Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Prevalence of osteoporosis among patients after stem cell transplantation: a systematic review and meta-analysis

Bone Marrow Transplantation (2024)Cite this article

Subjects

Abstract

The prevalence of osteoporosis in post stem cell transplantation (SCT) is poorly defined. We performed a systematic review and meta-analysis to determine the prevalence of osteoporosis in patients with hematologic diseases who underwent SCT. PubMed, EMBASE, and Web of Science were searched (from inception to 30th April 2023) using Medical Subject Headlines to find studies that assessed the prevalence of osteoporosis among post SCT. Thirteen articles meeting the inclusion criteria were included in the analysis. The pooled prevalence rates of osteoporosis, osteopenia, and decreased bone mineral density (BMD) were determined to be 14.2% (95% CI 9.7–18.8), 36.0% (95% CI 23.8–48.2), and 47.8% (95% CI 36.6–58.9), respectively. Substantial heterogeneity was observed among the included studies (I² values ranged from 81% to 99%). Subgroup analyses revealed variations in prevalence based on gender, follow-up duration, age, region, sample size, and study quality. These findings suggest a high prevalence of osteoporosis in post-SCT patients. Given the negative impact of osteoporosis on prognosis and recipient survival, clinicians should prioritize preventive measures, early diagnosis, and effective treatments to minimize its impact.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1
Fig. 2: Forest plot for the estimated osteoporosis prevalence in post-SCT.
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Kendler DL, Body JJ, Brandi ML, Broady R, Cannata-Andia J, Cannata-Ortiz MJ, et al. Bone management in hematologic stem cell transplant recipients. Osteoporos Int. 2018;29:2597–610.

    Article  CAS  PubMed  Google Scholar 

  2. Khan Z, Agarwal NB, Bhurani D, Khan MA. Risk factors for hematopoietic stem cell transplantation-associated bone loss. Transplant Cell Ther. 2021;27:212–21.

    Article  CAS  PubMed  Google Scholar 

  3. Compston JE, McClung MR, Leslie WD. Osteoporosis. Lancet. 2019;393:364–76.

    Article  CAS  PubMed  Google Scholar 

  4. Clynes MA, Harvey NC, Curtis EM, Fuggle NR, Dennison EM, Cooper C. The epidemiology of osteoporosis. Br Med Bull. 2020;133:105–17.

    PubMed  Google Scholar 

  5. Fuggle NR, Curtis EM, Ward KA, Harvey NC, Dennison EM, Cooper C. Fracture prediction, imaging and screening in osteoporosis. Nat Rev Endocrinol. 2019;15:535–47.

    Article  PubMed  Google Scholar 

  6. Force USPST, Curry SJ, Krist AH, Owens DK, Barry MJ, Caughey AB, et al. Screening for osteoporosis to prevent fractures: US Preventive Services Task Force recommendation statement. JAMA. 2018;319:2521–31.

    Article  Google Scholar 

  7. Evenepoel P, Claes K, Meijers B, Laurent MR, Bammens B, Naesens M, et al. Bone mineral density, bone turnover markers, and incident fractures in de novo kidney transplant recipients. Kidney Int. 2019;95:1461–70.

    Article  PubMed  Google Scholar 

  8. Krol CG, Dekkers OM, Kroon HM, Rabelink TJ, van Hoek B, Hamdy NA. Longitudinal changes in BMD and fracture risk in orthotopic liver transplant recipients not using bone-modifying treatment. J Bone Miner Res. 2014;29:1763–9.

    Article  CAS  PubMed  Google Scholar 

  9. Durette G, Jomphe V, Bureau NJ, Poirier C, Ferraro P, Lands LC, et al. Long-term bone mineral density changes and fractures in lung transplant recipients with cystic fibrosis. J Cyst Fibros. 2021;20:525–32.

    Article  CAS  PubMed  Google Scholar 

  10. Tran TVM, Li X, Maalouf NM. Bone health outcomes in post-lung transplant patients with cystic fibrosis. J Cyst Fibros. 2023;22:381–7.

    Article  CAS  PubMed  Google Scholar 

  11. Seguro L, Pereira RMR, Seguro LPC, Caparbo VF, Avila MS, Mangini S, et al. Bone metabolism impairment in heart transplant: results from a prospective cohort study. Transplantation. 2020;104:873–80.

    Article  PubMed  Google Scholar 

  12. Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021;372:n71.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Wells G, Shea B, O’Connell D, Peterson J, Welch V, Losos M. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses [Available from: https://www.ohri.ca/programs/clinical_epidemiology/oxford.asp.

  14. Duggan SN, Smyth ND, Murphy A, Macnaughton D, O’Keefe SJ, Conlon KC. High prevalence of osteoporosis in patients with chronic pancreatitis: a systematic review and meta-analysis. Clin Gastroenterol Hepatol. 2014;12:219–28.

    Article  PubMed  Google Scholar 

  15. Barberio B, Zamani M, Black CJ, Savarino EV, Ford AC. Prevalence of symptoms of anxiety and depression in patients with inflammatory bowel disease: a systematic review and meta-analysis. Lancet Gastroenterol Hepatol. 2021;6:359–70.

    Article  PubMed  Google Scholar 

  16. Benz E, Trajanoska K, Lahousse L, Schoufour JD, Terzikhan N, De Roos E, et al. Sarcopenia in COPD: a systematic review and meta-analysis. Eur Respir Rev. 2019;28:190049.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Castaneda S, Carmona L, Carvajal I, Arranz R, Diaz A, Garcia-Vadillo A. Reduction of bone mass in women after bone marrow transplantation. Calcif Tissue Int. 1997;60:343–7.

    Article  CAS  PubMed  Google Scholar 

  18. Baumgartner A, Moesch M, Zumsteg M, Struja T, Bernet S, Medinger M, et al. Predictors of impaired bone health in long-term survivors after allogeneic stem cell transplantation. Bone Marrow Transplant. 2019;54:1651–61.

    Article  PubMed  Google Scholar 

  19. Schimmer AD, Mah K, Bordeleau L, Cheung A, Ali V, Falconer M, et al. Decreased bone mineral density is common after autologous blood or marrow transplantation. Bone Marrow Transplant. 2001;28:387–91.

    Article  CAS  PubMed  Google Scholar 

  20. Leguy D, Magro L, Pierache A, Coiteux V, Yakoub Agha I, Cortet B, et al. Changes in bone mineral density after allogenic stem cell transplantation. Joint Bone Spine. 2022;89:105373.

    Article  CAS  PubMed  Google Scholar 

  21. Seneviratne AK, Wright C, Lam W, Lipton JH, Michelis FV. Comorbidity profile of adult survivors at 20 years following allogeneic hematopoietic cell transplantation. Eur J Haematol. 2021;106:241–9.

    Article  PubMed  Google Scholar 

  22. Gubrianska D, Machaczka M, Hassan M, Hagglund H, Ljungman P, Palmer M. Bone and hormonal status 10 years post-allogeneic bone marrow transplantation. Clin Transplant. 2019;33:e13742.

    Article  CAS  PubMed  Google Scholar 

  23. Yao S, Smiley SL, West K, Lamonica D, Battiwalla M, McCarthy PL, et al. Accelerated bone mineral density loss occurs with similar incidence and severity, but with different risk factors, after autologous versus allogeneic hematopoietic cell transplantation. Biol Blood Marrow Transplant. 2010;16:1130–7.

    Article  CAS  PubMed  Google Scholar 

  24. Abou-Mourad YR, Lau BC, Barnett MJ, Forrest DL, Hogge DE, Nantel SH, et al. Long-term outcome after allo-SCT: close follow-up on a large cohort treated with myeloablative regimens. Bone Marrow Transplant. 2010;45:295–302.

    Article  CAS  PubMed  Google Scholar 

  25. Yao S, McCarthy PL, Dunford LM, Roy DM, Brown K, Paplham P, et al. High prevalence of early-onset osteopenia/osteoporosis after allogeneic stem cell transplantation and improvement after bisphosphonate therapy. Bone Marrow Transplant. 2008;41:393–8.

    Article  CAS  PubMed  Google Scholar 

  26. Ria R, Scarponi AM, Falzetti F, Ballanti S, Di Ianni M, Sportoletti P, et al. Loss of bone mineral density and secondary hyperparathyroidism are complications of autologous stem cell transplantation. Leuk Lymphoma. 2007;48:923–30.

    Article  CAS  PubMed  Google Scholar 

  27. Massenkeil G, Fiene C, Rosen O, Michael R, Reisinger W, Arnold R. Loss of bone mass and vitamin D deficiency after hematopoietic stem cell transplantation: standard prophylactic measures fail to prevent osteoporosis. Leukemia. 2001;15:1701–5.

    Article  CAS  PubMed  Google Scholar 

  28. Schulte C, Beelen DW, Schaefer UW, Mann K. Bone loss in long-term survivors after transplantation of hematopoietic stem cells: a prospective study. Osteoporos Int. 2000;11:344–53.

    Article  CAS  PubMed  Google Scholar 

  29. Kashyap A, Kandeel F, Yamauchi D, Palmer JM, Niland JC, Molina A, et al. Effects of allogeneic bone marrow transplantation on recipient bone mineral density: a prospective study. Biol Blood Marrow Transplant. 2000;6:344–51.

    Article  CAS  PubMed  Google Scholar 

  30. Wang L, Yu W, Yin X, Cui L, Tang S, Jiang N, et al. Prevalence of osteoporosis and fracture in China: the China osteoporosis prevalence study. JAMA Netw Open. 2021;4:e2121106.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Tauchmanova L, Colao A, Lombardi G, Rotoli B, Selleri C. Bone loss and its management in long-term survivors from allogeneic stem cell transplantation. J Clin Endocrinol Metab. 2007;92:4536–45.

    Article  CAS  PubMed  Google Scholar 

  32. Anastasilakis AD, Tsourdi E, Makras P, Polyzos SA, Meier C, McCloskey EV, et al. Bone disease following solid organ transplantation: a narrative review and recommendations for management from The European Calcified Tissue Society. Bone. 2019;127:401–18.

    Article  PubMed  Google Scholar 

  33. Curtis EM, van der Velde R, Moon RJ, van den Bergh JP, Geusens P, de Vries F, et al. Epidemiology of fractures in the United Kingdom 1988-2012: Variation with age, sex, geography, ethnicity and socioeconomic status. Bone. 2016;87:19–26.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Zavatta G, Clarke BL. Glucocorticoid- and transplantation-induced osteoporosis. Endocrinol Metab Clin North Am. 2021;50:251–73.

    Article  PubMed  Google Scholar 

  35. Arias-Espinosa L, Acosta-Medina AA, Vargas-España A, Fuentes-Martin V, Colunga-Pedraza PR, Hawing-Zarate JA, et al. Acute leukemia relapse after hematopoietic stem cell transplantation: the good, the bad, and the ugly of isolated extramedullary relapse in a Latin American population. Transplant Cell Ther. 2023;29:510.e1–510.e9.

  36. Shen Y, Huang X, Wu J, Lin X, Zhou X, Zhu Z, et al. The global burden of osteoporosis, low bone mass, and its related fracture in 204 countries and territories, 1990-2019. Front Endocrinol (Lausanne). 2022;13:882241.

    Article  PubMed  Google Scholar 

  37. Banfi A, Podesta M, Fazzuoli L, Sertoli MR, Venturini M, Santini G, et al. High-dose chemotherapy shows a dose-dependent toxicity to bone marrow osteoprogenitors: a mechanism for post-bone marrow transplantation osteopenia. Cancer. 2001;92:2419–28.

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This study was funded by the National Natural Science Foundation of China (No. 81700044), the Huan-hua Talents Project from Sichuan Provincial People’s Hospital, and the Key R&D Program of the Department of Science and Technology of Sichuan Province (No. 2022YFS0600).

Author information

Author notes

  1. These authors contributed equally: Yu-Mei Yang, Shu-Jin Guo.

Authors and Affiliations

  1. Department of Health Management Center & Institute of Health Management, Sichuan Provincial People’s Hospital, University of Electronic Science and Technology of China, Chengdu, 610072, China

    Yu-Mei Yang, Shu-Jin Guo, Yu-Ping Liu & Ping Shuai

  2. Department of Hematology, Sichuan Provincial People’s Hospital, University of Electronic Science and Technology of China, Chengdu, 610072, China

    Rong Xiao

  3. Department of Endocrinology and Metabolism, Laboratory of Endocrinology and Metabolism, West China Hospital of Sichuan University, Chengdu, 610041, China

    Xi-Jie Yu

Authors
  1. Yu-Mei Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shu-Jin Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rong Xiao
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xi-Jie Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yu-Ping Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ping Shuai
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

YYM and PS conceived of the study concept and design. YYM and SJG performed the literature search, study selection and collected all data. YYM and PS contributed to the data analysis and interpretation of results. YYM drafted the manuscript, RX, XJY, and YPL revised the manuscript critically for important intellectual content. All authors reviewed the manuscript and approved the final submitted version.

Corresponding authors

Correspondence to Yu-Ping Liu or Ping Shuai.

Ethics declarations

Competing interests

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

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yang, YM., Guo, SJ., Xiao, R. et al. Prevalence of osteoporosis among patients after stem cell transplantation: a systematic review and meta-analysis. Bone Marrow Transplant (2024). https://doi.org/10.1038/s41409-024-02243-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/s41409-024-02243-0

Search

Advanced search

Quick links