Skip to main content
SpringerLink
Log in

Influence of high-fat diet on bone tissue: An experimental study in growing rats

  • Published:
The journal of nutrition, health & aging

Abstract

Background

The relationship between obesity and bone tissue remains contradictory, especially when the effect of high-fat diet is assessed in experimental models. The aim of this study was to evaluate the effects of high-fat diet on bone metabolism of growing rats.

Methods

Twenty weaned female Wistar rats were equally divided into two groups: SD (standard diet) and HFD (high-fat diet with 60 % of energy as fat). After five weeks of the two diets, the rats were euthanized, and the liver, blood and bones extracted. The liver was analysed for malondialdehyde (MDA) and reduced glutathione (GSH) concentrations. Blood was analysed by the ELISA method for osteoprotegerin (OPG) and tumour necrosis factor ligand superfamily member 11 (TNFSF11/RANKL). The bone tissue was analysed by dual-energy X-ray absorptiometry (DXA), mechanical tests, computed microtomography, histological quantitative analysis and scanning electron microscopy. The gene expressions of PPAR-γ Runx-2, RANKL and Cathepsin-K were also evaluated.

Results

HFD caused an increase in the MDA concentration, indicating oxidative stress. It also increased the expression of PPAR-γ, which is the gene that is related to adipocyte differentiation. There was an increase in BMD of the tibia of animals fed with the HFD, but other microstructural and mechanical properties were maintained unaltered. In addition, there were no changes in the gene expressions related to the differentiation of osteoblasts and osteoclasts, as well as no changes to the biochemical markers of bone formation and bone resorption.

Conclusion

Liver and gene parameters are changed in response to the HFD. However, although there was an increase in BMD, the microstructure and function of the bone did not change after a 5-week HFD.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6

Similar content being viewed by others

References

  1. Bloomfield HE, Koeller E, Greer N, MacDonald R, Kane R, Wilt TJ. Effects on Health Outcomes of a Mediterranean Diet With No Restriction on Fat Intake: A Systematic Review and Meta-analysis. Ann Intern Med 2016. doi:10.7326/M16-0361.

    Google Scholar 

  2. Kar S, Khandelwal B. Fast foods and physical inactivity are risk factors for obesity and hypertension among adolescent school children in east district of Sikkim, India. J Nat Sci Biol Med 2015;6(2):356–9. doi:10.4103/0976-9668.160004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Kafeshani O, Sarrafzadegan N, Nouri F, Mohammadifard N. Major dietary patterns in Iranian adolescents: Isfahan Healthy Heart Program, Iran. ARYA 2015;11:61–8.

    Google Scholar 

  4. Silva HG, Mendonça LM, Conceição FL, Zahar SEm Farias ML. Influence of obesity on bone density in postmenopausal women. Arq Bras Endocrinol Metabol 2007;51(6):943–9. doi:10.1590/S0004-27302007000600008.

    Article  PubMed  Google Scholar 

  5. Pinheiro MM, Schuch NJ, Genaro PS, Ciconelli RM, Ferraz MB, Martini LA. Nutrient intakes related to osteoporotic fractures in men and women—the Brazilian Osteoporosis Study (BRAZOS). Nutr J 2009;8(6):1–8. doi:10.1186/1475-2891-8-6.

    Google Scholar 

  6. Rendina-Ruedy E, Graef JL, Davis MR, Hembree KD, Gimble JM, Clarke SL, Lucas EA, Smith BJ. Strain differences in the attenuation of bone accrual in a young growing mouse model of insulin resistance. J Bone Miner Metab 2016;32(4):380–394. doi:10.1007/s00774-015-0685-z.

    Article  Google Scholar 

  7. Lim S, Joung H, Shin CS, Lee HK, Kim KS, Shin EK, Kim HY, Lim MK, Cho SI. Body composition changes with age have gender-specific impacts on bone mineral density. Bone 2004;35(3):792–8. doi:10.1016/j.bone.2004.05.016.

    Article  PubMed  Google Scholar 

  8. Lenchik L, Register TC, Hsu FC, Lohman K, Nicklas BJ, Freedman BI, Langefeld CD, Carr JJ, Bowden DW. Adiponectin as a novel determinant of bone mineral density and visceral fat. Bone 2003;33(4):646–51. doi:10.1016/S8756-3282(03)00237-0.

    Article  CAS  PubMed  Google Scholar 

  9. Paula FJAD, Rosen CJ. Obesity. Diabetes mellitus and last but not least, osteoporosis. Arq Bras Endocrinol Metab 2010;54(2):150–157. doi:10.1590/S0004-27302010000200010.

    Article  PubMed  Google Scholar 

  10. Tintut Y, Morony S, Demer LL. Hyperlipidemia promotes osteoclastc potential of bone marrow cells ex vivo. Arterioscler Thromb Vasc Biol 24:6-10. doi:10.1161/01. ATV.0000112023.62695.7f.

  11. Looker AC, Flegal KM, Melton LJ. Impact of increased overweight on the projected prevalence of osteoporosis in older women. Osteoporos Int 2007;18(3):307–13. doi:10.1007/s00198-006-0241-8.

    Article  CAS  PubMed  Google Scholar 

  12. Rosen CJ, Klibanski A. Bone, fat, and body composition: evolving concepts in the pathogenesis of osteoporosis. Am J Med 2009;122(5):409–14. doi:10.1016/j. amjmed.2008.11.027.

    Article  CAS  PubMed  Google Scholar 

  13. Bartelt A, Beil FT, Schinke T, Roeser K, Ruether W, Heeren J, Niemeier A. Apolipoprotein E-dependent inverse regulation of vertebral bone and adipose tissue mass in C57Bl/6 mice: modulation by diet-induced obesity. Bone 2010;47(4):736–45. doi:10.1016/j.bone.2010.07.002.

    Article  CAS  PubMed  Google Scholar 

  14. Zhao LJ, Liu YJ, Liu PY, Hamilton J, Recker RR, Deng HW. Relationship of obesity with osteoporosis. J Clin Endocrinol Metab 2007;92(5):1640–6. doi:10.1210/jc.2006-0572.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Matkovic V, Jelic T, Wardlaw GM, Ilich JZ, Goel PK, Wright JK, Andon MB, Smith KT, Heaney RP. Timing of peak bone mass in Caucasian females and its implication for the prevention of osteoporosis. Inference from a cross-sectional model. J Clin Invest 1994;93:799–808. doi:10.1172/JCI117034.

    CAS  PubMed  Google Scholar 

  16. Hsu YH, Venners SA, Terwedow HA, Feng Y, Niu T, Li Z, Laird N, Brain JD, Cummings SR, Bouxsein ML, Rosen CJ, Xu X. Relation of body composition, fat mass, and serum lipids to osteoporotic fractures and bone mineral density in Chinese men and women. Am J Clin Nutr 2006;83(1):146–54.

    Article  CAS  PubMed  Google Scholar 

  17. Leonard MB, Shults J, Wilson BA, Tershakovec AM, Zemel BS. Obesity during childhood and adolescence augments bone mass and bone dimensions. Am J Clin Nutr 2004;80(2):514–23.

    Article  CAS  PubMed  Google Scholar 

  18. de Onis M, Blossner M, Borghi E. Global prevalence and trends of overweight and obesity among preschool children. Am J Clin Nutr 2010;92:1257–1264. doi:10.3945/ajcn.2010.29786

    Article  PubMed  Google Scholar 

  19. Reeves PG, Nielsen FH, Fahey GC. 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 1993;123(11):1939–51.

    Article  CAS  PubMed  Google Scholar 

  20. Gerard-Monnier D, Erdelmeier I, Regnard K, Moze-Henry N, Yadan JC, Chaudiere J. Reactions of 1-methyl-2-phenylindole with malondialdehyde and 4-hydroxyalkenals. Analytical applications to a colorimetric assay of lipid peroxidation. Chem Res Toxicol 1998;11(10):1176–83. doi:10.1021/tx9701790.

    CAS  PubMed  Google Scholar 

  21. Sedlak J, Lindsay RH. Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman’s reagent. Anal Biochem 1968;25(1): 192–205. doi:10.1016/0003-2697(68)90092-4.

    Article  CAS  PubMed  Google Scholar 

  22. Falcai MJ, Zamarioli A, Leoni GB, Neto MDS, Volpon JB. Swimming Activity Prevents the Unloading Induced Loss of Bone Mass, Architecture, and Strenght in Rats, BioMed Res Int 2015. doi:10.1155/2015/507848.

    Google Scholar 

  23. Shimano RC, Macedo AP, Falcai MJ, Ervolino E, Shimano AC, Issa JP. Biomechanical and microstructural benefits of physical exercise associated with risedronate in bones of ovariectomized rats. Microsc Res Tech 2014;77(6):431–8. doi: 10.1002/jemt.22363.

    Article  CAS  PubMed  Google Scholar 

  24. Volpon JB, Silva AV, Falcai MJ, Louzada MJ, Zamarioli A, Kotake BG, JPM Issa. The osteogenic effects of swimming on bone mass, strength, and microarchitecture in rats with unloading-induced bone loss. Microsc Res Tech 2015;78(9):784–91. doi:10.1002/ jemt.22541.

    Article  PubMed  Google Scholar 

  25. Bouxsein ML, Boyd SK, Christiansen BA, Guldberg RE, Jepsen KJ, Muller R. Guidelines for assessment of bone microstructure in rodents using micro-computed tomography. J Bone Miner Res 2010;25(7):1468–86. doi:10.1002/jbmr.141.

    Article  PubMed  Google Scholar 

  26. Gasparini GA, Yanagihara GR, Shimano AC. Quantificação da Imagem do Microscópio Eletrônico de Varredura-QIMEV, Revista da Propriedade Industrial, Brazil, 2016.

    Google Scholar 

  27. Parfitt AM, Drezner MK, Glorieux FH, Kanis JA, Malluche H, Meunier PJ, Ott SM, Recker RR. Bone histomorphometry: standardization of nomenclature, symbols, and units. Report of the ASBMR Histomorphometry Nomenclature Committee. J Bone Miner Res 2(6):595-610. doi:10.1002/jbmr.5650020617.

  28. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001;25(4):402–8. doi:10.1006/meth.2001.1262.

    Article  CAS  PubMed  Google Scholar 

  29. Schwetz V, Pieber T, Obermayer-Pietsch B. The endocrine role of the skeleton: background and clinical evidence. Eur J Endocrinol 2012;166(6):959–67. doi:10.1530/eje-12-0030.

    Article  CAS  PubMed  Google Scholar 

  30. Nguyen TV, Howard GM, Kelly PJ, Eisman J. Bone mass, lean mass, and fat mass: same genes or same environments? Am J Epidemiol 1998;147(1):3–16.

    Article  CAS  PubMed  Google Scholar 

  31. Laet CD, Kanis JA, Oden A, Johanson H, Johnell O, Delmas P, Eisman JA, Kroger H, Fujiwara S, Garnero P, McCloskey EV, Mellstrom D, Melton LJ, Meunier PJ, Pols HA, Reeve J, Silman A, Tenenhouse A. Body mass index as a predictor of fracture risk: a meta-analysis,. Osteoporos Int 2005;16(11):1330–8. doi:10.1007/s00198-005-1863-y.

    Article  PubMed  Google Scholar 

  32. Ravn P, Cizza G, Bjarnason NH, Thompson D, Daley M, Wasnich RD, McClung M, Hosking D, Yates AJ, Christiansen C. Low body mass index is an important risk factor for low bone mass and increased bone loss in early postmenopausal women. Early Postmenopausal Intervention Cohort (EPIC) study group. J Bone Miner Res 1999;14(9):1622–7. doi: 10.1359/jbmr.1999.14.9.1622.

    CAS  Google Scholar 

  33. Burguera B, Hofbauer LC, Thomas T, Gori F, Evans GL, Khosla S, Riggs BL, Turner RT. Leptin reduces ovariectomy-induced bone loss in rats. Endocrinology 2001;(8):3546–53. doi: 10.1210/endo.142.8.8346.

    Article  Google Scholar 

  34. Ducy P, Amling M, Takeda S, Priemel M, Schilling AF, Beil FT, Shen J, Vinson C, Rueger JM, Karsenty G. Leptin inhibits bone formation through a hypothalamic relay: a central control of bone mass. Cell 2000;100(2):197–207. doi: 10.1016/S0092-8674(00)81558-5.

    Article  CAS  PubMed  Google Scholar 

  35. Jurimae J, Jurimae T, Leppik A, Kums T. The influence of ghrelin, adiponectin, and leptin on bone mineral density in healthy postmenopausal women. J Bone Miner Metab 2008;26(6):618–23. doi 10.1007/s00774-008-0861-5.

    Article  PubMed  Google Scholar 

  36. Biver E, Salliot C, Combescure C, Gossec L, Hardouin P, Legroux-Gerot I, Cortet B. Influence of adipokines and ghrelin on bone mineral density and fracture risk: a systematic review and meta-analysis. J Clin Endocrinol Metab 2011;96(9):2703–13. doi: 10.1210/jc.2011-0047.

    Article  CAS  PubMed  Google Scholar 

  37. Iwaniec UT, Dube MG, Boghossian S, Song H, Helferich WG, Turner RT Kalra SP. Body mass influences cortical bone mass independent of leptin signaling. Bone 2009;44(3):404–12. doi:10.1016/j.bone.2008.10.058.

    Article  CAS  PubMed  Google Scholar 

  38. Halade GV, Rahman MM, Williams PJ, Fernandes G. High fat diet-induced animal model of age-associated obesity and osteoporosis. J Nutr Biochem 2010;21(12):1162–9. doi:10.1016/j.jnutbio.2009.10.002.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Halade GV, El Jamali A, Williams PJ, Fajardo RJ, Fernandes G. Obesity-mediated inflammatory microenvironment stimulates osteoclastogenesis and bone loss in mice. Exp Gerontol 2011;46(1):43–52. doi:10.1016/j.exger.2010.09.014.

    Article  CAS  PubMed  Google Scholar 

  40. Wang Y, Dellatore P, Douard V, Qin L, Watford M, Ferraris R, Lin T, Shapses AS. High fat diet enriched with satured, but not monounsaturated fatty acids adversely affects femur, and both diets increase calcium absorption in older female mice. Nutr Res 2016;36(7): 742–50. doi: 10.1016/j.nutres.2016.03.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Macedo AP, Shimano RC, Ferrari DT, Issa JP, Jordao AA, Shimano AC. Influence of treadmill training on bone structure under osteometabolic alteration in rats subjected to high-fat diet. Scand J Med Sci Sports 2016. doi: 10.1111/sms.12650.

    Google Scholar 

  42. Goulding A, Taylor RW, Jones IE, McAuley KA, Manning PJ, Williams SM. Overweight and obese children have low bone mass and area for their weight. Int J Obes Relat Metab Disord 2000;24(5):627–32.

    Article  CAS  PubMed  Google Scholar 

  43. Goulding A, Taylor RW, Jones IE, Manning PJ, Williams SM. Spinal overload: a concern for obese children and adolescents? Osteoporos Int 2002;13(10):835–40. doi:10.1007/s001980200116.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Departamento de Biomecânica, Medicina e Reabilitação do Aparelho Locomotor. Faculdade de Medicina de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto–São Paulo, Brazil

    G. Rezende Yanagihara, R. Carminati Shimano, J. Atsuko Tida, J. Suzuki Yamanaka, J. P. Mardegan Issa & A. C. Shimano

  2. Departamento de Física e Química. Faculdade de Ciências Farmacêuticas de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto–São Paulo, Brazil

    S. Yasuyo Fukada

  3. Departamento de Morfologia, Fisiologia e Patologia Básica. Faculdade de Odontologia de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto–São Paulo, Brazil

    J. P. Mardegan Issa

  4. Instituto de Ciência e Inovação em Engenharia Mecânica e Engenharia Industrial, Departamento de Engenharia Mecânica, Faculdade de Engenharia, Universidade do Porto, Porto, Portugal

    João Manuel R. S. Tavares

  5. Faculdade de Engenharia da Universidade do Porto, Rua Dr. Roberto Frias, s/n, 4200-465, Porto, Portugal

    João Manuel R. S. Tavares

Authors
  1. G. Rezende Yanagihara
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. R. Carminati Shimano
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. Atsuko Tida
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J. Suzuki Yamanaka
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. S. Yasuyo Fukada
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. J. P. Mardegan Issa
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. A. C. Shimano
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. João Manuel R. S. Tavares
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to João Manuel R. S. Tavares.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yanagihara, G.R., Shimano, R.C., Atsuko Tida, J. et al. Influence of high-fat diet on bone tissue: An experimental study in growing rats. J Nutr Health Aging 21, 1337–1343 (2017). https://doi.org/10.1007/s12603-017-0871-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12603-017-0871-x

Key words

Search

Navigation