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Published in: Calcified Tissue International 6/2013

01-12-2013 | Original Research

Influence of Food Restriction Combined with Voluntary Running on Bone Morphology and Strength in Male Rats

Authors: Satoshi Hattori, Jong-Hoon Park, Umon Agata, Takayuki Akimoto, Masaya Oda, Michito Higano, Yuki Aikawa, Yoshiharu Nabekura, Hideyuki Yamato, Ikuko Ezawa, Naomi Omi

Published in: Calcified Tissue International | Issue 6/2013

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Abstract

Athletes, in particular endurance athletes and dancers, are chronically exposed to a state of low energy availability due to insufficient dietary energy intake and massive exercise energy expenditure. Low energy availability sometimes causes bone fragility, thereby increasing the risk of bone disorders. Although the decrease in energy availability shows no sexual dimorphism, epidemiological studies have reported that bone disorders are less frequent in male athletes than in female athletes. We hypothesized that bone tissue was not affected by low energy availability in males. The purpose of this study was to examine the influence of food restriction combined with voluntary running training on bone morphology and strength in adult male rats. Fourteen-week-old male Sprague–Dawley rats were divided randomly into four groups: control (C) group, food restriction (R) group, exercise (Ex) group, and food restriction plus exercise (REx) group. For the R and REx groups, 30 % food restriction was carried out in comparison with the C group. Bone strength, bone mineral density (BMD), bone architecture, and bone turnover rate were measured after a 13-week experimental period. Bone strength was not significantly lower in the REx group compared with the C group. BMD and trabecular bone volume showed no difference among groups. These findings indicate that bone morphology and strength were little affected by food restriction combined with exercise training in adult male rats.
Literature
1.
go back to reference Front HM (1979) Treatment of osteoporoses by manipulation of coherent bone cell populations. Clin Orthop Relat Res 143:227–244 Front HM (1979) Treatment of osteoporoses by manipulation of coherent bone cell populations. Clin Orthop Relat Res 143:227–244
2.
go back to reference Kanis JA (2002) Diagnosis of osteoporosis and assessment of fracture risk. Lancet 359(9321):1929–1936PubMedCrossRef Kanis JA (2002) Diagnosis of osteoporosis and assessment of fracture risk. Lancet 359(9321):1929–1936PubMedCrossRef
4.
go back to reference Iwamoto J, Takeda T, Ichimura S (1998) Effect of exercise on tibial and lumbar vertebral bone mass in mature osteopenic rats: bone histomorphometry study. J Orthop Sci 3(5):257–263PubMedCrossRef Iwamoto J, Takeda T, Ichimura S (1998) Effect of exercise on tibial and lumbar vertebral bone mass in mature osteopenic rats: bone histomorphometry study. J Orthop Sci 3(5):257–263PubMedCrossRef
5.
go back to reference Ferguson VL, Greenberg AR, Bateman TA, Ayers RA, Simske SJ (1999) The effects of age and dietary restriction without nutritional supplementation on whole bone structural properties in C57BL/6J mice. Biomed Sci Instrum 35:85–91PubMed Ferguson VL, Greenberg AR, Bateman TA, Ayers RA, Simske SJ (1999) The effects of age and dietary restriction without nutritional supplementation on whole bone structural properties in C57BL/6J mice. Biomed Sci Instrum 35:85–91PubMed
6.
go back to reference Manore MM, Kam LC, Loucks AB, International Association of Athletics Federations (2007) The female athlete triad: components, nutrition issues, and health consequences. J Sports Sci 25:S61–S71PubMedCrossRef Manore MM, Kam LC, Loucks AB, International Association of Athletics Federations (2007) The female athlete triad: components, nutrition issues, and health consequences. J Sports Sci 25:S61–S71PubMedCrossRef
7.
go back to reference Nattiv A, Loucks AB, Manore MM, Sanborn CF, Sundgot-Borgen J, Warren MP, American College of Sports Medicine (2007) American college of sports medicine position stand: the female athlete triad. Med Sci Sports Exerc 39(10):1867–1882PubMedCrossRef Nattiv A, Loucks AB, Manore MM, Sanborn CF, Sundgot-Borgen J, Warren MP, American College of Sports Medicine (2007) American college of sports medicine position stand: the female athlete triad. Med Sci Sports Exerc 39(10):1867–1882PubMedCrossRef
8.
go back to reference Loucks AB (2004) Energy balance and body composition in sports and exercise. J Sports Sci 22(1):1–14PubMedCrossRef Loucks AB (2004) Energy balance and body composition in sports and exercise. J Sports Sci 22(1):1–14PubMedCrossRef
9.
go back to reference Yeager KK, Agostini R, Nattiv A, Drinkwater B (1993) The female athlete triad: disordered eating, amenorrhea, osteoporosis. Med Sci Sports Exerc 25(7):775–777PubMedCrossRef Yeager KK, Agostini R, Nattiv A, Drinkwater B (1993) The female athlete triad: disordered eating, amenorrhea, osteoporosis. Med Sci Sports Exerc 25(7):775–777PubMedCrossRef
10.
go back to reference Devlin MJ, Cloutier AM, Thomas NA, Panus DA, Lotinun S, Pinz I et al (2010) Caloric restriction leads to high marrow adiposity and low bone mass in growing mice. J Bone Miner Res 25(9):2078–2088PubMedCrossRef Devlin MJ, Cloutier AM, Thomas NA, Panus DA, Lotinun S, Pinz I et al (2010) Caloric restriction leads to high marrow adiposity and low bone mass in growing mice. J Bone Miner Res 25(9):2078–2088PubMedCrossRef
11.
go back to reference Talbott SM, Cifuentes M, Dunn MG, Shapses SA (2001) Energy restriction reduces bone density and biomechanical properties in aged female rats. J Nutr 131(9):2382–2387PubMed Talbott SM, Cifuentes M, Dunn MG, Shapses SA (2001) Energy restriction reduces bone density and biomechanical properties in aged female rats. J Nutr 131(9):2382–2387PubMed
13.
go back to reference Dimarco NM, Dart L, Sanborn CB (2007) Modified activity–stress paradigm in an animal model of the female athlete triad. J Appl Physiol 103(5):1469–1478PubMedCrossRef Dimarco NM, Dart L, Sanborn CB (2007) Modified activity–stress paradigm in an animal model of the female athlete triad. J Appl Physiol 103(5):1469–1478PubMedCrossRef
14.
go back to reference Loucks AB (2007) New animal model opens opportunities for research on the female athlete triad. J Appl Physiol 103(5):1467–1468PubMedCrossRef Loucks AB (2007) New animal model opens opportunities for research on the female athlete triad. J Appl Physiol 103(5):1467–1468PubMedCrossRef
15.
go back to reference Swift SN, Baek K, Swift JM, Bloomfield SA (2012) Restriction of dietary energy intake has a greater impact on bone integrity than does restriction of calcium in exercising female rats. J Nutr 142(6):1038–1045PubMedCrossRef Swift SN, Baek K, Swift JM, Bloomfield SA (2012) Restriction of dietary energy intake has a greater impact on bone integrity than does restriction of calcium in exercising female rats. J Nutr 142(6):1038–1045PubMedCrossRef
16.
go back to reference Trüssel A, Müller R, Webster D (2012) Toward mechanical systems biology in bone. Ann Biomed Eng 40(11):2475–2487PubMedCrossRef Trüssel A, Müller R, Webster D (2012) Toward mechanical systems biology in bone. Ann Biomed Eng 40(11):2475–2487PubMedCrossRef
17.
go back to reference Joo YI, Sone T, Fukunaga M, Lim SG, Onodera S (2003) Effects of endurance exercise on three-dimensional trabecular bone microarchitecture in young growing rats. Bone 33(4):485–493PubMedCrossRef Joo YI, Sone T, Fukunaga M, Lim SG, Onodera S (2003) Effects of endurance exercise on three-dimensional trabecular bone microarchitecture in young growing rats. Bone 33(4):485–493PubMedCrossRef
18.
go back to reference Chen MM, Yeh JK, Aloia JF, Tierney JM, Sprintz S (1994) Effect of treadmill exercise on tibial cortical bone in aged female rats: a histomorphometry and dual energy X-ray absorptiometry study. Bone 15(3):313–319PubMedCrossRef Chen MM, Yeh JK, Aloia JF, Tierney JM, Sprintz S (1994) Effect of treadmill exercise on tibial cortical bone in aged female rats: a histomorphometry and dual energy X-ray absorptiometry study. Bone 15(3):313–319PubMedCrossRef
19.
go back to reference Xie L, Jacobson JM, Choi ES, Busa B, Donahue LR, Miller LM et al (2006) Low-level mechanical vibrations can influence bone resorption and bone formation in the growing skeleton. Bone 39(5):1059–1066PubMedCrossRef Xie L, Jacobson JM, Choi ES, Busa B, Donahue LR, Miller LM et al (2006) Low-level mechanical vibrations can influence bone resorption and bone formation in the growing skeleton. Bone 39(5):1059–1066PubMedCrossRef
20.
go back to reference Bennell KL, Crossley K (1996) Musculoskeletal injuries in track and field: incidence, distribution and risk factors. Aust J Sci Med Sport 28(3):69–75PubMed Bennell KL, Crossley K (1996) Musculoskeletal injuries in track and field: incidence, distribution and risk factors. Aust J Sci Med Sport 28(3):69–75PubMed
21.
go back to reference Hame SL, LaFemina JM, McAllister DR, Schaadt GW, Dorey FJ (2004) Fractures in the collegiate athlete. Am J Sports Med 32(2):446–451PubMedCrossRef Hame SL, LaFemina JM, McAllister DR, Schaadt GW, Dorey FJ (2004) Fractures in the collegiate athlete. Am J Sports Med 32(2):446–451PubMedCrossRef
22.
go back to reference Roemmich JN, Sinning WE (1997) Weight loss and wrestling training: effects on growth-related hormones. J Appl Physiol 82(6):1760–1764PubMed Roemmich JN, Sinning WE (1997) Weight loss and wrestling training: effects on growth-related hormones. J Appl Physiol 82(6):1760–1764PubMed
23.
go back to reference De Souza MJ, Arce JC, Pescatello LS, Scherzer HS, Luciano AA (1994) Gonadal hormones and semen quality in male runners: a volume threshold effect of endurance training. Int J Sports Med 15(7):383–391PubMedCrossRef De Souza MJ, Arce JC, Pescatello LS, Scherzer HS, Luciano AA (1994) Gonadal hormones and semen quality in male runners: a volume threshold effect of endurance training. Int J Sports Med 15(7):383–391PubMedCrossRef
24.
go back to reference Burge MR, Lanzi RA, Skarda ST, Eaton RP (1997) Idiopathic hypogonadotropic hypogonadism in a male runner is reversed by clomiphene citra. Fertil Steril 67(4):783–785PubMedCrossRef Burge MR, Lanzi RA, Skarda ST, Eaton RP (1997) Idiopathic hypogonadotropic hypogonadism in a male runner is reversed by clomiphene citra. Fertil Steril 67(4):783–785PubMedCrossRef
25.
go back to reference Reeves PG, Nielsen FH, Fahey GCJ (1993) AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr 123(11):1939–1951PubMed Reeves PG, Nielsen FH, Fahey GCJ (1993) AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr 123(11):1939–1951PubMed
26.
go back to reference Holloszy JO (1992) Exercise and food restriction in rats. J Nutr 122(3 Suppl):774–777PubMed Holloszy JO (1992) Exercise and food restriction in rats. J Nutr 122(3 Suppl):774–777PubMed
27.
go back to reference Omi N, Ezawa I (1995) The effect of ovariectomy on bone metabolism in rats. Bone 17:163S–168SPubMed Omi N, Ezawa I (1995) The effect of ovariectomy on bone metabolism in rats. Bone 17:163S–168SPubMed
28.
go back to reference Harada S, Tominari T, Matsumoto C, Hirata M, Takita M, Inada M et al (2011) Nobiletin, a polymethoxy flavonoid, suppresses bone resorption by inhibiting NFκB-dependent prostaglandin E synthesis in osteoblasts and prevents bone loss due to estrogen deficiency. J Pharmacol Sci 115(1):89–93PubMedCrossRef Harada S, Tominari T, Matsumoto C, Hirata M, Takita M, Inada M et al (2011) Nobiletin, a polymethoxy flavonoid, suppresses bone resorption by inhibiting NFκB-dependent prostaglandin E synthesis in osteoblasts and prevents bone loss due to estrogen deficiency. J Pharmacol Sci 115(1):89–93PubMedCrossRef
29.
go back to reference Iwasaki Y, Kazama JJ, Yamato H, Fukagawa M (2011) Changes in chemical composition of cortical bone associated with bone fragility in rat model with chronic kidney disease. Bone 48(6):1260–1267PubMedCrossRef Iwasaki Y, Kazama JJ, Yamato H, Fukagawa M (2011) Changes in chemical composition of cortical bone associated with bone fragility in rat model with chronic kidney disease. Bone 48(6):1260–1267PubMedCrossRef
31.
go back to reference Tatsumi S, Ito M, Asaba Y, Tsutsumi K, Ikeda K (2008) Life-long caloric restriction reveals biphasic and dimorphic effects on bone metabolism in rodents. Endocrinology 149(2):634–641PubMedCrossRef Tatsumi S, Ito M, Asaba Y, Tsutsumi K, Ikeda K (2008) Life-long caloric restriction reveals biphasic and dimorphic effects on bone metabolism in rodents. Endocrinology 149(2):634–641PubMedCrossRef
32.
go back to reference Dimarco NM, Dart L, Sanborn CB (2007) Modified activity–stress paradigm in an animal model of the female athlete triad. J Appl Physiol 103(5):1469–1478PubMedCrossRef Dimarco NM, Dart L, Sanborn CB (2007) Modified activity–stress paradigm in an animal model of the female athlete triad. J Appl Physiol 103(5):1469–1478PubMedCrossRef
33.
go back to reference Westerbeek ZW, Hepple RT, Zernicke RF (2008) Effects of aging and caloric restriction on bone structure and mechanical properties. J Gerontol A Biol Sci Med Sci 63(11):1131–1136PubMedCrossRef Westerbeek ZW, Hepple RT, Zernicke RF (2008) Effects of aging and caloric restriction on bone structure and mechanical properties. J Gerontol A Biol Sci Med Sci 63(11):1131–1136PubMedCrossRef
34.
go back to reference Lambert J, Lamothe JM, Zernicke RF, Auer RN, Reimer RA (2005) Dietary restriction does not adversely affect bone geometry and mechanics in rapidly growing male Wistar rats. Pediatr Res 57(2):227–231PubMedCrossRef Lambert J, Lamothe JM, Zernicke RF, Auer RN, Reimer RA (2005) Dietary restriction does not adversely affect bone geometry and mechanics in rapidly growing male Wistar rats. Pediatr Res 57(2):227–231PubMedCrossRef
35.
go back to reference Mosley JR, March BM, Lynch J, Lanyon LE (1997) Strain magnitude related changes in whole bone architecture in growing rats. Bone 20(3):191–198PubMedCrossRef Mosley JR, March BM, Lynch J, Lanyon LE (1997) Strain magnitude related changes in whole bone architecture in growing rats. Bone 20(3):191–198PubMedCrossRef
36.
go back to reference Hsieh YF, Robling AG, Ambrosius WT, Burr DB, Turner CH (2001) Mechanical loading of diaphyseal bone in vivo: the strain threshold for an osteogenic response varies with location. J Bone Miner Res 16(12):2291–2297PubMedCrossRef Hsieh YF, Robling AG, Ambrosius WT, Burr DB, Turner CH (2001) Mechanical loading of diaphyseal bone in vivo: the strain threshold for an osteogenic response varies with location. J Bone Miner Res 16(12):2291–2297PubMedCrossRef
37.
go back to reference Martin B, Golden E, Carlson OD, Egan JM, Mattson MP, Maudsley S (2008) Caloric restriction: impact upon pituitary function and reproduction. Ageing Res Rev 7(3):209–224PubMedCrossRef Martin B, Golden E, Carlson OD, Egan JM, Mattson MP, Maudsley S (2008) Caloric restriction: impact upon pituitary function and reproduction. Ageing Res Rev 7(3):209–224PubMedCrossRef
38.
go back to reference Kinoshita M, Moriyama R, Tsukamura H, Maeda KI (2003) A rat model for the energetic regulation of gonadotropin secretion: role of the glucose-sensing mechanism in the brain. Domest Anim Endocrinol 25(1):109–120PubMedCrossRef Kinoshita M, Moriyama R, Tsukamura H, Maeda KI (2003) A rat model for the energetic regulation of gonadotropin secretion: role of the glucose-sensing mechanism in the brain. Domest Anim Endocrinol 25(1):109–120PubMedCrossRef
39.
go back to reference Martin B, Pearson M, Kebejian L, Golden E, Keselman A, Bender M et al (2007) Sex-dependent metabolic, neuroendocrine, and cognitive responses to dietary energy restriction and excess. Endocrinology 148(9):4318–4333PubMedCrossRef Martin B, Pearson M, Kebejian L, Golden E, Keselman A, Bender M et al (2007) Sex-dependent metabolic, neuroendocrine, and cognitive responses to dietary energy restriction and excess. Endocrinology 148(9):4318–4333PubMedCrossRef
40.
go back to reference Brecchia G, Bonanno A, Galeati G, Federici C, Maranesi M, Gobbetti A et al (2006) Hormonal and metabolic adaptation to fasting: effects on the hypothalamic–pituitary–ovarian axis and reproductive performance of rabbit does. Domest Anim Endocrinol 31(2):105–122PubMedCrossRef Brecchia G, Bonanno A, Galeati G, Federici C, Maranesi M, Gobbetti A et al (2006) Hormonal and metabolic adaptation to fasting: effects on the hypothalamic–pituitary–ovarian axis and reproductive performance of rabbit does. Domest Anim Endocrinol 31(2):105–122PubMedCrossRef
41.
go back to reference Wayne NL, Wade GN, Rissman EF (1991) Effects of food restriction and social cues on sexual maturation and growth in male musk shrews (Suncus murinus). J Reprod Fertil 91(1):385–392PubMedCrossRef Wayne NL, Wade GN, Rissman EF (1991) Effects of food restriction and social cues on sexual maturation and growth in male musk shrews (Suncus murinus). J Reprod Fertil 91(1):385–392PubMedCrossRef
42.
go back to reference Katch VL, Martin R, Martin J (1979) Effects of exercise intensity on food consumption in the male rat. Am J Clin Nutr 32(7):1401–1407PubMed Katch VL, Martin R, Martin J (1979) Effects of exercise intensity on food consumption in the male rat. Am J Clin Nutr 32(7):1401–1407PubMed
43.
go back to reference Routtenberg A, Kuznesof AW (1967) Self-starvation of rats living in activity wheels on a restricted feeding schedule. J Comp Physiol Psychol 64(3):414–421PubMedCrossRef Routtenberg A, Kuznesof AW (1967) Self-starvation of rats living in activity wheels on a restricted feeding schedule. J Comp Physiol Psychol 64(3):414–421PubMedCrossRef
44.
go back to reference Lambert KG (1993) The activity–stress paradigm: possible mechanisms and applications. J Gen Psychol 120(1):21–32PubMedCrossRef Lambert KG (1993) The activity–stress paradigm: possible mechanisms and applications. J Gen Psychol 120(1):21–32PubMedCrossRef
Metadata
Title
Influence of Food Restriction Combined with Voluntary Running on Bone Morphology and Strength in Male Rats
Authors
Satoshi Hattori
Jong-Hoon Park
Umon Agata
Takayuki Akimoto
Masaya Oda
Michito Higano
Yuki Aikawa
Yoshiharu Nabekura
Hideyuki Yamato
Ikuko Ezawa
Naomi Omi
Publication date
01-12-2013
Publisher
Springer US
Published in
Calcified Tissue International / Issue 6/2013
Print ISSN: 0171-967X
Electronic ISSN: 1432-0827
DOI
https://doi.org/10.1007/s00223-013-9787-6

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