnell O, Nilsson B, Wiklund P. Bone morphometry in alcoholics.  Clin Orthop. 1982;  165 253-258
• 31 Jones B, Bovee B, Harris J, Cowan D. Intrinsic risk factors for exercise-related injuries among male and female army trainees.  Am J Sports Med. 1993;  21 705-710
• 32 Jones B H, Thacker S B, Gilchrist J, Kimsey Jr C D, Sosin D M. Prevention of lower extremity stress fractures in athletes and soldiers: a systematic review.  Epidemiol Rev. 2002;  24 228-247
• 33 Kim D J, Park B L, Koh J-M, Kim G S, Kim L H, Cheong H S, Shin H D, Hong J M, Kim T H, Shin H I, Park E K, Kim S Y. Methionine synthase reductase polymorphisms are associated with serum osteocalcin levels in postmenopausal women.  Exp Mol Med. 2006;  38 519-524
• 34 Koplan J, Powell K, Shiriey R, Campbell C. An epidemiologic study of the benefits and risks of running.  JAMA. 1979;  248 3118-3121
• 35 Lappe J, Davies K, Recker R, Heaney R. Quantitative ultrasound: use in screening for susceptibility to stress fractures in female army recruits.  J Bone Miner Res. 2005;  20 571-578
• 36 Macera C. Lower extremity injuries in runners.  Sports Med. 1992;  13 50-57
• 37 Markey K L. Stress fractures.  Clin Sports Med. 1987;  6 405-426
• 38 McBryde Jr A M. Stress fractures in runners.  Clin Sports Med. 1985;  4 737-752
• 39 Milgrom C, Finestone A, Sharkey N, Hamel A, Mandes V, Burr D, Arndt A, Ekenman I. Metatarsal strains are sufficient to cause fatigue fracture during cyclic overloading.  Foot Ankle Int. 2002;  23 230-235
• 40 Milgrom C, Giladi M, Simkin A, Rand N, Kedem R, Kashtan H, Stein M, Gomori M. The area moment of inertia of the tibia: a risk factor for stress fractures.  J Biomech. 1989;  22 1243-1248
• 41 Myburgh K H, Hutchins J, Fataar A B, Hough S F, Noakes T D. Low bone density is an etiologic factor for stress fractures in athletes.  Ann Intern Med. 1990;  113 754-759
• 42 Nattiv A, Armsey Jr T D. Stress injury to bone in the female athlete.  Clin Sports Med. 1997;  16 197-224
• 43 Nilsson B, Westlin N. Serum density in alcoholism and after gastrectomy.  Calcif Tissue Res. 1972;  10 229-232
• 44 Page A E, Hayman A R, Andersson L MB, Chambers T J, Warburton M J. Degradation of bone matrix proteins by osteoclast cathepsins.  Int J Biochem. 1993;  25 545-550
• 45 Pouilles J M, Bernard J, Tremollieres F, Louvet J P, Ribot C. Femoral bone density in young male adults with stress fractures.  Bone. 1989;  10 105-108
• 46 Protzman R R, Griffis C G. Stress fractures in men and women undergoing military training.  J Bone Joint Surg Am. 1977;  59 825
• 47 Ross J, Woodward A. Risk factors for injury during basic military training.  J Med. 1994;  36 1120-1126
• 48 Roy S, DeLuca C, Snyder-Mackler L, Emley M, Crenshaw R, Lyons J. Fatigue, recovery and low back pain in varsity rowers.  Med Sci Sports Exerc. 1990;  22 463-469
• 49 Saville P. Changes in bone mass with age and alcoholism.  J Bone Joint Surg Am. 1965;  47 492-499
• 50 Shaffer R A, Brodine S K, Almeida S A, Williams K M, Ronaghy S. Use of simple measures of physical activity to predict stress fractures in young men undergoing a rigorous physical training program.  Am J Epidemiol. 1999;  149 236-242
• 51 Sharkey N A, Ferris L, Smith T S, Matthews D K. Strain and loading of the second metatarsal during heel-lift.  J Bone Joint Surg Am. 1995;  77 1050-1057
• 52 Swissa A, Milgrom C, Giladi M, Kashtan H, Stein M, Margulies J, Chisin R, Aharonson Z. The effect of pretraining sports activity on the incidence of stress fractures among military recruits. A prospective study.  Clin Orthop. 1989;  245 256-260
• 53 Taimela S, Kujala U, Osterman K. Stress injury proneness: a prospective study during a physical training program.  Int J Sports Med. 1999;  11 162-165
• 54 Taimela S, Kujala U M, Dahlstrom S. Risk factors for stress fractures during physical training programs.  Clin J Sports Med. 1992;  2 105-108
• 55 Valimaki V-V, Alfthan H, Lehmuskallio E, Löyttyniemi E, Sahi T, Suominen H, Välimäki M J. Risk factors for clinical stress fractures in male military recruits: a prospective cohort study.  Bone. 2005;  37 267-273
• 56 Valimaki V-V, Piippo K, Valimaki S, Loyttyniemi E, Kontula K, Valimaki M J. Relation of the XbaI and PvuII polymorphisms of the estrogen receptor gene and the CAG repeat polymorphism of the androgen receptor gene to peak bone mass and bone turnover rate among young healthy men.  Osteoporos Int. 2005;  16 1633-1640
• 57 Warden S J, Burr D B, Brukner P D. Stress fractures: pathophysiology, epidemiology, and risk factors.  Curr Osteoporos Rep. 2006;  4 103-109
• 58 Williams A, Weiss N, Ure C. Effect of weight, smoking and estrogen use on the risk of hip and forearm fractures in postmenopausal women.  Obstet Gynecol. 1982;  60 695-699
• 59 Winfield A C, Moore J, Bracker M, Johnson C W. Risk factors associated with stress reactions in female Marines.  Mil Med. 1997;  162 698-702
• 60 Zanker C L, Swaine I L. Responses of bone turnover markers to repeated endurance running in humans under conditions of energy balance or energy restriction.  Eur J Appl Physiol. 2000;  83 434-440