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:

Impact of body mass index at different transplantation stages on postoperative outcomes in patients with hematological malignancies: a meta-analysis

Abstract

Although the association between body mass index (BMI) and overall survival (OS) has been reported in leukemia patients of different ages, whether BMI levels at different stages of hematopoietic stem cell transplantation (HSCT) have different effects on postoperative survival remains controversial. We searched four electronic databases from inception through July 2017 without any language restrictions and included studies on different types of hematological malignancies reporting both BMI time points and HSCT. Of the 1420 articles identified, 26 articles were eligible for inclusion in this meta-analysis. Three weight groups (obese, overweight and underweight) were individually compared with the normal group. Summary risk estimates for OS and event-free survival (EFS) were calculated with random- or fixed-effects models. For BMI at the pre-HSCT stage, a statistically significant positive association of increased risk of OS (RR: 1.17; 95% CI: 1.08–1.27) and EFS (RR: 1.29; 95% CI: 1–1.67) was identified in underweight individuals compared with those with normal weights. For BMI in the HSCT stage, a lower BMI was significantly associated with poorer OS (RR: 1.34; 95% CI: 1.01–1.78) and EFS (RR: 1.53; 95% CI: 1.09–2.06) compared with a normal BMI. Our results indicated that lower BMI at the pre-HSCT stage or during HSCT is associated with poorer survival.

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

Access options

Buy this article

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Gomez Alvarez ME. [Parenteral nutrition in hematopoietic stem cell transplantation]. Farm Hosp. 2004;28:116–22.

    CAS  PubMed  Google Scholar 

  2. Martin-Salces M, de Paz R, Canales MA, Mesejo A, Hernandez-Navarro F. Nutritional recommendations in hematopoietic stem cell transplantation. Nutrition. 2008;24:769–75. https://doi.org/10.1016/j.nut.2008.02.021.

    Article  CAS  PubMed  Google Scholar 

  3. Garcia-Luna PP, Parejo Campos J, Pereira Cunill JL. [Causes and impact of hyponutrition and cachexia in the oncologic patient]. Nutr Hosp. 2006;21(Suppl 3):10–16.

    PubMed  Google Scholar 

  4. Lobato-Mendizabal E, Ruiz-Arguelles GJ, Marin-Lopez A. Leukaemia and nutrition. I: malnutrition is an adverse prognostic factor in the outcome of treatment of patients with standard-risk acute lymphoblastic leukaemia. Leuk Res. 1989;13:899–906.

    Article  CAS  Google Scholar 

  5. Sullivan DH. The role of nutrition in increased morbidity and mortality. Clin Geriatr Med. 1995;11:661–74.

    Article  CAS  Google Scholar 

  6. Calle EE, Rodriguez C, Walker-Thurmond K, Thun MJ. Overweight, obesity, and mortality from cancer in a prospectively studied cohort of U.S. adults. N Engl J Med. 2003;348:1625–38. https://doi.org/10.1056/NEJMoa021423.

    Article  PubMed  Google Scholar 

  7. Larsson SC, Wolk A. Overweight and obesity and incidence of leukemia: a meta-analysis of cohort studies. Int J Cancer. 2008;122:1418–21. https://doi.org/10.1002/ijc.23176.

    Article  CAS  PubMed  Google Scholar 

  8. Castillo JJ, Reagan JL, Ingham RR, Furman M, Dalia S, Merhi B, et al. Obesity but not overweight increases the incidence and mortality of leukemia in adults: a meta-analysis of prospective cohort studies. Leuk Res. 2012;36:868–75. https://doi.org/10.1016/j.leukres.2011.12.020.

    Article  PubMed  Google Scholar 

  9. Orgel E, Genkinger JM, Aggarwal D, Sung L, Nieder M, Ladas EJ. Association of body mass index and survival in pediatric leukemia: a meta-analysis. Am J Clin Nutr. 2016;103:808–17. https://doi.org/10.3945/ajcn.115.124586.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Gelelete CB, Pereira SH, Azevedo AM, Thiago LS, Mundim M, Land MG, et al. Overweight as a prognostic factor in children with acute lymphoblastic leukemia. Obes (Silver Spring). 2011;19:1908–11. https://doi.org/10.1038/oby.2011.195.

    Article  Google Scholar 

  11. Hijiya N, Panetta JC, Zhou Y, Kyzer EP, Howard SC, Jeha S, et al. Body mass index does not influence pharmacokinetics or outcome of treatment in children with acute lymphoblastic leukemia. Blood. 2006;108:3997–4002. https://doi.org/10.1182/blood-2006-05-024414.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Aldhafiri FK, McColl JH, Reilly JJ. Prognostic significance of being overweight and obese at diagnosis in children with acute lymphoblastic leukemia. J Pediatr Hematol Oncol. 2014;36:234–6. https://doi.org/10.1097/MPH.0000000000000056.

    Article  PubMed  Google Scholar 

  13. Baillargeon J, Langevin AM, Lewis M, Estrada J, Mullins J, Pitney A, et al. Obesity and survival in a cohort of predominantly Hispanic children with acute lymphoblastic leukemia. J Pediatr Hematol Oncol. 2006;28:575–8. https://doi.org/10.1097/01.mph.0000212985.33941.d8.

    Article  PubMed  Google Scholar 

  14. Nikolousis E, Nagra S, Paneesha S, Delgado J, Holder K, Bratby L, et al. Allogeneic transplant outcomes are not affected by body mass index (BMI) in patients with haematological malignancies. Ann Hematol. 2010;89:1141–5. https://doi.org/10.1007/s00277-010-1001-6.

    Article  PubMed  Google Scholar 

  15. Jaime-Perez JC, Colunga-Pedraza PR, Gutierrez-Gurrola B, Brito-Ramirez AS, Gutierrez-Aguirre H, Cantu-Rodriguez OG, et al. Obesity is associated with higher overall survival in patients undergoing an outpatient reduced-intensity conditioning hematopoietic stem cell transplant. Blood Cells Mol Dis. 2013;51:61–65.

    Article  Google Scholar 

  16. Amankwah EK, Saenz AM, Hale GA, Brown PA. Association between body mass index at diagnosis and pediatric leukemia mortality and relapse: a systematic review and meta-analysis. Leuk Lymphoma. 2016;57:1140–8. https://doi.org/10.3109/10428194.2015.1076815.

    Article  PubMed  Google Scholar 

  17. Nakao M, Chihara D, Niimi A, Ueda R, Tanaka H, Morishima Y, et al. Impact of being overweight on outcomes of hematopoietic SCT: a meta-analysis. Bone Marrow Transplant. 2014;49:66–72. https://doi.org/10.1038/bmt.2013.128.

    Article  CAS  PubMed  Google Scholar 

  18. Larsson SC, Wolk A. Obesity and risk of non-Hodgkin’s lymphoma: a meta-analysis. Int J Cancer. 2007;121:1564–70. https://doi.org/10.1002/ijc.22762.

    Article  CAS  PubMed  Google Scholar 

  19. Moher D, Shamseer L, Clarke M, Ghersi D, Liberati A, Petticrew M, et al. Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015 statement. Syst Rev. 2015;4:1 https://doi.org/10.1186/2046-4053-4-1.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Navarro WH, Loberiza FR Jr., Bajorunaite R, van Besien K, Vose JM, Lazarus HM, et al. Effect of body mass index on mortality of patients with lymphoma undergoing autologous hematopoietic cell transplantation. Biol Blood Marrow Transplant: J Am Soc Blood Marrow Transplant. 2006;12:541–51.

    Article  Google Scholar 

  21. Navarro WH, Agovi MA, Logan BR, Ballen K, Bolwell BJ, Frangoul H, et al. Obesity does not preclude safe and effective myeloablative hematopoietic cell transplantation (HCT) for acute myelogenous leukemia (AML) in adults. Biol Blood Marrow Transplant. 2010;16:1442–50. https://doi.org/10.1016/j.bbmt.2010.04.009.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Vogl DT, Wang T, Pérez WS, Stadtmauer EA, Heitjan DF, Lazarus HM, et al. Effect of obesity on outcomes after autologous hematopoietic stem cell transplantation for multiple myeloma. Biol Blood Marrow Transplant. 2011;17:1765–74. https://doi.org/10.1016/j.bbmt.2011.05.005.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Lee HJ, Licht AS, Hyland AJ, Ford LA, Sait SNJ, Block AW, et al. Is obesity a prognostic factor for acute myeloid leukemia outcome? Ann Hematol. 2012;91:359–65. https://doi.org/10.1007/s00277-011-1319-8.

    Article  PubMed  Google Scholar 

  24. Sucak GT, Suyan IE, Baysal NA, AltIndal Ş, Çakar MK, Ak IŞZ, et al. The role of body mass index and other body composition parameters in early post-transplant complications in patients undergoing allogeneic stem cell transplantation with busulfan-cyclophosphamide conditioning. Int J Hematol. 2012;95:95–101. https://doi.org/10.1007/s12185-011-0980-y.

    Article  CAS  PubMed  Google Scholar 

  25. Fuji S, Takano K, Mori T, Eto T, Taniguchi S, Ohashi K, et al. Impact of pretransplant body mass index on the clinical outcome after allogeneic hematopoietic SCT. Bone Marrow Transplant. 2014;49:1505–12. https://doi.org/10.1038/bmt.2014.178.

    Article  CAS  PubMed  Google Scholar 

  26. Gleimer M, Li Y, Chang L, Paczesny S, Hanauer DA, Frame DG, et al. Baseline body mass index among children and adults undergoing allogeneic hematopoietic cell transplantation: clinical characteristics and outcomes. Bone Marrow Transplant. 2015;50:402–10. https://doi.org/10.1038/bmt.2014.280.

    Article  CAS  PubMed  Google Scholar 

  27. Lau JE, Weber C, Earl M, Rybicki LA, Carlstrom KD, Wenzell CM, et al. Outcomes after autologous SCT in lymphoma patients grouped by weight. Bone Marrow Transplant. 2015;50:652–7. https://doi.org/10.1038/bmt.2014.327.

    Article  CAS  PubMed  Google Scholar 

  28. Yang J, Xue SL, Zhang X, Zhou YN, Qin LQ, Shen YP, et al. Effect of body mass index on overall survival of patients with allogeneic hematopoietic stem cell transplantation. Eur J Clin Nutr. 2017;71:750–4. https://doi.org/10.1038/ejcn.2016.225.

    Article  CAS  PubMed  Google Scholar 

  29. Le Blanc K, Ringden O, Remberger M. A low body mass index is correlated with poor survival after allogeneic stem cell transplantation. Haematologica. 2003;88:1044–52.

    PubMed  Google Scholar 

  30. Baumgartner A, Zueger N, Bargetzi A, Medinger M, Passweg JR, Stanga Z, et al. Association of nutritional parameters with clinical outcomes in patients with acute myeloid leukemia undergoing haematopoietic stem cell transplantation. Ann Nutr Metab. 2016;69:89–98. https://doi.org/10.1159/000449451.

    Article  CAS  PubMed  Google Scholar 

  31. Hadjibabaie M, Tabeefar H, Alimoghaddam K, Iravani M, Eslami K, Honarmand H, et al. The relationship between body mass index and outcomes in leukemic patients undergoing allogeneic hematopoietic stem cell transplantation. Clin Transplant. 2012;26:149–55. https://doi.org/10.1111/j.1399-0012.2011.01445.x.

    Article  PubMed  Google Scholar 

  32. Dietrich S, Radujkovic A, Stolzel F, Falk CS, Benner A, Schaich M, et al. Pretransplant metabolic distress predicts relapse of acute myeloid leukemia after allogeneic stem cell transplantation. Transplantation. 2015;99:1065–71. https://doi.org/10.1097/TP.0000000000000471.

    Article  CAS  PubMed  Google Scholar 

  33. Meloni G, Proia A, Capria S, Romano A, Trape G, Trisolini SM, et al. Obesity and autologous stem cell transplantation in acute myeloid leukemia. Bone Marrow Transplant. 2001;28:365–7.

    Article  CAS  Google Scholar 

  34. Urbain P, Birlinger J, Ihorst G, Biesalski H-K, Finke J, Bertz H. Body mass index and bioelectrical impedance phase angle as potentially modifiable nutritional markers are independent risk factors for outcome in allogeneic hematopoietic cell transplantation. Ann Hematol. 2013;92:111–9.

    Article  Google Scholar 

  35. Bulley S, Gassas A, Dupuis LL, Aplenc R, Beyene J, Greenberg ML, et al. Inferior outcomes for overweight children undergoing allogeneic stem cell transplantation. Br J Haematol. 2008;140:214–7.

    PubMed  Google Scholar 

  36. Barker CC, Agovi MA, Logan B, Lazarus HM, Ballen KK, Gupta V, et al. Childhood obesity and outcomes after bone marrow transplantation for patients with severe aplastic anemia. Biol Blood Marrow Transplant: J Am Soc Blood Marrow Transplant. 2011;17:737–44. https://doi.org/10.1016/j.bbmt.2010.08.019. e-pub ahead of print 2010/09/08.

    Article  Google Scholar 

  37. Aplenc R, Zhang MJ, Sung L, Zhu X, Ho VT, Cooke K, et al. Effect of body mass in children with hematologic malignancies undergoing allogeneic bone marrow transplantation. Blood. 2014;123:3504–11. https://doi.org/10.1182/blood-2013-03-490334.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Pine M, Wang L, Harrell FE Jr., Calder C, Manes B, Evans M, et al. The effect of obesity on outcome of unrelated cord blood transplant in children with malignant diseases. Bone Marrow Transplant. 2011;46:1309–13.

    Article  CAS  Google Scholar 

  39. Hoffmeister PA, Storer BE, Macris PC, Carpenter PA, Baker KS. Relationship of body mass index and arm anthropometry to outcomes after pediatric allogeneic hematopoietic cell transplantation for hematologic malignancies. Biol Blood Marrow Transplant. 2013;19:1081–6. https://doi.org/10.1016/j.bbmt.2013.04.017.

    Article  PubMed  Google Scholar 

  40. Radujkovic A, Becker N, Benner A, Penack O, Platzbecker U, Stolzel F, et al. Pre-transplant weight loss predicts inferior outcome after allogeneic stem cell transplantation in patients with myelodysplastic syndrome. Oncotarget. 2015;6:35095–106. https://doi.org/10.18632/oncotarget.4805. e-pub ahead of print 2015/09/12.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Fuji S, Mori T, Khattry N, Cheng J, Do YR, Yakushijin K, et al. Severe weight loss in 3 months after allogeneic hematopoietic SCT was associated with an increased risk of subsequent non-relapse mortality. Bone Marrow Transplant. 2015;50:100–5. https://doi.org/10.1038/bmt.2014.228.

    Article  CAS  PubMed  Google Scholar 

  42. White M, Murphy AJ, Hallahan A, Ware RS, Fraser C, Davies PSW. Survival in overweight and underweight children undergoing hematopoietic stem cell transplantation. Eur J Clin Nutr. 2012;66:1120–3. https://doi.org/10.1038/ejcn.2012.109.

    Article  CAS  PubMed  Google Scholar 

  43. Fleming DR, Rayens MK, Garrison J. Impact of obesity on allogeneic stem cell transplant patients: a matched case-controlled study. Am J Med. 1997;102:265–8. https://doi.org/10.1016/S0002-9343(96)00450-0.

    Article  CAS  PubMed  Google Scholar 

  44. Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ. 2003;327:557–60. https://doi.org/10.1136/bmj.327.7414.557.

    Article  PubMed  PubMed Central  Google Scholar 

  45. McClune BL, Weisdorf DJ, Pedersen TL, Tunes da Silva G, Tallman MS, Sierra J, et al. Effect of age on outcome of reduced-intensity hematopoietic cell transplantation for older patients with acute myeloid leukemia in first complete remission or with myelodysplastic syndrome. J Clin Oncol. 2010;28:1878–87. https://doi.org/10.1200/JCO.2009.25.4821.

    Article  PubMed  PubMed Central  Google Scholar 

  46. Sengsayadeth S, Savani BN, Blaise D, Malard F, Nagler A, Mohty M. Reduced intensity conditioning allogeneic hematopoietic cell transplantation for adult acute myeloid leukemia in complete remission—a review from the Acute Leukemia Working Party of the EBMT. Haematologica. 2015;100:859–69. https://doi.org/10.3324/haematol.2015.123331.

    Article  PubMed  PubMed Central  Google Scholar 

  47. Prospective Studies C, Whitlock G, Lewington S, Sherliker P, Clarke R, Emberson J, et al. Body-mass index and cause-specific mortality in 900 000 adults: collaborative analyses of 57 prospective studies. Lancet. 2009;373:1083–96. https://doi.org/10.1016/S0140-6736(09)60318-4.

    Article  Google Scholar 

  48. He J, McGee D, Niu X, Choi W. Examining the dynamic association of BMI and mortality in the Framingham Heart Study. Int J Environ Res Public Health. 2009;6:3115–26. https://doi.org/10.3390/ijerph6123115.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank the anonymous reviewers for their helpful suggestions. This work was supported by the National Natural Science Foundation of China (no. 81703221 to GR) and the Special Fund for Basic Scientific Research (no. 1610422016003 to GR and no. 1610422017007 to GR). ORCID profile (Dr. Guangxu Ren): 0000-0003-2378-260×.

Author contributions

GR designed the research. GR and WC conducted the research. SY, LW, LL, JH and JW analyzed the data. GR drafted the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Guangxu Ren.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ren, G., Cai, W., Wang, L. et al. Impact of body mass index at different transplantation stages on postoperative outcomes in patients with hematological malignancies: a meta-analysis. Bone Marrow Transplant 53, 708–721 (2018). https://doi.org/10.1038/s41409-018-0234-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41409-018-0234-1

This article is cited by

Search

Quick links