Skip to main content

Advertisement

Log in

The microarchitecture and chemical composition of the femur neck of senescent female rats after different physical training protocols

  • Original Article
  • Published:
GeroScience Aims and scope Submit manuscript

Abstract

A sedentary lifestyle, coupled with a decrease in estrogen, impairs bone homeostasis, favoring to the development of osteopenia and osteoporosis, both recognized as risk factors for fractures. Here, we investigated the quality of the femur, particularly the femur neck region, and the ambulation performance of senescent rats subjected to three different physical training protocols during the periestropause period. Forty-eight female rats, 18 months of age, were subjected to a 120-day training period, three times a week. The rats were distributed into four groups: aerobic training (AT), strength training (ST), concurrent training (CT), or no training (NT). After the experimental period, at 21 months of age, ambulation performance and femur were analyzed using microtomography, Raman stereology, densitometry, and mechanical strength tests. The results demonstrated greater remodeling activity and improvement in resistance and bone microarchitecture in the femur neck of senescent female rats after undergoing physical training. Our verified higher intensities of bands related to collagen, phosphate, amide III, and amide I. Furthermore, the analysis of the secondary collagen structures indicated alterations in the collagen network due to the exercise, resulting in increased bone strength. Both AT and strength-based training proved beneficial, with AT showing greater adaptations in bone density and stiffness in the femur, while strength-based training greater adaptations in trabecular and cortical structure. These insights contribute to the understanding of the potential interventions for preventing osteopenia and osteoporosis, which are critical risk factors for fractures.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12
Fig. 13

Similar content being viewed by others

References

  1. Cavedon V, Milanese C, Laginestra FG, Giuriato G, Pedrinolla A, Ruzzante F, et al. Bone and skeletal muscle changes in oldest-old women: the role of physical inactivity. Aging Clin Exp Res. 2020;32:207–14. https://doi.org/10.1007/s40520-019-01352-x.

    Article  PubMed  Google Scholar 

  2. Marques EA, Wanderley F, Machado L, Sousa F, Viana JL, Moreira- Gonçalves D, et al. Effects of resistance and aerobic exercise on physical function, bone mineral density, OPG and RANKL in older women. Exp Gerontol. 2011;46:524–32. https://doi.org/10.1016/j.exger.2011.02.005.

    Article  CAS  PubMed  Google Scholar 

  3. Arazi H, Samadpour M, Eghbali E. The effects of concurrent training (aerobic resistance) and milk consumption on some markers of bone mineral density in women with osteoporosis. BMC Womens Health. 2018;18:202. https://doi.org/10.1186/s12905-018-0694-x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Body J-J, Bergmann P, Boonen S, Boutsen Y, Bruyere O, Devogelaer J-P, et al. Non-pharmacological management of osteoporosis: a consensus of the Belgian Bone Club. Osteoporos Int. 2011;22:2769–88. https://doi.org/10.1007/s00198-011-1545x.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Martyn-St James M, Carroll S. Effects of different impact exercise modalities on bone mineral density in premenopausal women: a meta-analysis. J Bone Miner Metab. 2010;28:251–67. https://doi.org/10.1007/s00774-009-0139-6.

    Article  PubMed  Google Scholar 

  6. Martelli S, Beck B, Saxby D, Lloyd D, Pivonka P, Taylor M. Modelling human locomotion to inform exercise prescription for osteoporosis. Curr Osteoporos Rep. 2020;18:301–11. https://doi.org/10.1007/s11914-020-00592-5.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Stringhetta-Garcia CT, Morais SRL, Fernandes F, Perez-Ueno MJ, Almeida RP, Louzada MJQ, et al. Effects of strength training and raloxifene on femoral neck metabolism and microarchitecture of aging female Wistar rats. Sci Rep. 2017;7:1–12. https://doi.org/10.1038/s41598-017-13098-5.

    Article  CAS  Google Scholar 

  8. Singulani MP, Stringhetta-Garcia CT, Santos LF, Morais SRL, Louzada MJQ, Oliveira SHP, et al. Effects of strength training on osteogenic differentiation and bone strength in aging female Wistar rats. Sci Rep. 2017;7:42878. https://doi.org/10.1038/srep42878.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Peres-Ueno MP, Fernandes F, Brito VGB, Nicola AC, Stringhetta-Garcia CT, Castoldi RC, et al. Effect of pre-treatment of strength training and raloxifene in periestropause on bone healing. Bone. 2020;134:115285. https://doi.org/10.1016/j.bone.2020.115285.

    Article  CAS  PubMed  Google Scholar 

  10. Kim S-W, Seo M-W, Jung H-C, Song J-K. Effects of high-impact weight-bearing exercise on bone mineral density and bone metabolism in middle-aged premenopausal women: a randomized controlled trial. Appl Sci. 2021;11(2):846. https://doi.org/10.3390/app11020846.

    Article  CAS  Google Scholar 

  11. Alp A. Effects of aerobic exercise on bone specific alkaline phosphatase and urinary CTX levels in premenopausal women. Rehabil Derg. 2013;59:310–3. https://doi.org/10.4274/tftr.93546.

    Article  Google Scholar 

  12. Babatunde OO, Forsyth JJ, Gidlow CJ. A meta-analysis of brief high-impact exercises for enhancing bone health in premenopausal women. Osteoporos Int. 2012;23:109–19. https://doi.org/10.1007/s00198-011-1801-0.

    Article  CAS  PubMed  Google Scholar 

  13. Armamento-Villareal R, Aguirre L, Waters DL, Napoli N, Qualls C, Villareal DT. Effect of aerobic or resistance exercise, or both, on bone mineral density and bone metabolism in obese older adults while dieting: a randomized controlled trial. J Bone Miner Res. 2020;35:430–9. https://doi.org/10.1002/jbmr.3905.

  14. Pinheiro MB, Oliveira J, Bauman A, Fairhall N, Kwok W, Sherrington C. Evidence on physical activity and osteoporosis prevention for people aged 65+ years: a systematic review to inform the WHO guidelines on physical activity and sedentary behavior. Int J Behav Nutr Phys Act. 2020;17:150. https://doi.org/10.1186/s12966-020-01040-4.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Pereira LJ, Macari S, Coimbra CC, Pereira TDS, Barrioni BR, Gomez RS, et al. Aerobic and resistance training improve alveolar bone quality and interferes with bone-remodeling during orthodontic tooth movement in mice. Bone. 2020;138:115496. https://doi.org/10.1016/j.bone.2020.115496.

    Article  CAS  PubMed  Google Scholar 

  16. Benedetti MG, Furlini G, Zati A, Mauro GL. The effectiveness of physical exercise on bone density in osteoporotic patients. Biomed Res Int. 2018:1–10. https://doi.org/10.1155/2018/4840531.

  17. Del Vecchio A, Casolo A, Negro F, Scorcelletti M, Bazzucchi I, Enoka R, et al. The increase in muscle force after 4 weeks of strength training is mediated by adaptations in motor unit recruitment and rate coding. J Physiol. 2019;597:1873–87. https://doi.org/10.1113/JP277250.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Remaud A, Cornu C, Guével A. Neuromuscular adaptations to 8-week strength training: isotonic versus isokinetic mode. Eur J Appl Physiol. 2010;108:59–69. https://doi.org/10.1007/s00421-009-1164-9.

    Article  PubMed  Google Scholar 

  19. Hawley JA, Hargreaves M, Joyner MJ, Zierath JR. Integrative biology of exercise. Cell. 2014;159:738–49. https://doi.org/10.1016/j.cell.2014.10.029.

    Article  CAS  PubMed  Google Scholar 

  20. Konopka AR, Harber MP. Skeletal muscle hypertrophy after aerobic exercise training. Exerc Sport Sci Rev. 2014;42:53–61. https://doi.org/10.1249/JES.0000000000000007.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Bagheri R, Robinson I, Moradi S, Purcell J, Schwab E, Silva T. Muscle protein synthesis responses following aerobic-based exercise or high-intensity interval training with or without protein ingestion: a systematic review. Sports Med. 2022;52:2713–32. https://doi.org/10.1007/s40279-022-01707-x.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Long JA, Evans HM. The oestrous cycle in the rats and its associated phenomena, in: Mem. Univ. Calif. Berkeley: University of California Press; 1922. p. 1–48.

    Google Scholar 

  23. Nicola AC, Ferreira LB, Mata MM, Vilhena-Franco T, Leite CM, Martins AB, et al. Vasopressinergic activity of the suprachiasmatic nucleus and mRNA expression of clock genes in the hypothalamus-pituitary-gonadal axis in female aging. Front Endocrinol. (Lausanne). 2021;12:1–13. https://doi.org/10.3389/fendo.2021.652733.

    Article  Google Scholar 

  24. Ferreira LB, Nicola AC, Anselmo-Franci JA, Dornelles RCM. Activity of neurons in the preoptic area and their participation in reproductive senescence: preliminary findings. Exp Gerontol. 2015;72:157–61. https://doi.org/10.1016/j.exger.2015.10.003.

    Article  PubMed  Google Scholar 

  25. Nicola AC, Leite CM, Nishikava MM, Castro JCB, Anselmo-Franci JA, Dornelles RCM. The transition to reproductive senescence is characterized by increase in A6 and AVPV neuron activity with attenuation of noradrenaline content. Exp Gerontol. 2016;81:19–27. https://doi.org/10.1016/j.exger.2016.04.015.

    Article  CAS  PubMed  Google Scholar 

  26. Dishman RK, Armstrong RB, Delp MD, Graham RE, Dunn AL. Open-field behavior is not related to treadmill performance in exercising rats. Physiol Behav. 1988;43:541–6. https://doi.org/10.1016/0031-9384(88)90206-5.

    Article  CAS  PubMed  Google Scholar 

  27. Henrique JS, França EF, Cardoso FS, Serra FT, Almeida AA, Fernandes J, Arida RM, Gomes da Silva S. Cortical and hippocampal expression of inflammatory and intracellular signaling proteins in aged rats submitted to aerobic and resistance physical training. Exp Gerontol. 2018;110:284–90. https://doi.org/10.1016/j.exger.2018.06.025.

    Article  CAS  PubMed  Google Scholar 

  28. Nokia MS, Lensu S, Ahtiainen JP, Johansson PP, Koch LG, Britton SL, Kainulainen H. Physical exercise increases adult hippocampal neurogenesis in male rats provided it is aerobic and sustained. J Physiol. 2016;594:1855–73. https://doi.org/10.1113/JP271552.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Picoli CC, Romero PVS, Gilio GR, Guariglia DA, Tófolo LP, Moraes SMF, et al. Peak velocity as an alternative method for training prescription in mice. Front Physiol. 2018;9:42. https://doi.org/10.3389/fphys.2018.00042.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Montenegro LHM, Moita L, Reis FK, Oliveira E, Lisboa P, Moura E, et al. Effects of a moderate physical training on the leptin synthesis by adipose tissue of adult rats submitted to a perinatal lowprotein diet. Horm Metab Res. 2012;44:814–8. https://doi.org/10.1055/s-00321316350.

    Article  Google Scholar 

  31. Hornberger TA Jr, Farrar RP. Physiological hypertrophy of the FHL muscle following 8 weeks of progressive resistance exercise in the rat. Can J Appl Physiol. 2004;29:16–31. https://doi.org/10.1139/h04-00.

    Article  CAS  PubMed  Google Scholar 

  32. Stringhetta-Garcia CT, Singulani MP, Santos LF, Louzada MJQ, Nakamune ACS, Chaves-Neto AH, et al. The effects of strength training and raloxifene on bone health in aging ovariectomized rats. Bone. 2016;85:45–54. https://doi.org/10.1016/j.bone.2015.11.023.

    Article  CAS  PubMed  Google Scholar 

  33. Kennel PF, Fonteneau P, Martin E, Schmidt JM, Azzouz M, Borg J, et al. Electromyographical and motor performance studies in the pmn mouse model of neurodegenerative disease. Neurobiol Dis. 1996;3:137–47. https://doi.org/10.1006/nbdi.1996.0014.

    Article  CAS  PubMed  Google Scholar 

  34. Santos LF, Fernandes-Breitenbach F, Silva RA, Santos DR, Peres-Ueno MJ, Ervolino E, et al. The action of oxytocin on the bone of senescent female rats. Life Sci. 2022;297:120484. https://doi.org/10.1016/j.lfs.2022.120484.

    Article  CAS  PubMed  Google Scholar 

  35. Laidler PM, Taga EM, Van Etten RL. Human liver acid phosphatases: cysteine residues of the low-molecular-weight enzyme. Arch Biochem Biophys. 1982;216:512–21. https://doi.org/10.1016/0003-9861(82)90240-5.

    Article  CAS  PubMed  Google Scholar 

  36. Lau KH, Onishi T, Wergedal JE, Singer FR, Baylink DJ. Characterization and assay of tartrate-resistant acid phosphatase activity in serum: potential use to assess bone resorption. Clin Chem. 1987;33:458–62. https://doi.org/10.1093/clinchem/33.4.458.

    Article  CAS  PubMed  Google Scholar 

  37. Fernandes F, Stringhetta-Garcia CT, Peres-Ueno MJ, Fernandes F, Nicola AC, Castoldi RC, et al. Oxytocin and bone quality in the femoral neck of rats in periestropause. Sci Rep. 2020;10:7937. https://doi.org/10.1038/s41598-020-64683-0.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Turner CH, Burr DB. Basic biomechanical measurements of bone: a tutorial. Bone. 1993;14:595–608. https://doi.org/10.1016/8756-3282(93)90081-K.

    Article  CAS  PubMed  Google Scholar 

  39. Fernandes-Breitenbach F, Peres-Ueno MJ, Santos LF, Brito VG, Castoldi RC, Louzada MJ, et al. Analysis of the femoral neck from rats in the periestropause treated with oxytocin and submitted to strength training. Bone. 2022;162:16452. https://doi.org/10.1016/j.bone.2022.116452.

    Article  CAS  Google Scholar 

  40. Huang Z, McWilliams A, Lui H, McLean DI, Lam S, Zeng H. Near-infrared raman spectroscopy for optical diagnosis of lung cancer. Int J Cancer. 2003;107:1047–52. https://doi.org/10.1002/ijc.11500.

    Article  CAS  PubMed  Google Scholar 

  41. Katainen E, Elomaa M, Laakkonen UM, Sippola E, Niemelä P, Suhonen J, Järvinen K. Quantification of the amphetamine content in seized street samples by Raman spectroscopy. J Forensic Sci. 2007;52:88–92. https://doi.org/10.1111/j.1556-4029.2006.00306.x.

    Article  CAS  PubMed  Google Scholar 

  42. Hanlon EB, Manoharan R, Koo TW, Shafer KE, Motz JT, Fitzmaurice M, et al. Prospects for in vivo raman spectroscopy. Phys Med Biol. 2000;45:R1–R59. https://doi.org/10.1088/0031-9155/45/2/201.

    Article  CAS  PubMed  Google Scholar 

  43. Choo-Smith LP, Edwards HGM, Endtz HP, Kros JM, HeuleF BH, et al. Medical applications of Raman spectroscopy: from proof of principle to clinical implementation. Biopolymers. 2002;67:1–9. https://doi.org/10.1002/bip.10064.

    Article  CAS  PubMed  Google Scholar 

  44. Silveira L, Sathaiah S, Zângaro RA, Pacheco MTT, Chavantes MC, Pasqualucci CAG. Correlation between near-infrared Raman spectroscopy and the histopathological analysis of atherosclerosis in human coronary arteries. Lasers Surg Med. 2002;30:290–7. https://doi.org/10.1002/lsm.10053.

    Article  PubMed  Google Scholar 

  45. Cheng WT, Liu MT, Liu HN, Lin SY. Micro-Raman spectroscopy used to identify and grade human skin pilomatrixoma. Microsc Res Tech. 2005;68:75–9. https://doi.org/10.1002/jemt.20229.

    Article  CAS  PubMed  Google Scholar 

  46. Minghim R, Paulovich FV, Andrade LA. Content-based text mapping using multi-dimensional projections for exploration of document collections. In: Erbacher RF, Roberts JC, Grohn MT, Borner K, editors. Visualization and Data Analysis 2006, vol. 6060; 2006. https://doi.org/10.1117/12.650880.

    Chapter  Google Scholar 

  47. Paulovich FV, Moraes ML, Maki RM, Ferreira M, Oliveira ON Jr, Oliveira MCF. Information visualization techniques for sensing and biosensing. Analyst. 2011;136:1344–50. https://doi.org/10.1039/C0AN00822B.

    Article  CAS  PubMed  Google Scholar 

  48. Coffey VG, Hawley JA. Concurrent exercise training: do opposites distract? J Physiol. 2017;595:2883–96. https://doi.org/10.1113/JP272270.

    Article  CAS  PubMed  Google Scholar 

  49. Viecelli C, Ewald CY. The non-modifiable factors age, gender, and genetics influence resistance exercise. Front Aging. 2022;12:1005848. https://doi.org/10.3389/fragi.2022.1005848.

    Article  Google Scholar 

  50. Fyfe JJ, Bishop DJ, Stepto NK. Interference between concurrent resistance and endurance exercise: molecular bases and the role of individual training variables. Sports Med. 2014;44:743–62. https://doi.org/10.1007/s40279-014-0162-1.

    Article  PubMed  Google Scholar 

  51. Schumann M, Feuerbacher JF, Sünkeler M, Freitag N, Rønnestad BR, Doma K, Lundberg TR. Compatibility of concurrent aerobic and strength training for skeletal muscle size and function: an updated systematic review and meta-analysis. Sports Med. 2022;52:601–12. https://doi.org/10.1007/s40279-021-01587-7.

    Article  PubMed  Google Scholar 

  52. Rodríguez-Molinero A, Herrero-Larrea A, Miñarro A, et al. The spatial parameters of gait and their association with falls, functional decline and death in older adults: a prospective study. Sci Rep. 2019;9:8813. https://doi.org/10.1038/s41598-019-45113-2.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Barbosa GM, Cunha JE, Cunha TM, Martinho LB, Castro PATS, Oliveira FFB, et al. Clinical-like cryotherapy improves footprint patterns and reduces synovial inflammation in a rat model of post-traumatic knee osteoarthritis. Sci Rep. 2019;9:14518. https://doi.org/10.1038/s41598-019-50958-8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Radak Z, Kumagai S, Taylor AW, Naito H, Goto S. Effects of exercise on brain function: role of free radicals. Appl Physiol Nutr Metab. 2007;32:942–6. https://doi.org/10.1139/H07-081.

    Article  CAS  PubMed  Google Scholar 

  55. Radak Z, Suzuki K, Higuchi M, Balogh L, Boldogh I, Koltai E. Physical exercise, reactive oxygen species and neuroprotection. Free Radic Biol Med. 2016;98:187–96. https://doi.org/10.1016/j.freeradbiomed.2016.01.024.

    Article  CAS  PubMed  Google Scholar 

  56. Quana H, Koltai E, Suzuki K, Aguiar AS Jr, Pinho R, Boldogh I, et al. Exercise, redox system and neurodegenerative diseases. Biochim Biophys Acta (BBA) - Mol Basis Dis. 2020;1866:1–12. https://doi.org/10.1016/j.bbadis.2020.165778.

    Article  CAS  Google Scholar 

  57. Radak Z, Ihasz F, Koltai E, Goto S, Taylor AW, Boldogh I. The redox associated adaptive response of brain to physical exercise. Free Radic Res. 2014;48:84–92. https://doi.org/10.3109/10715762.2013.826352.

    Article  CAS  PubMed  Google Scholar 

  58. van Praag H, Fleshner M, Schwartz MW, Mattson MP. Exercise, energy intake, glucose homeostasis, and the brain. J Neurosci. 2014;34:15139–49. https://doi.org/10.1523/JNEUROSCI.2814-14.2014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Chen H, Zhou X, Fujita H, Onozuka M, Kubo KY. Age-related changes in trabecular and cortical bone microstructure. Int J Endocrinol. 2013;2013:1–9. https://doi.org/10.1155/2013/213234.

    Article  Google Scholar 

  60. Watson SL, Weeks BK, Weis LJ, Harding AT, Horan SA, Beck BR. 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. 2019;33:211–20. https://doi.org/10.1002/jbmr.3659.

    Article  Google Scholar 

  61. Mustafy T, Londono I, Moldovan F, Villemure I. High impact exercise improves bone microstructure and strength in growing rats. Sci Rep. 2019;9:13128. https://doi.org/10.1038/s41598-019-49432-2.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Turner CH, Robling AG. Mechanisms by which exercise improves bone strength. J Bone Miner Metab. 2005;23:16–22. https://doi.org/10.1007/BF03026318.

    Article  CAS  PubMed  Google Scholar 

  63. Gomarasca M, Banfi G, Lombardi G. Myokines: The endocrine coupling of skeletal muscle and bone, in: Adv. Clin. Chem. 1st ed. Elsevier Inc.; 2020. p. 155–218. https://doi.org/10.1016/bs.acc.2019.07.010.

    Book  Google Scholar 

Download references

Acknowledgements

We thank the Universidade Estadual Paulista “Júlio de Mesquita Filho,” Multiuser Laboratory for Biotechnology and Bioengineering (MUBIO) of Araçatuba Dental School, FINEP (FINEP/CT-INFRA Convênio FINEP: 01.12.0530.00-PROINFRA 01/2011) and the Brazilian Society of Physiology for supporting the present study. We would also like to thank technician Pedro Luiz Florindo and Dr. Danilo de Sandre for monitoring and helping with the care of animals during the aging process and for monitoring and helping with the care of animals during the period of the study. We would also like to thank the Brazilian agency FAPESP (2021/13884-0, 2020/05423-0, and 2018/22214-6)

Funding

This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) – Código de Financiamento 001.

Author information

Authors and Affiliations

Authors

Contributions

Rafael Augusto dos Santos Silva: care of experimental animals, data collection, data analysis, data tabulation, discussion of results, paper editing. Melise Jacon Peres-Ueno: data analysis, discussion of results. Luis Fernando Gadioli Santos and Angela Nicola: data collection and data analysis. Fernanda Fernandes: data collection, data analysis, and discussion of results. Rafael Jesus Gonçalves Rubira: analysis of Raman spectra of bone tissues and discussion of results; Rafael Pereira: statistical analysis and discussion of results; Antonio Hernandes Chaves-Neto: TRAP and FAL analysis and discussion of results. Rita Cássia Menegati Dornelles: guidance and monitoring of all experimental steps, data analysis, data tabulation, discussion of results, paper editing.

Corresponding author

Correspondence to Rita Cássia Menegati Dornelles.

Ethics declarations

Ethics approval

The study was conducted according to national (CONCEA—National Association for Animals Experiments Control: http://concea.mct.gov.br) and institutional laws and was approved by the Ethics Committee on Animal Use (CEUA), of the São Paulo State University (Unesp), School of Dentistry, Araçatuba, São Paulo, Brazil (Authorization Protocol 00826-2018).

Consent to participate

For this type of study, formal consent is not required.

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

ESM 1

(DOCX 4808 kb)

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

dos Santos Silva, R.A., Peres-Ueno, M.J., Nicola, A.C. et al. The microarchitecture and chemical composition of the femur neck of senescent female rats after different physical training protocols. GeroScience 46, 1927–1946 (2024). https://doi.org/10.1007/s11357-023-00948-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11357-023-00948-6

Keywords

Navigation