Advertisement

Bone and skeletal muscle changes in oldest-old women: the role of physical inactivity

  • Valentina Cavedon
  • Chiara MilaneseEmail author
  • Fabio Giuseppe Laginestra
  • Gaia Giuriato
  • Anna Pedrinolla
  • Federico Ruzzante
  • Federico Schena
  • Massimo Venturelli
Original Article

Abstract

Background

Alterations in bone and muscle parameters related to advanced aging and physical inactivity have never been investigated in oldest-old women.

Aims

To investigate the impact of physical inactivity on bone mineral density (BMD) and body composition at the systemic and regional levels in oldest-old (> 75 years old) women. We hypothesized that, further to aging, alterations in bone and body composition parameters are exacerbated in the locomotor limbs that have experienced physical inactivity.

Methods

Whole-body and regional (lower limbs and trunk) BMD and fat-free soft tissue mass (FFSTM) were measured by means of dual-energy X-ray absorptiometry in 11 oldest-old wheelchair-bound women (OIW), 11 oldest-old mobile women (OMW), and 11 young healthy women (YW), all matched for weight (± 10 kg), height (± 10 cm).

Results

Whole-body BMD was reduced by 15% from YW to OMW and 10% from OMW to OIW. Whole-body FFSTM was also reduced from YW to OIW (− 13%). Lower limb BMD was progressively reduced among YW, OMW and OIW (− 23%). Similarly, lower limb FFSTM was reduced among YW (12,816 ± 1797 g), OMW (11,999 ± 1512 g) and OIW (10,037 ± 1489 g). Trunk BMD was progressively reduced among YW, OMW and OIW (− 19%), while FFSTM was similar among the three groups ~ 19801 g.

Conclusions

The results of the present study suggest that the alterations in bone and body composition parameters are exacerbated in the physical inactive oldest-old. These negative effects of physical inactivity are not confined to the locomotor limbs, and a systemic decline of bone and muscle parameters are likely associated with the physical inactivity.

Keywords

Oldest-old Osteoporosis Sarcopenia Physical inactivity 

Notes

Funding

There was no funding received for this study.

Compliance with ethical standards

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

Statement of human and animal rights

The present study involved human participants and all the procedures were in accordance with the ethical standards of the institutional and/or national research committee (Institutional Review Board of the Department of Neurological, Neuropsychological, Morphological and Movement Sciences; University of Verona. Prot. nr 227. Date: 29 September 2010. Tit. II/9) and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

References

  1. 1.
    Gough M, Godde K (2019) Accelerated aging: the role of socioeconomic, social, demographic, and biological factors on bone mineral density. Res Aging 41:443–466.  https://doi.org/10.1177/0164027518816516 CrossRefPubMedGoogle Scholar
  2. 2.
    Hannan MT, Felson DT, Dawson-Hughes B et al (2000) Risk factors for longitudinal bone loss in elderly men and women: the Framingham osteoporosis study. J Bone Miner Res 15:710–720CrossRefPubMedGoogle Scholar
  3. 3.
    Tarantino U, Baldi J, Celi M et al (2013) Osteoporosis and sarcopenia: the connections. Aging Clin Exp Res 25:S93–S95.  https://doi.org/10.1007/s40520-013-0097-7 CrossRefPubMedGoogle Scholar
  4. 4.
    Siris ES, Brenneman SK, Barrett-Connor E et al (2006) The effect of age and bone mineral density on the absolute, excess, and relative risk of fracture in postmenopausal women aged 50–99: results from the national osteoporosis risk assessment (NORA). Osteoporos Int 17:565–574CrossRefPubMedGoogle Scholar
  5. 5.
    Adami S, Giannini S, Giorgino R et al (2003) The effect of age, weight, and lifestyle factors on calcaneal quantitative ultrasound: the ESOPO study. Osteoporos Int 14:198–207CrossRefPubMedGoogle Scholar
  6. 6.
    Drey M, Sieber CC, Bertsch T et al (2016) Osteosarcopenia is more than sarcopenia and osteopenia alone. Aging Clin Exp Res 28:895–899.  https://doi.org/10.1007/s40520-015-0494-1 CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Binkley N, Buehring B (2009) Beyond FRAX: it’s time to consider “sarco-osteopenia”. J Clin Densitom 12:413–416.  https://doi.org/10.1016/j.jocd.2009.06.004 CrossRefPubMedGoogle Scholar
  8. 8.
    Cooper C (1997) The crippling consequences of fractures and their impact on quality of life. Am J Med 103:12S–17S (Discussion 17S–19S)CrossRefPubMedGoogle Scholar
  9. 9.
    Beaudart C, Biver E, Bruyère O et al (2018) Quality of life assessment in musculo-skeletal health. Aging Clin Exp Res 30:413–418.  https://doi.org/10.1007/s40520-017-0794-8 CrossRefPubMedGoogle Scholar
  10. 10.
    Marques A, Lourenço Ó, da Silva J (2015) The burden of osteoporotic hip fractures in Portugal: costs, health related quality of life and mortality. Osteoporos Int 26:2623–2630CrossRefPubMedGoogle Scholar
  11. 11.
    Borgström F, Lekander I, Ivergård M et al (2013) The international costs and utilities related to osteoporotic fractures study (ICUROS)—quality of life during the first 4 months after fracture. Osteoporos Int 24:811–823CrossRefPubMedGoogle Scholar
  12. 12.
    Piscitelli P, Brandi M, Cawston H et al (2014) Epidemiological burden of postmenopausal osteoporosis in Italy from 2010 to 2020: estimations from a disease model. Calcif Tissue Int 95:419–427.  https://doi.org/10.1007/s00223-014-9910-3 CrossRefPubMedGoogle Scholar
  13. 13.
    Tarantino U, Cannata G, Cerocchi I et al (2007) Surgical approach to fragility fractures: problems and perspectives. Aging Clin Exp Res 19:12–21PubMedGoogle Scholar
  14. 14.
    Johnell O, Kanis JA (2006) An estimate of the worldwide prevalence and disability associated with osteoporotic fractures. Osteoporos Int 17:1726–1733CrossRefPubMedGoogle Scholar
  15. 15.
    Marin-Mio RV, Moreira LDF, Camargo M et al (2018) Lean mass as a determinant of bone mineral density of proximal femur in postmenopausal women. Arch Endocrinol Metab 62:431–437.  https://doi.org/10.20945/2359-3997000000059 CrossRefPubMedGoogle Scholar
  16. 16.
    Hirschfeld HP, Kinsella R, Duque G (2017) Osteosarcopenia: where bone, muscle, and fat collide. Osteoporos Int 28:2781–2790.  https://doi.org/10.1007/s00198-017-4151-8 CrossRefGoogle Scholar
  17. 17.
    Ilich JZ, Kelly OJ, Inglis JE et al (2014) Interrelationship among muscle, fat, and bone: connecting the dots on cellular, hormonal, and whole body levels. Ageing Res Rev 15:51–60.  https://doi.org/10.1016/j.arr.2014.02.007 CrossRefPubMedGoogle Scholar
  18. 18.
    Binder EF, Kohrt WM (2000) Relationships between body composition and bone mineral content and density in older women and men. Clin Exerc Physiol 2:84–91Google Scholar
  19. 19.
    Gillette-Guyonnet S, Nourhashemi F, Lauque S et al (2000) Body composition and osteoporosis in elderly women. Gerontology 46:189–193CrossRefPubMedGoogle Scholar
  20. 20.
    Marcell TJ (2003) Sarcopenia: causes, consequences, and preventions. J Gerontol A Biol Sci Med Sci 58:M911–M916CrossRefPubMedGoogle Scholar
  21. 21.
    Di Monaco M, Castiglioni C, Milano E et al (2018) Is there a definition of low lean mass that captures the associated low bone mineral density? A cross-sectional study of 80 men with hip fracture. Aging Clin Exp Res 30:1429–1435.  https://doi.org/10.1007/s40520-018-1058-y CrossRefPubMedGoogle Scholar
  22. 22.
    Yoshimura N, Muraki S, Oka H et al (2017) Is osteoporosis a predictor for future sarcopenia or vice versa? Four-year observations between the second and third ROAD study surveys. Osteoporos Int 28:189–199.  https://doi.org/10.1007/s00198-016-3823-0 CrossRefPubMedGoogle Scholar
  23. 23.
    Cruz-Jentoft AJ, Baeyens JP, Bauer JM et al (2010) Sarcopenia: European consensus on definition and diagnosis. Age Ageing 39:412–423.  https://doi.org/10.1093/ageing/afq034 CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Di Iorio A, Abate M, Di Renzo D et al (2006) Sarcopenia: age-related skeletal muscle changes from determinants to physical disability. Int J Immunopathol Pharmacol 19:703–719CrossRefPubMedGoogle Scholar
  25. 25.
    Seriolo B, Paolino S, Casabella A et al (2013) Osteoporosis in the elderly. Aging Clin Exp Res 25:S27–S29.  https://doi.org/10.1007/s40520-013-0107-9 CrossRefPubMedGoogle Scholar
  26. 26.
    Kanis JA, Cooper C, Rizzoli R et al (2019) Executive summary of European guidance for the diagnosis and management of osteoporosis in postmenopausal women. Aging Clin Exp Res 31:15–17.  https://doi.org/10.1007/s40520-018-1109-4 CrossRefPubMedGoogle Scholar
  27. 27.
    Naro F, Venturelli M, Monaco L et al (2019) Skeletal muscle fiber size and gene expression in the oldest-old with differing degrees of mobility. Front Physiol 10:313.  https://doi.org/10.3389/fphys.2019.00313 CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Venturelli M, Reggiani C, Richardson RS et al (2018) Skeletal muscle function in the oldest-old: the role of intrinsic and extrinsic factors. Exerc Sport Sci Rev 46:188–194.  https://doi.org/10.1249/JES.0000000000000155 CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Lacombe J, Cairns BJ, Green J et al (2016) The effects of age, adiposity, and physical activity on the risk of seven site-specific fractures in postmenopausal women. J Bone Miner Res 31:1559–1568.  https://doi.org/10.1002/jbmr.2826 CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Weaver CM, Gordon CM, Janz KF et al (2016) The National Osteoporosis Foundation’s position statement on peak bone mass development and lifestyle factors: a systematic review and implementation recommendations. Osteoporos Int 27:1281–1386.  https://doi.org/10.1007/s00198-015-3440-3 CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Venturelli M, Saggin P, Muti E et al (2015) In vivo and in vitro evidence that intrinsic upper- and lower-limb skeletal muscle function is unaffected by ageing and disuse in oldest-old humans. Acta Physiol 215:58–71.  https://doi.org/10.1111/apha.12524 CrossRefGoogle Scholar
  32. 32.
    Girgis CM, Mokbel N, Digirolamo DJ (2014) Therapies for musculoskeletal disease: can we treat two birds with one stone? Curr Osteoporos Rep 12:142–153.  https://doi.org/10.1007/s11914-014-0204-5 CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Venturelli M, Morgan GR, Donato AJ et al (2014) Cellular aging of skeletal muscle: telomeric and free radical evidence that physical inactivity is responsible and not age. Clin Sci 127:415–421.  https://doi.org/10.1042/CS20140051 CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Evans WJ (2004) Protein nutrition, exercise and aging. J Am Coll Nutr 23:601S–609SCrossRefPubMedGoogle Scholar
  35. 35.
    Svejme O, Ahlborg HG, Karlsson MK (2014) Physical activity reduces bone loss in the distal forearm in post-menopausal women: a 25-year prospective study. Scand J Med Sci Sports 24:159–165.  https://doi.org/10.1111/j.1600-0838.2012.01504.x CrossRefPubMedGoogle Scholar
  36. 36.
    Milanese C, Piscitelli F, Zenti MG et al (2013) Ten-week whole-body vibration training improves body composition and muscle strength in obese women. Int J Med Sci 10:307–311.  https://doi.org/10.7150/ijms.5161 CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Nilsson M, Ohlsson C, Eriksson AL et al (2008) Competitive physical activity early in life is associated with bone mineral density in elderly Swedish men. Osteoporos Int 19:1557–1566.  https://doi.org/10.1007/s00198-008-0600-8 CrossRefPubMedGoogle Scholar
  38. 38.
    Chen P, Miller PD, Delmas PD et al (2006) Change in lumbar spine BMD and vertebral fracture risk reduction in teriparatide-treated postmenopausal women with osteoporosis. J Bone Miner Res 21:1785–1790CrossRefPubMedGoogle Scholar
  39. 39.
    Bischoff H, Freitag P, Jundt G et al (1999) Type I osteogenesis imperfecta: diagnostic difficulties. Clin Rheumatol 18:48–51CrossRefPubMedGoogle Scholar
  40. 40.
    Sato M, Grese TA, Dodge JA et al (1999) Emerging therapies for the prevention or treatment of postmenopausal osteoporosis. J Med Chem 42:1–24CrossRefPubMedGoogle Scholar
  41. 41.
    Sorva A, Välimäki M, Risteli J et al (1994) Serum ionized calcium, intact PTH and novel markers of bone turnover in bedridden elderly patients. Eur J Clin Investig 24:806–812CrossRefGoogle Scholar
  42. 42.
    Folstein MF, Folstein SE, McHugh PR (1975) “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12:189–198.  https://doi.org/10.1016/0022-3956(75)90026-6 CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Tinetti ME (1986) Performance-oriented assessment of mobility problems in elderly patients. J Am Geriatr Soc 34:119–126CrossRefPubMedGoogle Scholar
  44. 44.
    Nana A, Slater GJ, Stewart AD et al (2015) Methodology review: using dual-energy X-ray absorptiometry (DXA) for the assessment of body composition in athletes and active people. Int J Sport Nutr Exerc Metab 25:198–215CrossRefPubMedGoogle Scholar
  45. 45.
    Box GEP, Cox DR (1964) An analysis of transformations. J Royal Stat Soc Series B Stat Methodol 26:211–252Google Scholar
  46. 46.
    Cohen J (1988) Statistical power analysis for the behavioral sciences, 2nd edn. Lawrence Erlbaum Associates, HillsdaleGoogle Scholar
  47. 47.
    Faul F, Erdfelder E, Buchner A et al (2009) Statistical power analyses using G*Power 3.1: tests for correlation and regression analyses. Behav Res Methods 41:1149–1160.  https://doi.org/10.3758/brm.41.4.1149 CrossRefGoogle Scholar
  48. 48.
    Filippin LI, Teixeira VN, da Silva MP et al (2015) Sarcopenia: a predictor of mortality and the need for early diagnosis and intervention. Aging Clin Exp Res 27:249–254.  https://doi.org/10.1007/s40520-014-0281-4 CrossRefPubMedGoogle Scholar
  49. 49.
    Lam H, Qin YX (2008) The effects of frequency-dependent dynamic muscle stimulation on inhibition of trabecular bone loss in a disuse model. Bone 43:1093–1100.  https://doi.org/10.1016/j.bone.2008.07.253 CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Ashe MC, Fehling P, Eng JJ et al (2006) Bone geometric response to chronic disuse following stroke: a pQCT study. J Musculoskelet Neuronal Interact 6:226–233PubMedGoogle Scholar
  51. 51.
    Pereira Silva JA, Costa Dias F, Fonseca JE et al (2004) Low bone mineral density in professional scuba divers. Clin Rheumatol 23:19–20CrossRefPubMedGoogle Scholar
  52. 52.
    Rittweger J, Frost HM, Schiessl H et al (2005) Muscle atrophy and bone loss after 90 days’ bed rest and the effects of flywheel resistive exercise and pamidronate: results from the LTBR study. Bone 36:1019–1029CrossRefPubMedGoogle Scholar
  53. 53.
    Leblanc AD, Schneider VS, Evans HJ et al (1990) Bone mineral loss and recovery after 17 weeks of bed rest. J Bone Miner Res 5:843–850CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of Neurosciences, Biomedicine and Movement SciencesUniversity of VeronaVeronaItaly
  2. 2.Department of Internal MedicineUniversity of UtahSalt Lake CityUSA

Personalised recommendations