Effects of muscular strength training and growth hormone (GH) supplementation on femoral bone tissue: analysis by Raman spectroscopy, dual-energy X-ray absorptiometry, and mechanical resistance Original Article First Online: 15 June 2019 Abstract
The aim of the present study was to verify the effects of muscular strength training and growth hormone (GH) supplementation on femoral bone tissue by Raman spectroscopy (Raman), dual-energy X-ray absorptiometry (DXA), and mechanical resistance (F-max) analysis. A total of 40 male Wistar animals, 60 days old, were used. The animals were distributed into four groups: control (C), control with GH (GHC), muscular strength training (T), and muscular strength training with GH (GHT). Blood samples were collected for the quantification of creatine kinase (CK-MB) and the femurs were removed for analysis by Raman, DXA, and F-max. A more pronounced increase in the bone mineral components was verified in the T group, for all the variables obtained by the Raman (calcium, phosphate, amide, and collagen). In addition, for animals submitted to GH supplementation, there was a reduction in the variable bone mineral density (BMD) obtained by the DXA (
p < 0.05). Finally, the animals that received GH supplementation presented a higher F-max, but without statistical significance ( p > 0.05). It was concluded that animals that received GH supplementation demonstrated a decrease in BMD. In addition, T alone was able to promote increased calcium, phosphate, amide, and collagen compounds in bone tissue. Keywords Physical training Growth hormone Bone tissue Muscular strength Anabolics Notes Acknowledgments
The authors are grateful to the Brazilian Agency of Resources for Higher Education Personnel (CAPES) for supporting the development of this study.
This study was funded by Brazilian Agency of Resources for Higher Education Personnel (CAPES).
Compliance with ethical standards Conflict of interest
The authors declare that they have no conflict of interest.
All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted. All procedures were approved by the ethics committee for animal use from University of Western São Paulo - UNOESTE (SP, Brazil; protocol no. 2626). This article does not contain any studies with human participants performed by any of the authors.
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Castoldi RC, Teixeira GR, de Malheiro OCM et al (2015) Effects of 14 weeks resistance training on muscle tissue in wistar rats. Int J Morphol 33:446–451.
https://doi.org/10.4067/S0717-95022015000200007 CrossRef Google Scholar
Lui JC, Colbert M, Cheung CSF et al (2019) Cartilage-targeted IGF-1 treatment to promote longitudinal bone growth. Mol Ther 38:6–12.
https://doi.org/10.1016/j.ymthe.2019.01.017 Google Scholar
Qi Z, Liu W, Lu J (2016) The mechanisms underlying the beneficial effects of exercise on bone remodeling: roles of bone-derived cytokines and microRNAs. Prog Biophys Mol Biol 122:131–139.
https://doi.org/10.1016/j.pbiomolbio.2016.05.010 CrossRef Google Scholar
Kjær M, Magnusson P, Langberg H (2006) Extracellular matrix adaptation of tendon and skeletal muscle to exercise tendon and collagen synthesis. J Anat 2:1–5.
https://doi.org/10.1111/j.1469-7580.2006.00549.x Google Scholar
Patrocínio-Silva TL, de SAMF, Goulart RL et al (2016) Low-level laser therapy associated to a resistance training protocol on bone tissue in diabetic rats. Arch Endocrinol Metab 60:457–464.
https://doi.org/10.1590/2359-3997000000190 CrossRef Google Scholar
Hong AR, Kim SW (2018) Effects of resistance exercise on bone health. Endocrinol Metab 33:435–444.
https://doi.org/10.3803/EnM.2018.33.4.435 CrossRef Google Scholar
Watson SL, Weeks BK, Weis LJ et al (2018) High-intensity resistance and impact training improves bone mineral density and physical function in postmenopausal women with osteopenia and osteoporosis: the LIFTMOR randomized controlled trial. J Bone Miner Res 33:211–220.
https://doi.org/10.1002/jbmr.3284 CrossRef Google Scholar
Dror A, Virk K, Lee K et al (2018) Resistance training threshold for elevating bone mineral density in growing female rats. Int J Sports Med 39:382–389.
https://doi.org/10.1055/s-0043-125447 CrossRef Google Scholar
Ozaki GAT, Koike TE, Castoldi RC et al (2014) Physical exercise remobilization effects on bone density in adults and elderly rats. Motricidade 10:71–78.
https://doi.org/10.6063/motricidade.10(3).2725 CrossRef Google Scholar
Peres-Ueno MJ, Stringhetta-Garcia CT, Castoldi RC et al (2017) Model of hindlimb unloading in adult female rats: characterizing bone physicochemical, microstructural, and biomechanical properties. PLoS One 12:1–15.
https://doi.org/10.1371/journal.pone.0189121 CrossRef Google Scholar
Gupta V (2011) Adult growth hormone deficiency. Indian J Endocrinol Metab 15:197–202.
https://doi.org/10.4103/2230-8210.84865 CrossRef Google Scholar
Sundström K, Cedervall T, Ohlsson C et al (2014) Combined treatment with GH and IGF-I: additive effect on cortical bone mass but not on linear bone growth in female rats. Endocrinology 155:4798–4807.
https://doi.org/10.1210/en.2014-1160 CrossRef Google Scholar
Al Herbish AS, Almutair A, Bin Abbas B et al (2016) Diagnosis and management of growth disorders in Gulf Cooperation Council (GCC) countries: current procedures and key recommendations for best practice. Int J Pediatr Adolesc Med 3:91–102.
https://doi.org/10.1016/j.ijpam.2016.07.002 CrossRef Google Scholar
Díez JJ, Sangiao-Alvarellos S, Cordido F (2018) Treatment with growth hormone for adults with growth hormone deficiency syndrome: benefits and risks. Int J Mol Sci 19:1–19.
https://doi.org/10.3390/ijms19030893 CrossRef Google Scholar
McGrath RP, Ottenbacher KJ, Vincent BM et al (2017) Muscle weakness and functional limitations in an ethnically diverse sample of older adults. Ethn Health 0:1–12.
https://doi.org/10.1080/13557858.2017.1418301 CrossRef Google Scholar
Loche S, Carta L, Ibba A, Guzzetti C (2014) Growth hormone treatment in non-growth hormone-deficient children. Ann Pediatr Endocrinol Metab 19(1).
Crowe BJ, Rekers-Mombarg LTM, Robling K et al (2006) Effect of growth hormone dose on bone maturation and puberty in children with idiopathic short stature. J Clin Endocrinol Metab 91:169–175.
https://doi.org/10.1210/jc.2005-0891 CrossRef Google Scholar
Siebert DM, Rao AL (2018) The use and abuse of human growth hormone in sports. Sport Heal A Multidiscip Approach 10:419–426.
https://doi.org/10.1177/1941738118782688 CrossRef Google Scholar
Barroso O, Mazzoni I, Rabin O (2008) Hormone abuse in sports: the antidoping perspective. Asian J Androl 10:391–402.
https://doi.org/10.1111/j.1745-7262.2008.00402.x CrossRef Google Scholar
Erotokritou-Mulligan I, Eryl Bassett E, Cowan DA et al (2010) The use of growth hormone (GH)-dependent markers in the detection of GH abuse in sport: physiological intra-individual variation of IGF-I, type 3 pro-collagen (P-III-P) and the GH-2000 detection score. Clin Endocrinol 72:520–526.
https://doi.org/10.1111/j.1365-2265.2009.03668.x CrossRef Google Scholar
Hoffman JR, Im J, Rundell KW et al (2003) Effect of muscle oxygenation during resistance exercise on anabolic hormone response. Med Sci Sports Exerc 35:1929–1934.
https://doi.org/10.1249/01.MSS.0000093613.30362.DF CrossRef Google Scholar
Renno ACM, Silveira Gomes AR, Nascimento RB et al (2007) Effects of a progressive loading exercise program on the bone and skeletal muscle properties of female osteopenic rats. Exp Gerontol 42:517–522.
https://doi.org/10.1016/j.exger.2006.11.014 CrossRef Google Scholar
Movasaghi Z, Rehman S, Rehman IU (2007) Raman spectroscopy of biological tissues. Appl Spectrosc Rev 42:493–541.
https://doi.org/10.1080/05704920701551530 CrossRef Google Scholar
Koike TE, Watanabe AY, Kodama FY et al (2018) Physical exercise after immobilization of skeletal muscle of adult and aged rats. Rev Bras Med do Esporte 24:60–63.
https://doi.org/10.1590/1517-869220182401172423 CrossRef Google Scholar
Aguiar AF, Agati LB, Müller SS et al (2010) Effects of high-impact exercise training on bone mechanical proprieties – an experimental study in female Wistar rats. Acta Ortopédica Bras 18:245–249.
https://doi.org/10.1590/S1413-78522010000500002 CrossRef Google Scholar
Manchado FDB, Gobatto CA, Contarteze RVL et al (2006) Máxima fase estável de lactato é ergômetro-dependente em modelo experimental utilizando ratos. Rev Bras Med do Esporte 12:259–262.
https://doi.org/10.1590/S1517-86922006000500007 CrossRef Google Scholar
Longui CA (2008) GH treatment in patients with idiopathic short stature. Arq Bras Endocrinol Metabol 52:750–756.
https://doi.org/10.1590/S0004-27302008000500006 CrossRef Google Scholar
Tinggaard J, Jensen RB, Sundberg K et al (2014) Ovarian morphology and function during growth hormone therapy of short girls born small for gestational age. Fertil Steril 102:1733–1741.
https://doi.org/10.1016/j.fertnstert.2014.09.014 CrossRef Google Scholar
Kaminsky P, Walker PM, Deibener J et al (2012) Growth hormone potentiates thyroid hormone effects on post-exercise phosphocreatine recovery in skeletal muscle. Growth Hormon IGF Res 22:240–244.
https://doi.org/10.1016/j.ghir.2012.08.001 CrossRef Google Scholar
De Mello Malheiro OC, Giacomini CT, Justulin LA et al (2009) Calcaneal tendon regions exhibit different MMP-2 activation after vertical jumping and treadmill running. Anat Rec (Hoboken) 292:1656–1662.
https://doi.org/10.1002/ar.20953 CrossRef Google Scholar
Castoldi RC, Camargo RCT, Magalhães AJB et al (2013) Concurrent training effect on muscle fibers in Wistar rats. Motriz Rev Educ Fis 19:171–723.
https://doi.org/10.1590/S1980-65742013000400008 CrossRef Google Scholar
Kendall C, Stone N, Shepherd N et al (2003) Raman spectroscopy, a potential tool for the objective identification and classification of neoplasia in Barrett’s oesophagus. J Pathol 200:602–609.
https://doi.org/10.1002/path.1376 CrossRef Google Scholar
Souza F de B, Pacheco MTT, VilaVerde AB et al (2003) Avaliação do ácido láctico intramuscular através da espectroscopia Raman: novas perspectivas em medicina do esporte. Rev Bras Med do Esporte 9:388–395.
https://doi.org/10.1590/S1517-86922003000600004 CrossRef Google Scholar
McManus LL, Bonnier F, Burke G a., et al (2012) Assessment of an osteoblast-like cell line as a model for human primary osteoblasts using Raman spectroscopy. Analyst 137:1559–1569. doi:
Cheng W-T, Liu M-T, Liu H-N, Lin S-Y (2005) Micro-Raman spectroscopy used to identify and grade human skin pilomatrixoma. Microsc Res Tech 68:75–79.
https://doi.org/10.1002/jemt.20229 CrossRef Google Scholar
Gazi E, Dwyer J, Gardner P et al (2003) Applications of Fourier transform infrared microspectroscopy in studies of benign prostate and prostate cancer. A pilot study. J Pathol 201:99–108.
https://doi.org/10.1002/path.1421 CrossRef Google Scholar
Malini R, Venkatakrishna K, Kurien J et al (2006) Discrimination of normal, inflammatory, premalignant, and malignant oral tissue: a Raman spectroscopy study. Biopolymers 81:179–193.
https://doi.org/10.1002/bip.20398 CrossRef Google Scholar
Shafer-Peltier KE, Haka AS, Fitzmaurice M et al (2002) Raman microspectroscopic model of human breast tissue: implications for breast cancer diagnosis in vivo. J Raman Spectrosc 33:552–563.
https://doi.org/10.1002/jrs.877 CrossRef Google Scholar
Castoldi RC, Louzada MJQ, de OBRSM et al (2017) Effects of aerobic, anaerobic, and concurrent training on bone mineral density of rats. Mot rev educ fis 23:71–75.
https://doi.org/10.1590/s1980-6574201700010011 CrossRef Google Scholar
Val FF de A, Okubo R, Falcai MJ et al (2013) Effects of high-impact exercise training on bone mechanical proprieties - an experimental study in female Wistar rats. Rev Bras Med do Esporte 19:252–255.
https://doi.org/10.1590/S1517-86922013000400005 CrossRef Google Scholar
Mandair GS, Morris MD (2015) Contributions of Raman spectroscopy to the understanding of bone strength. Bonekey Rep 4:1–8.
https://doi.org/10.1038/bonekey.2014.115 CrossRef Google Scholar
Torres-del-Pliego E, Vilaplana L, Güerri-Fernández R, Diez-Pérez A (2013) Measuring bone quality. Curr Rheumatol Rep 15:373–378.
https://doi.org/10.1007/s11926-013-0373-8 CrossRef Google Scholar
Burket J, Gourion-Arsiquaud S, Havill LM et al (2011) Microstructure and nanomechanical properties in osteons relate to tissue and animal age. J Biomech 44:277–284.
https://doi.org/10.1016/j.jbiomech.2010.10.018 CrossRef Google Scholar
da Silva FF, de Souza RA, Pacheco MTT et al (2011) Effects of different swimming exercise intensities on bone tissue composition in mice: a Raman spectroscopy study. Photomed Laser Surg 29:217–225.
https://doi.org/10.1089/pho.2010.2784 CrossRef Google Scholar
Inoue-Lima TH, Vasques GA, Scalco RC et al (2019) IGF-1 assessed by pubertal status has the best positive predictive power for GH deficiency diagnosis in peripubertal children. J Pediatr Endocrinol Metab 32:173–179.
https://doi.org/10.1515/jpem-2018-0435 CrossRef Google Scholar
Davies RD, Parent EC, Steinback CD, Kennedy MD (2018) The effect of different training loads on the lung health of competitive youth swimmers. Int J Exerc Sci 11:999–1018
Cruzat VF, Donato Júnior J, Tirapegui J, Schneider CD (2008) Growth hormone and physical exercise: current considerations. Brazilian J Pharm Sci 44:549–562.
https://doi.org/10.1590/S1516-93322008000400003 Google Scholar
Godfrey RJ, Madgwick Z, Whyte GP (2003) The exercise-induced growth hormone response in athletes. Sport Med 33:599–613.
https://doi.org/10.2165/00007256-200333080-00005 CrossRef Google Scholar
Rozario KS, Lloyd C RF (2015) GH and IGF-1 physiology in childhood. editors. Endotext [Internet]., South Dartmouth (MA)
de Rezende Gomes M, Santana de Oliveira Pires I, Alves de Castro I, Tirapegui J (2004) Effect of moderate physical exercise on plasma and tissue levels of insulin-like growth factor–1 in adult rats. Nutr Res 24:555–564.
https://doi.org/10.1016/j.nutres.2004.04.003 CrossRef Google Scholar
Rawlings JS (2004) The JAK/STAT signaling pathway. J Cell Sci 117:1281–1283.
https://doi.org/10.1242/jcs.00963 CrossRef Google Scholar
Gent J, van den Eijnden M, van Kerkhof P, Strous GJ (2003) Dimerization and signal transduction of the growth hormone receptor. Mol Endocrinol 17:967–975.
https://doi.org/10.1210/me.2002-0261 CrossRef Google Scholar
Herrington J (2001) Signaling pathways activated by the growth hormone receptor. Trends Endocrinol Metab 12:252–257.
https://doi.org/10.1016/S1043-2760(01)00423-4 CrossRef Google Scholar
Gebel A, Lesinski M, Behm DG, Granacher U (2018) Effects and dose–response relationship of balance training on balance performance in youth: a systematic review and meta-analysis. Sport Med 48:2067–2089.
https://doi.org/10.1007/s40279-018-0926-0 CrossRef Google Scholar
Borde R, Hortobágyi T, Granacher U (2015) Dose–response relationships of resistance training in healthy old adults: a systematic review and meta-analysis. Sport Med 45:1693–1720.
https://doi.org/10.1007/s40279-015-0385-9 CrossRef Google Scholar
Kraemer WJ, Flanagan SD, Volek JS et al (2013) Resistance exercise induces region-specific adaptations in anterior pituitary gland structure and function in rats. J Appl Physiol 115:1641–1647.
https://doi.org/10.1152/japplphysiol.00687.2013 CrossRef Google Scholar
Menagh P, Turner R, Jump D et al (2009) Growth hormone regulates the balance between bone formation and bone marrow adiposity. J Bone Miner Res 25:757–768. 091012153414059-44.
https://doi.org/10.1359/jbmr.091015 Google Scholar
Leme JACA, Silveira RF, Gomes RJ et al (2009) Long-term physical training increases liver IGF-I in diabetic rats. Growth Hormon IGF Res 19:262–266.
https://doi.org/10.1016/j.ghir.2008.12.004 CrossRef Google Scholar
Hojan K, Milecki P, Leszczyński P (2013) The impact of aerobic exercises on bone mineral density in breast cancer women during endocrine therapy. Polish Orthop Traumatol 78:47–51
Castoldi RC, Louzada MJQ, De Oliveira BRSM et al (2017) Effects of aerobic, anaerobic, and concurrent training on bone mineral density of rats. Motriz Rev Educ Fis 23:71–75.
https://doi.org/10.1590/S1980-6574201700010011 CrossRef Google Scholar
Ehrnborg C, Rosén T (2008) Physiological and pharmacological basis for the ergogenic effects of growth hormone in elite sports. Asian J Androl 10:373–383.
https://doi.org/10.1111/j.1745-7262.2008.00403.x CrossRef Google Scholar
Ghiasi R, Mohammadi M, Ashrafi Helan J et al (2015) Influence of two various durations of resistance exercise on oxidative stress in the male rat’s hearts. J Cardiovasc Thorac Res 7:149–153.
https://doi.org/10.15171/jcvtr.2015.32 CrossRef Google Scholar Copyright information
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