Skip to main content
SpringerLink
Log in

Prevalence of osteosarcopenia and its association with mortality and fractures among patients undergoing hemodialysis

  • Original Article
  • Published:
Journal of Bone and Mineral Metabolism Aims and scope Submit manuscript

Abstract

Introduction

Osteosarcopenia is an age-related syndrome characterized by the coexistence of osteoporosis and sarcopenia. Little is known about the clinical implications of osteosarcopenia among patients undergoing hemodialysis. This study investigated the prevalence of osteosarcopenia and its association with all-cause mortality and fractures in this population.

Materials and methods

This retrospective cohort study included outpatients undergoing hemodialysis in Japan. Sarcopenia was defined according to the recommendations of the Asian Working Group for Sarcopenia 2019. Osteoporosis was defined as a T-score of the calcaneus bone < – 2.5. We divided patients into three groups: robust (no osteoporosis or sarcopenia), osteoporosis or sarcopenia alone (osteoporosis without sarcopenia or sarcopenia without osteoporosis), and osteosarcopenia (osteoporosis and sarcopenia). Cox proportional-hazard and negative binomial regression models were used to estimate the associations between osteosarcopenia and all-cause mortality and fractures.

Results

Among the 328 patients (mean age, 65.5 ± 11.3 years; men, 59.1%), the prevalence of osteosarcopenia was 22.9%. During the follow-up period (1972 person-years), 131 deaths and 113 fractures occurred. Patients with osteoporosis or sarcopenia alone (hazard ratio 1.36; 95% confidence interval 0.85–2.18) and osteosarcopenia (hazard ratio 2.13; 95% confidence interval, 1.23–3.68) showed a higher risk of all-cause mortality than the robust group. Similar results were observed for the risk of fractures in patients with osteosarcopenia.

Conclusions

Patients undergoing hemodialysis showed a high prevalence of osteosarcopenia, and osteosarcopenia was associated with a poor prognosis in this patient population. Assessing osteosarcopenia may be useful for accurate prognostic stratification of patients undergoing hemodialysis.

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

Fig. 1

Similar content being viewed by others

Data availability

The datasets generated and/or analyzed during the current study are not publicly available because of ethical restrictions and participant confidentiality concerns but are available from the corresponding author to qualified researchers on reasonable request.

References

  1. 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

    Article  CAS  PubMed  Google Scholar 

  2. Teng Z, Zhu Y, Teng Y, Long Q, Hao Q, Yu X, Yang L, Lv Y, Liu J, Zeng Y, Lu S (2021) The analysis of osteosarcopenia as a risk factor for fractures, mortality, and falls. Osteoporos Int 32:2173–2183. https://doi.org/10.1007/s00198-021-05963-x

    Article  CAS  PubMed  Google Scholar 

  3. Fahimfar N, Zahedi Tajrishi F, Gharibzadeh S, Shafiee G, Tanha K, Heshmat R, Nabipour I, Raeisi A, Jalili A, Larijani B, Ostovar A (2020) Prevalence of osteosarcopenia and its association with cardiovascular risk factors in iranian older people: Bushehr Elderly Health (BEH) Program. Calcif Tissue Int 106:364–370. https://doi.org/10.1007/s00223-019-00646-6

    Article  CAS  PubMed  Google Scholar 

  4. Kirk B, Zanker J, Duque G (2020) Osteosarcopenia: epidemiology, diagnosis, and treatment-facts and numbers. J Cachexia Sarcopenia Muscle 11:609–618. https://doi.org/10.1002/jcsm.12567

    Article  PubMed  PubMed Central  Google Scholar 

  5. Balogun S, Winzenberg T, Wills K, Scott D, Callisaya M, Cicuttini F, Jones G, Aitken D (2019) Prospective associations of osteosarcopenia and osteodynapenia with incident fracture and mortality over 10 years in community-dwelling older adults. Arch Gerontol Geriatr 82:67–73. https://doi.org/10.1016/j.archger.2019.01.015

    Article  PubMed  Google Scholar 

  6. Saeki C, Tsubota A (2021) Influencing factors and molecular pathogenesis of sarcopenia and osteosarcopenia in chronic liver disease. Life (Basel) 11:899. https://doi.org/10.3390/life11090899

    Article  CAS  PubMed  Google Scholar 

  7. Inoue T, Maeda K, Nagano A, Shimizu A, Ueshima J, Murotani K, Sato K, Hotta K, Morishita S, Tsubaki A (2021) related factors and clinical outcomes of osteosarcopenia: a narrative review. Nutrients 13:291. https://doi.org/10.3390/nu13020291

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Xiang T, Fu P, Zhou L (2023) Sarcopenia and osteosarcopenia among patients undergoing hemodialysis. Front Endocrinol (Lausanne) 14:1181139. https://doi.org/10.3389/fendo.2023.1181139

    Article  PubMed  Google Scholar 

  9. Wang Y, Ma W, Pu J, Chen F (2023) Interrelationships between sarcopenia, bone turnover markers and low bone mineral density in patients on hemodialysis. Ren Fail 45:2200846. https://doi.org/10.1080/0886022X.2023.2200846

    Article  PubMed  PubMed Central  Google Scholar 

  10. Mazzaferro S, Cianciolo G, De Pascalis A, Guglielmo C, Urena Torres PA, Bover J, Tartaglione L, Pasquali M, La Manna G (2018) Bone, inflammation and the bone marrow niche in chronic kidney disease: What do we know? Nephrol Dial Transplant 33:2092–2100. https://doi.org/10.1093/ndt/gfy115

    Article  CAS  PubMed  Google Scholar 

  11. Hsu CY, Chen LR, Chen KH (2020) Osteoporosis in patients with chronic kidney diseases: a systemic review. Int J Mol Sci 21:6846. https://doi.org/10.3390/ijms21186846

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Abdalbary M, Sobh M, Elnagar S, Elhadedy MA, Elshabrawy N, Abdelsalam M, Asadipooya K, Sabry A, Halawa A, El-Husseini A (2022) Management of osteoporosis in patients with chronic kidney disease. Osteoporos Int 33:2259–2274. https://doi.org/10.1007/s00198-022-06462-3

    Article  CAS  PubMed  Google Scholar 

  13. Fouque D, Kalantar-Zadeh K, Kopple J, Cano N, Chauveau P, Cuppari L, Franch H, Guarnieri G, Ikizler TA, Kaysen G, Lindholm B, Massy Z, Mitch W, Pineda E, Stenvinkel P, Trevino-Becerra A, Wanner C (2008) A proposed nomenclature and diagnostic criteria for protein-energy wasting in acute and chronic kidney disease. Kidney Int 73:391–398. https://doi.org/10.1038/sj.ki.5002585

    Article  CAS  PubMed  Google Scholar 

  14. Taal MW, Roe S, Masud T, Green D, Porter C, Cassidy MJ (2003) Total hip bone mass predicts survival in chronic hemodialysis patients. Kidney Int 63:1116–1120. https://doi.org/10.1046/j.1523-1755.2003.00837.x

    Article  PubMed  Google Scholar 

  15. Shu X, Lin T, Wang H, Zhao Y, Jiang T, Peng X, Yue J (2022) Diagnosis, prevalence, and mortality of sarcopenia in dialysis patients: a systematic review and meta-analysis. J Cachexia Sarcopenia Muscle 13:145–158. https://doi.org/10.1002/jcsm.12890

    Article  PubMed  PubMed Central  Google Scholar 

  16. Yamamoto S, Matsuzawa R, Abe Y, Hoshi K, Yoneki K, Harada M, Watanabe T, Shimoda T, Suzuki Y, Matsunaga Y, Kamiya K, Yoshida A, Matsunaga A (2018) Utility of regular management of physical activity and physical function in hemodialysis patients. Kidney Blood Press Res 43:1505–1515. https://doi.org/10.1159/000494016

    Article  PubMed  Google Scholar 

  17. Yoshikoshi S, Yamamoto S, Suzuki Y, Imamura K, Harada M, Kamiya K, Matsunaga A (2023) Reserved gait capacity and mortality among patients undergoing hemodialysis. Nephrol Dial Transplant 38:2704–2712. https://doi.org/10.1093/ndt/gfad109

    Article  PubMed  Google Scholar 

  18. Taal MW, Cassidy MJ, Pearson D, Green D, Masud T (1999) Usefulness of quantitative heel ultrasound compared with dual-energy X-ray absorptiometry in determining bone mineral density in chronic haemodialysis patients. Nephrol Dial Transplant 14:1917–1921. https://doi.org/10.1093/ndt/14.8.1917

    Article  CAS  PubMed  Google Scholar 

  19. Organization WH (1994) Assessment of fracture risk and its application to screening for postmenopausal osteoporosis: report of a WHO study group [meeting held in Rome from 22 to 25 June 1992]. World Health Organization

    Google Scholar 

  20. Yoshikoshi S, Yamamoto S, Suzuki Y, Imamura K, Harada M, Osada S, Kamiya K, Matsunaga A (2022) Associations between dynapenia, cardiovascular hospitalizations, and all-cause mortality among patients on haemodialysis. J Cachexia Sarcopenia Muscle 13:2417–2425. https://doi.org/10.1002/jcsm.13039

    Article  PubMed  PubMed Central  Google Scholar 

  21. Xu W, Wang M, Jiang C-M, Zhang Y-MJAPjocn, (2011) Anthropometric equation for estimation of appendicular skeletal muscle mass in Chinese adults. Asia Pac J Clin Nutr 20:551–556

    Google Scholar 

  22. Chen LK, Woo J, Assantachai P, Auyeung TW, Chou MY et al (2020) Asian Working Group for Sarcopenia: 2019 consensus update on sarcopenia diagnosis and treatment. J Am Med Dir Assoc 21:e2. https://doi.org/10.1016/j.jamda.2019.12.012

    Article  Google Scholar 

  23. Yamada K, Furuya R, Takita T, Maruyama Y, Yamaguchi Y, Ohkawa S, Kumagai H (2008) Simplified nutritional screening tools for patients on maintenance hemodialysis. Am J Clin Nutr 87:106–113. https://doi.org/10.1093/ajcn/87.1.106

    Article  CAS  PubMed  Google Scholar 

  24. Liu J, Huang Z, Gilbertson DT, Foley RN, Collins AJ (2010) An improved comorbidity index for outcome analyses among dialysis patients. Kidney Int 77:141–151. https://doi.org/10.1038/ki.2009.413

    Article  PubMed  Google Scholar 

  25. White IR, Royston P, Wood AM (2011) Multiple imputation using chained equations: issues and guidance for practice. Stat Med 30:377–399. https://doi.org/10.1002/sim.4067

    Article  PubMed  Google Scholar 

  26. Ma L, Zhao S (2017) Risk factors for mortality in patients undergoing hemodialysis: a systematic review and meta-analysis. Int J Cardiol 238:151–158. https://doi.org/10.1016/j.ijcard.2017.02.095

    Article  PubMed  Google Scholar 

  27. Knol MJ, VanderWeele TJ, Groenwold RH, Klungel OH, Rovers MM, Grobbee DE (2011) Estimating measures of interaction on an additive scale for preventive exposures. Eur J Epidemiol 26:433–438. https://doi.org/10.1007/s10654-011-9554-9

    Article  PubMed  PubMed Central  Google Scholar 

  28. Gourlay ML, Fine JP, Preisser JS, May RC, Li C, Lui LY, Ransohoff DF, Cauley JA, Ensrud KE, Study of Osteoporotic Fractures Research G (2012) Bone-density testing interval and transition to osteoporosis in older women. N Engl J Med 366:225–233. https://doi.org/10.1056/NEJMoa1107142

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Lewiecki EM, Gordon CM, Baim S, Leonard MB, Bishop NJ, Bianchi ML, Kalkwarf HJ, Langman CB, Plotkin H, Rauch F, Zemel BS, Binkley N, Bilezikian JP, Kendler DL, Hans DB, Silverman S (2008) International Society for Clinical Densitometry 2007 adult and pediatric official positions. Bone 43:1115–1121. https://doi.org/10.1016/j.bone.2008.08.106

    Article  PubMed  Google Scholar 

  30. Huang T, Li C, Chen F, Xie D, Yang C, Chen Y, Wang J, Li J, Zheng F (2023) Prevalence and risk factors of osteosarcopenia: a systematic review and meta-analysis. BMC Geriatr 23:369. https://doi.org/10.1186/s12877-023-04085-9

    Article  PubMed  PubMed Central  Google Scholar 

  31. Knauer K, Chaudry O, Uder M, Kohl M, Kemmler W, Bickelhaupt S, Engelke K (2023) Effects of high-intensity resistance training on visceral adipose tissue and abdominal aortic calcifications in older men with osteosarcopenia–results from the FrOST study. Clin Interv Aging 18:71–80. https://doi.org/10.2147/CIA.S388026

    Article  PubMed  PubMed Central  Google Scholar 

  32. Jeong JH, Biruete A, Tomayko EJ, Wu PT, Fitschen P, Chung HR, Ali M, McAuley E, Fernhall B, Phillips SA, Wilund KR (2019) Results from the randomized controlled IHOPE trial suggest no effects of oral protein supplementation and exercise training on physical function in hemodialysis patients. Kidney Int 96:777–786. https://doi.org/10.1016/j.kint.2019.03.018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Cruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyere O, Cederholm T, Cooper C, Landi F, Rolland Y, Sayer AA, Schneider SM, Sieber CC, Topinkova E, Vandewoude M, Visser M, Zamboni M, Writing Group for the European Working Group on Sarcopenia in Older P, the Extended Group for E (2019) Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing 48:16–31. https://doi.org/10.1093/ageing/afy169

    Article  PubMed  Google Scholar 

  34. Fielding RA, Vellas B, Evans WJ, Bhasin S, Morley JE et al (2011) Sarcopenia: an undiagnosed condition in older adults. current consensus definition: prevalence, etiology, and consequences. International working group on sarcopenia. J Am Med Dir Assoc 12:249–256. https://doi.org/10.1016/j.jamda.2011.01.003

    Article  PubMed  Google Scholar 

  35. Tromp AM, Smit JH, Deeg DJ, Lips P (1999) Quantitative ultrasound measurements of the tibia and calcaneus in comparison with DXA measurements at various skeletal sites. Osteoporos Int 9:230–235. https://doi.org/10.1007/s001980050142

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We appreciate the contributions of the renal staff at the dialysis facility for their assistance with data collection.

Funding

This study was funded by the Japan Society for the Promotion of Science (JSPS). KAKENHI [Grant No. 19K11372] received by A. Matsunaga.

Author information

Authors and Affiliations

  1. Department of Rehabilitation Sciences, Kitasato University Graduate School of Medical Sciences, Kanagawa, Japan

    Shun Yoshikoshi, Kentaro Kamiya & Atsuhiko Matsunaga

  2. Research Team for Social Participation and Healthy Aging, Tokyo Metropolitan Institute for Geriatrics and Gerontology, Tokyo, Japan

    Shun Yoshikoshi

  3. Department of Epidemiology and Prevention, Center for Clinical Sciences, National Center for Global Health and Medicine, 1-21-1, Toyama, Shinjuku-ku, Tokyo, 162-8655, Japan

    Shohei Yamamoto

  4. Center for Outcomes Research and Economic Evaluation for Health, National Institute of Public Health, Saitama, Japan

    Yuta Suzuki

  5. Research Team for Human Care, Tokyo Metropolitan Institute for Geriatrics and Gerontology, Tokyo, Japan

    Keigo Imamura

  6. Department of Rehabilitation, Sagami Circulatory Organ Clinic, Kanagawa, Japan

    Manae Harada

Authors
  1. Shun Yoshikoshi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shohei Yamamoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yuta Suzuki
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Keigo Imamura
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Manae Harada
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Kentaro Kamiya
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Atsuhiko Matsunaga
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

SY and SY conceptualized the study and were responsible for methodology and formal analysis; AM was responsible for funding acquisition and project administration; SY, SY, YS, KI, and MH were responsible for investigation; SY was responsible for data curation, visualization, and writing the original draft; AM and KK were responsible for supervision; and all authors reviewed and edited the manuscript.

Corresponding author

Correspondence to Shohei Yamamoto.

Ethics declarations

Conflict of interest

All authors have no conflict of interest.

Additional information

Publisher's Note

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

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 44 kb)

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yoshikoshi, S., Yamamoto, S., Suzuki, Y. et al. Prevalence of osteosarcopenia and its association with mortality and fractures among patients undergoing hemodialysis. J Bone Miner Metab (2024). https://doi.org/10.1007/s00774-024-01503-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00774-024-01503-9

Keywords

Search

Navigation