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The effects of a 5-month physical training on iliac bone morphology in monkeys

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Summary

The present study was designed to provide data on the effects on bone of 5 months of daily exercise in nonhuman primates. The subjects were five male rhesus monkeys with mature skeletons with a body mass of 8–10 kg. The exercise schedule selected to provide endurance training was a daily continuous 1-h climbing task. An iliac crest bone biopsy was performed prior to and at the end of the physical training. The histomorphometric bone study was based upon bone mass and bone cell activity measurements made on nondecalcified bone slides, using trichromic and fluorescent labelling techniques. Results showed a decrease in bone formation, resulting in reduced bone mass at the end of the 5 months. This effect is suggested to be related to the unphysiological climbing regimen imposed on these animals which are naturally used to short periods of rapid exercise. From these investigations it was concluded that even if it is well tolerated, long-term physical endurance training can induce bone loss in primates. Further investigations are needed to determine with accuracy the relationships between bone physiology and physical exercise, and particularly with regard to its type, intensity and duration.

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References

  • Aloia JF, Cohn SH, Ostuni JA, Cane R, Ellis K (1978) Prevention of involutional bone loss by exercise. Ann Intern Med 89:356–358

    Google Scholar 

  • Baron R, Vignery A, Neff L, Silverglate A, Santa Maria A (1983) Processing of undecalcified bone specimens for bone histomorphometry. In: Recker E (ed) Bone histomorphometry. Technique and interpretation. CRC Press, Boca Raton, Fla., pp 13–35

    Google Scholar 

  • Bell NH, Godsen RN, Henry DP, Shary J, Epstein S (1988) The effects of muscle-building exercise on vitamin-D and mineral metabolism. J Bone Min Res 3:369–373

    Google Scholar 

  • Bernard J, Ribot C, Guezennee C, Montalègre JF, Garry P, Becker JM, Moulinas JM (1988) Etude longitudinale de la densité osseuse vertébrale de jeunes recrues soumises à un exercice physique contrôlé. Méd Armées 16:573–576

    Google Scholar 

  • Bilanin JE, Suzette-Blanchard M, Russek-Cohen E (1989) Lower vertebral bone density in male long distance runners. Med Sci Sports Exerc 21:66–70

    Google Scholar 

  • Bourne GH (1975) Collected anatomical and physiological data from the Rhesus monkey. In: Bourne GH (ed) The rhesus monkey. Academic Press, New York, pp 1–63

    Google Scholar 

  • Bourrin S, Zérath E, Vico L, Milhaud C, Alexandre C (1992) Bone mass and bone cellular variations after five months of physical training in rhesus monkeys: histomorphometric study. Calcif Tissue Int 50:404–410

    Google Scholar 

  • Cann EC, Genant HK, Young DR (1980) Comparison of vertebral and peripheral mineral losses in disuse osteoporosis in monkeys. Radiology 134:525–529

    Google Scholar 

  • Cheverud JM (1981) Epiphyseal union and dental eruption in Macaca mulatta. Am J Phys Anthropol 56:157–167

    Google Scholar 

  • Compston JE, Mellish RWE, Croucher P, Newcombe R, Garrahan NJ (1989) Structural mechanisms of trabecular bone loss in man. Bone Mineral 6:339–350

    Google Scholar 

  • Dalen N, Olsson KE (1974) Bone mineral content and physical activity. Acta Orthop Scand 45:170–174

    Google Scholar 

  • Dalsky GP (1989) The role of exercise in the prevention of osteoporosis. Compr Ther 15:30–37

    Google Scholar 

  • Dalsky GP, Stocke KS, Ehsani AA, Slatopolski E, Lee WC, Birge SJ (1988) Weight-bearing exercise training and lumbar bone mineral content in postmenopausal women. Ann Intern Med 108:824–828

    Google Scholar 

  • Dempster DW (1989) Perspectives. Bone histomorphometry in glucocorticoid-induced osteoporosis. J Bone Min Res 4:137–141

    Google Scholar 

  • Devlin H, Ferguson MWJ, Carter DH (1990) Cancellous bone resorption in the proximal ilium of the ovariectomized rat. Calcif Tissue Int 46:395–400

    Google Scholar 

  • Drinkwater BL, Nilson K, Chesnut III CH, Bremner WJ, Shainholtz S, Southworth MB (1984) Bone mineral content of amenorrheic and eumenorrheic athletes. N Engl J Med 311:277–281

    Google Scholar 

  • Egrise D, Martin D, Vienne A, Neve P, Schoutens A (1992) The number of fibroblastic colonies formed from bone marrow is decreased and the in vitro proliferation rate of trabecular bone cells increased in aged rats. Bone 13:355–361

    Google Scholar 

  • Faugère MC, Friedler RM, Fanti P, Malluche HH (1990) Bone changes occurring early after cessation of ovarian function in Beagle dogs: a histomorphometric study employing sequential biopsies. J Bone Min Res 5:263–271

    Google Scholar 

  • Frost HM (1987) Bone “mass” and the “mechanostat”: a proposal. Anat Rec 219:1–9

    Google Scholar 

  • Gisolfi CV, Mora F, Natterman R, Myers RD (1978) New apparatus for exercising a monkey seated in a primate chair. J Appl Physiol 44:129–132

    Google Scholar 

  • Goldstein SA (1987) The mechanical properties of trabecular bone: dependance on anatomic location and function. J Biomech 20:1055–1061

    Google Scholar 

  • Grigoriev AI, Koslovskaya IB (1988) Physiological responses of skeletomuscular system to muscle exercises under long-term hypokinetic conditions. Physiologist 31:S93-S97

    Google Scholar 

  • Hackney AC, Sinning WE, Bruot BC (1988) Reproductive hormonal profiles of endurance-trained and untrained males. Med Sci Sports Exerc 20:60–65

    Google Scholar 

  • Hohimer AR, Hales JR, Rowell LB, Smith OA (1983) Regional distribution of blood flow during mild dynamic leg exercise in the baboon. J Appl Physiol 55:1173–1177

    Google Scholar 

  • Hou JCH, Salem GJ, Zernicke RF, Barnard J (1990) Structural and mechanical adaptations of immature trabecular bone to strenuous exercise. J Appl Physiol 69:1309–1314

    Google Scholar 

  • Jaworski ZFG, Kimmel DB, Jee WSS (1983) Cell kinetics underlying skeletal growth and bone tissue turnover. In: Recker E (ed) Bone histomorphometry. Techniques and interpretation. CRC Press, Boca Raton, Fla., pp 241–264

    Google Scholar 

  • Jee WSS, Park HZ, Roberts WE, Kenner GH (1970) Corticosteroid and bone. Am J Anat 129:477–480

    Google Scholar 

  • Kerr GR, Weisman HA, Allen JA, Wallace J, Scheffler G (1973) Malnutrition studies in Macaca mulatta. II — The effect on organ size and skeletal growth. Am J Clin Nutr 26:620–630

    Google Scholar 

  • Kiiskinen A (1977) Physical training and connective tissues in young mice. Physical properties of Achilles tendons and long bones. Growth 41:123–137

    Google Scholar 

  • Kirk JH (1972) Growth of maturing Macaca mulatta. Lab Anim Sci 22:573–575

    Google Scholar 

  • Klein-Nulend J, Veldhuijzen JP, De Jong M, Burger EH (1987) Increased bone formation and decreased bone resorption in fetal mouse calvaria as a result of intermittent compressive force in vitro. Bone Min 2:441–448

    Google Scholar 

  • Lanyon LE, Rubin CT, Baust G (1986) Modulation of bone loss during calcium insufficiency of controlled dynamic loading. Calcif Tissue Int 38:209–216

    Google Scholar 

  • Leblanc AD, Evans HJ, Johnson PC, Jhingran S (1983) Changes in total body calcium balance with exercise in the rat. J Appl Physiol 55:201–204

    Google Scholar 

  • Lindsay R (1987) Prevention of osteoporosis. Clin Orthop Rel Res 222:44–59

    Google Scholar 

  • Ljunghall S, Joborn H, Roxin LE, Skarfors ET, Wide LE, Lithell HO (1988) Increase in serum parathyroid hormone levels after prolonged physical exercise. Med Sci Sports Exerc 20:122–125

    Google Scholar 

  • Longcope C, Hoberg S, Steuterman S, Baran D (1989) The effect of ovariectomy on spine bone mineral density in rhesus monkeys. Bone 10:341–344

    Google Scholar 

  • Mahoney SA (1980) Cost of locomotion and heat balance during rest and running from 0 to 55° C in a patas monkey. J Appl Physiol 49:789–800

    Google Scholar 

  • Meunier PJ (1982) Mécanismes histologiques des ostéoporoses. Déductions thérapeutiques. Rev Fr Endocrinol Clin 23:161–169

    Google Scholar 

  • Milhaud C (1987) Modèles animaux et étude des effets de la microgravité. I — Intérêt des modèles. Bull Acad Vét Fr 60:435–440

    Google Scholar 

  • Napier JR, Napier PH (1973) A handbook of living primates. Academic Press, London, 415 p

    Google Scholar 

  • National Academy of Sciences (1978) Nutrient requirements of nonhuman Primates. In: Requirements of Domestic Animal Series n° 14, National Research Council, Washington DC

    Google Scholar 

  • Nogués C, Milhaud C (1988) A new technique for iliac crest biopsy in rhesus monkeys for use in weightlessness experiments: some results of ground studies. Aviat Space Environ Med 59:374–378

    Google Scholar 

  • Nogués C, Milhaud C, Pesquiès P (1984) Use of primate model in weightlessness bone physiology. Histological approach after iliac crest biopsy. Bone Mineralization Workshop, Brussels, ESA SP-203

  • Nunamaker DM, Butterweck DM, Provost MT (1990) Fatigue fractures in thoroughbred racehorses: relationship with age, peak bone strain and training. J Orthop Res 8:604–611

    Google Scholar 

  • Parfitt AM, Drezner MK, Glorieux FH, Kanis JA, Malluche H, Meunier PJ, Ott SM, Recker RR (1987) Bone histomorphometry: standardization of nomenclature, symbols and units. J Bone Min Res 2:595–610

    Google Scholar 

  • Pope NS, Gould KG, Anderson DC, Mann DR (1989) Effects of age and sex on bone density in the rhesus monkey. Bone 10:109–112

    Google Scholar 

  • Robertshaw D, Taylor CR, Mazzia LM (1973) Sweating in primates: secretion by adrenal medulla during exercise. Am J Physiol 224:678–681

    Google Scholar 

  • Rubin CT, Pratt GW, Porter AL, Lanyon LE, Poss R (1988) Ultrasonic measurement of immobilization-induced osteopenia: an experimental study in sheep. Calcif Tissue Int 42:309–312

    Google Scholar 

  • Rubin CT, Bain SD, McLeod KJ (1992) Suppression of the osteogenic response in the aging skeleton. Calcif Tissue Int 50:306–313

    Google Scholar 

  • Sandler RB (1988) Muscle strength and skeletal competence: implications for early prophylaxis. Calcif Tissue Int 42:281–283

    Google Scholar 

  • Silbermann M, Bar-Shira-Maymon B, Coleman R, Reznick A, Weisman Y, Steinhagen-Thiessen E, Von der Mark H, Von der Mark K (1990) Long-term physical exercise retards trabecular bone loss in lumbar vertebrae of aging female mice. Calcif Tissue Int 46:80–93

    Google Scholar 

  • Smith OA, King RL, Rushmer RF, Ruch TC (1962) Techniques for determination of cardiovascular response to exercise in unanesthetized monkeys. J Appl Physiol 17:718–721

    Google Scholar 

  • Woo SLY, Kuei SC, Amiel D, Gomez MA, Hayes WC, White FC, Akeson WH (1981) The effect of prolonged physical training on the properties of long bone: a study of Wolff's law. J Bone Joint Surg 63A:780–787

    Google Scholar 

  • Young DR, Thomson GA, Howard WH, Adachi RR, Lutwak L (1975) Short-term blood calcium regulation in the monkey. Indian J Nutr Diet 12:243–257

    Google Scholar 

  • Zérath E, Mestries JC, Gan C, Nogués C, Milhaud C (1990a) Five months of daily standardized exercise for sedentary monkeys. J Med Primatol 19:583–594

    Google Scholar 

  • Zérath E, Nogués C, Borne M, Sourdaine P (1990b) Bone effects of 13 days of weightlessness on rat and monkey. Some results of Biocosmos 1887 and ground simulations. Physiologist 33:S94-S95

    Google Scholar 

  • Zérath E, Holy X, Malouvier A, Caissard JC, Nogués C (1991) Rat and monkey bone study in the Biocosmos 2044 space experiment. Physiologist 34:S194-S195

    Google Scholar 

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Zerath, E., Milhaud, C. & Nogues, C. The effects of a 5-month physical training on iliac bone morphology in monkeys. Europ. J. Appl. Physiol. 67, 1–6 (1993). https://doi.org/10.1007/BF00377695

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