Adequate Energy Intake Prevents Low Bone Mass Under Exercise and Low Intake of Nutrients in Young Female Rats
American Journal of Sports Science
Volume 7, Issue 3, September 2019, Pages: 127-135
Received: Aug. 14, 2019; Accepted: Sep. 9, 2019; Published: Sep. 19, 2019
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Yuki Aikawa, Comprehensive Human Sciences, University of Tsukuba, Tsukuba, Japan; Department of Science of Living, Tsu City College, Tsu, Japan
Yuya Kakutani, Comprehensive Human Sciences, University of Tsukuba, Tsukuba, Japan; Faculty of Health and Nutrition, Osaka Shoin Women’s University, Higashi-Osaka, Japan
Umon Agata, Comprehensive Human Sciences, University of Tsukuba, Tsukuba, Japan; Department of Pharmaceutical and Medical Business Sciences, Nihon Pharmaceutical University, Ina-machi, Japan
Satoshi Hattori, Comprehensive Human Sciences, University of Tsukuba, Tsukuba, Japan; Faculty of Sport Science, Waseda University, Tokorozawa, Japan
Hitomi Ogata, Graduate School of Integrated Arts and Sciences, Hiroshima University, Higashi-Hiroshima, Japan
Ken Kiyono, Graduate School of Engineering Science, Osaka University, Toyonaka, Japan
Ikuko Ezawa, Department of food and nutrition, Japan Women’s University, Bunkyo-ku, Japan
Naomi Omi, Faculty of Health and Sport Sciences, University of Tsukuba, Tsukuba, Japan
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We examined the effects of adequate energy intake on bone strength and bone mass under exercise and low nutrient intake using a rat model of the female athlete triad (FAT). Seven-week-old female rats were divided into four groups: sedentary and ad libitum feeding group (SED), exercise and ad libitum feeding group (EX), exercise and 30% food restriction group (EX-FR), and exercise, 30% food restriction and adequate energy intake group (EX-FR + Ene). Excise groups were performed a voluntary running. The EX-FR + Ene group was fed glucose ad-libitum to adequate energy intake. The experiment lasted for 12 weeks. The energy availability, internal organ weight, bone size, bone strength, bone mass, and calcium absorption in the EX-FR group were significantly lower than those in the EX group. There were no significant differences in these parameters except bone strength in between the EX and EX-FR + Ene groups. The breaking energy in the EX-FR + Ene group was significantly lower than those in the EX group. Our results provide evidence that adequate energy intake is important for optimal bone growth in young female athletes.
Female Athlete Triad, Food Restriction, Energy Supplementation, Bone Strength, Running Exercise
To cite this article
Yuki Aikawa, Yuya Kakutani, Umon Agata, Satoshi Hattori, Hitomi Ogata, Ken Kiyono, Ikuko Ezawa, Naomi Omi, Adequate Energy Intake Prevents Low Bone Mass Under Exercise and Low Intake of Nutrients in Young Female Rats, American Journal of Sports Science. Vol. 7, No. 3, 2019, pp. 127-135. doi: 10.11648/j.ajss.20190703.17
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Nattiv A, Loucks AB, Manore MM, Sanborn CF, Sundgot-Borgen J, Warren MP (2007) American College of Sports Medicine. American College of Sports Medicine position stand. The Female Athlete Triad. Med Sci Sports Exerc 39 (10): 1867-1882.
Lauder TD, Dixit S, Pezzin LE, Williams MV, Campbell CS, Davis GD (2000) The relation between stress fractures and bone mineral density: evidence from active-duty Army women. Arch Phys Med Rehabil 81 (1): 73-79.
Loucks AB, Kiens B, Wright HH (2011) Energy availability in athletes. J Sports Sci 29 Suppl 1: S7-S15.
Talbott SM, Cifuentes M, Dunn MG, Shapses SA (2001) Energy restriction r educes bone density and biomechanical properties in aged female rats. J Nutr 131 (9): 2382-2387.
Hawkins J, Cifuentes M, Pleshko NL, Ambia-Sobhan H, Shapses SA (2010) Energy Restriction Is Associated with Lower Bone Mineral Density of the Tibia and Femur in Lean but Not Obese Female Rats. J Nutr 140 (1): 31-37.
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): 1038-1045.
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): 1469-1478.
Aikawa Y, Agata U, Kakutani Y, Higano M, Hattori S, Ogata H, Ezawa I, Omi N (2015) The interaction of voluntary running exercise and food restriction induces low bone strength and low bone mineral density in young female rats. Calcif Tissue Int 97 (1): 90-99.
Aikawa Y, Agata U, Kakutani Y, Kato S, Noma Y, Ogata H, Ezawa I, Omi N (2016) The preventive effect of calcium supplementation on weak bones caused by the interaction of exercise and food restriction in young female rats during the period from acquiring bone mass to maintaining bone mass. Calcif Tissue Int 98 (1): 94-103.
Noda S, Sawaki M, Shiraishi K, Yamasaki K, Yamaguchi R (2002) Age-related changes of genital systems in the female Crj:CD (SD) IGS rats during sexual maturation. J Vet Med Sci 64 (4): 315-319.
Anantharaman-Barr HG, Decombaz J (1989) The effect of wheel running and the estrous cycle on energy expenditure in female rats. Physiol Behav 46 (2): 259-263.
Ezawa I, Okada R, Nozaki Y, Ogata, E (1979) Breaking-properties and ash contents of the femur of growing rat fed a low calcium diet. Nippon Eiyo Shokuryo Gakkaishi, J Jpn Soc Food Nutr 32 (5): 329-335.
Omi N, Morikawa N, Ezawa I (1994) The effect of voluntary exercise on bone mineral density and skeletal muscles in the rat model at ovariectomized and sham stages. Bone miner 24 (3): 211-222.
Omi N, Goseki M, Oida S, Sasaki S, Ezawa I (1994) The nutritional evaluation of globin on maintenance of bone metabolism in ovariectomized osteoporotic rats. J Nutr Sci Vitaminol 40 (5): 443-457.
Cashman KD (2007) Diet, nutrition, and bone health. J Nutr 137 (11 Suppl): 2507S-2512S.
Takeda S, Kobayashi Y, Park JH, Ezawa I, Omi N (2012) Effect of different intake levels of dietary protein and physical exercise on bone mineral density and bone strength in growing male rats. J Nutr Sci Vitaminol 58 (4): 240-246.
Stubbs RJ, Hughes DA, Johnstone AM, Whybrow S, Horgan GW, King N, Blundell J (2004) Rate and extent of compensatory changes in energy intake and expenditure in response to altered exercise and diet composition in humans. Am J Physiol Regul Integr Comp Physiol 286 (2): R350-R358.
Erben RG, Brunner KS, Breig B (2004) Long-term sensitivity of uterus and hypothalamus/pituitary axis to 17 beta-estradiol is higher than that of bone in rats. J Bone Miner 19 (11): 1827-1832.
Wang G (1923) The relation between “spontaneous” activity and oestrous cycle in the white rat. Comp Psychol Monogr 2: 1-27.
Ammann P, Rizzoli R (2003) Bone strength and its determinants. Osteoporos Int 14 (Suppl 3): S13-S18.
Omi N, Nakamura T, Ezawa I (1998) Modulation of bone mass and turnover in growing rats by voluntary weight-bearing exercise and glucose supplementation. J Nutr Sci Vitaminol 44 (3): 409-421.
Ackerman KE, Cano Sokoloff N, DE Nardo Maffazioli G, Clarke HM, Lee H, Misra M (2015) Fractures in Relation to Menstrual Status and Bone Parameters in Young Athletes. Med Sci Sports Exerc. 47 (8): 1577-86.
Pando R, Masarwi M, Shtaif B, Idelevich A, Monsonego-Ornan E, Shahar R, Phillip M, Gat-Yablonski G (2014) Bone quality is affected by food restriction and by nutrition-induced catch-up growth. J Endocrinol 223 (3): 227-39.
Cifuentes M, Morano AB, Chowdhury HA, Shapses SA (2002) Energy restriction reduces fractional calcium absorption in mature obese and lean rats. J Nutr 132 (9): 2660-2666.
Shah BG, Trick KD, Belonje B (1990) Effects of dietary calcium on the metabolism of trace elements in male and female rats. J Nutr Biochem 1 (11): 585-591.
Cashman KD, Flynn A (1996) Effect of dietary calcium intake and meal calcium content on calcium absorption in the rat. Br J Nutr 76 (3): 463-470.
Ihle R, Loucks AB (2004) Dose-response relationships between energy availability and bone turnover in young exercising women. J Bone Miner Res 9 (8): 1231-1240.
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