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  • Review Article
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Effects of smoking on outcomes of hematopoietic cell transplantation: a systemic review and future directions

Abstract

Hematopoietic cell transplantation (HCT) survivors are at risk of increased mortality compared to the general population. Smoking by HCT survivors has been reported to impact a variety of health outcomes, resulting in an increased risk for infections, cardio-pulmonary diseases, and cancer. The purpose of our study was to conduct a systematic literature search to determine the relationship between tobacco smoking pre-HCT and post-HCT outcomes. We conducted an electronic literature search from all languages from multiple peer-reviewed databases of studies that evaluated the effects of tobacco smoking prior to HCT on clinical outcomes. Data were extracted from the studies according to a strict selection criterion. Due to differences in primary endpoint and different populations evaluated in different studies, a meta-analysis was not possible, and a descriptive quantitative analysis is provided. Out of the 447 publications fulfilling the selection criteria for the electronic search, 17 articles were included in the final sample. The studies varied in terms of study design, patient characteristics, and HCT type. Considerable variability in definition of smoking was observed. We found that smoking pre-HCT was associated with a higher incidence of cardiovascular diseases, new infections, pulmonary complications, and cancers in comparison to non-smokers. Moreover, smoking pre-HCT was significantly associated with increased risks of both relapse and non-relapse mortality, and inversely related to median overall survival. Smoking adversely affects mortality in all HCT survivors by increasing the risks of both malignant and non-malignant complications. Thus, guidelines are urgently needed to formulate lifestyle factor modifications for HCT survivors focusing on smoking cessation strategies and abstinence maintenance in former smokers. Given the strength of these findings, guidelines should include systematic definitions of smoking for use in clinical trials as well as in standardized data reporting.

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References

  1. http://www.who.int/mediacentre/factsheets/fs339/en/. Accessed 30 Jan 2018.

  2. U.S. Department of Health and Human Services. The Health Consequences of Smoking—50 Years of Progress: A Report of the Surgeon General. Atlanta: U.S. Department of Health and Human Services, Centers for Disease Control and Prevention, National Center for Chronic Disease Prevention and Health Promotion, Office on Smoking and Health; 2014.

  3. Xu X, Bishop EE, Kennedy SM, Simpson SA, Pechacek TF. Annual healthcare spending attributable to cigarette smoking: an update. Am J Prev Med. 2015;48:326–33.

    Article  Google Scholar 

  4. https://www.cdc.gov/tobacco/about/osh/index.htm. Accessed 14 Jan 2018.

  5. Jha P, Ramasundarahettige C, Landsman V, Rostron B, Thun M, Anderson RN, et al. 21st-century hazards of smoking and benefits of cessation in the United States. New Engl J Med. 2013;368:341–50.

    Article  CAS  Google Scholar 

  6. Gooley TA, Chien JW, Pergam SA, Hingorani S, Sorror ML, Boeckh M, et al. Reduced mortality after allogeneic hematopoietic-cell transplantation. New Engl J Med. 2010;363:2091–101.

    Article  CAS  Google Scholar 

  7. Ehlers SL, Bronars CA, Patten CA, Brockman T, Hughes C, Decker PA, et al. Accuracy of self-reported tobacco use status among hematopoietic SCT patients. Bone Marrow Transplant. 2014;49:961.

    Article  CAS  Google Scholar 

  8. Bishop MM, Lee SJ, Beaumont JL, Andrykowski MA, Rizzo JD, Sobocinski KA. The preventive health behaviors of long-term survivors of cancer and hematopoietic stem cell transplantation compared with matched controls. Biol Blood Marrow Transplant. 2010;16:207–14.

    Article  Google Scholar 

  9. Marks DI, Ballen K, Logan BR, Wang Z, Sobocinski KA, Bacigalupo, et al. The effect of smoking on allogeneic transplant outcomes. Biol Blood Marrow Transplant. 2009;15:1277–87.

    Article  CAS  Google Scholar 

  10. Majhail NS, Brazauskas R, Rizzo JD, Sobecks RM, Wang Z, Horowitz MM. et al. Secondary solid cancers after allogeneic hematopoietic cell transplantation using busulfan-cyclophosphamide conditioning. Blood. 2011;117:316–22.

    Article  CAS  Google Scholar 

  11. Majhail N, Rizzo J, Lee S, Aljurf M, Atsuta Y, Bonfim C, et al. Recommended screening and preventive practices for long-term survivors after hematopoietic cell transplantation. Bone Marrow Transplant. 2012;47:337–41.

    Article  CAS  Google Scholar 

  12. Chow EJ, Wong K, Lee SJ, Cushing-Haugen KL, Flowers ME, Friedman DL, et al. Late cardiovascular complications after hematopoietic cell transplantation. Biol Blood Marrow Transplant. 2014;20:794–800.

    Article  Google Scholar 

  13. Tichelli A, Passweg J, Wójcik D, Rovó A, Harousseau JL, Masszi T, et al. Late cardiovascular events after allogeneic hematopoietic stem cell transplantation: a retrospective multicenter study of the Late Effects Working Party of the European Group for Blood and Marrow Transplantation. Haematologica. 2008;93:1203–10.

    Article  Google Scholar 

  14. Qazilbash MH, Amjad AI, Qureshi S, Qureshi SR, Saliba RM, Khan ZU, et al. Outcome of allogeneic hematopoietic stem cell transplantation in patients with low left ventricular ejection fraction. Biol Blood Marrow Transplant. 2009;15:1265–70.

    Article  Google Scholar 

  15. Miceli MH, Dong L, Grazziutti ML, Fassas A, Thertulien R, Van Rhee F, et al. Iron overload is a major risk factor for severe infection after autologous stem cell transplantation: a study of 367 myeloma patients. Bone Marrow Transplant. 2006;37:857.

    Article  CAS  Google Scholar 

  16. Hanajiri R, Kakihana K, Kobayashi T, Doki N, Sakamaki H, Ohashi K. Tobacco smoking is associated with infectious pulmonary complications after allogeneic hematopoietic stem cell transplantation. Bone Marrow Transplant. 2015;50:1141–3.

    Article  CAS  Google Scholar 

  17. Ehlers SL, Gastineau DA, Patten CA, Decker PA, Rausch SM, Cerhan, et al. The impact of smoking on outcomes among patients undergoing hematopoietic SCT for the treatment of acute leukemia. Bone Marrow Transplant. 2011;46:285.

    Article  CAS  Google Scholar 

  18. Savani BN, Montero A, Wu C, Nlonda N, Read E, Dunbar C, et al. Prediction and prevention of transplant-related mortality from pulmonary causes after total body irradiation and allogeneic stem cell transplantation. Biol Blood Marrow Transplant. 2005;11:223–30.

    Article  Google Scholar 

  19. Tran BT, Halperin A, Chien JW. Cigarette smoking and outcomes after allogeneic hematopoietic stem cell transplantation. Biol Blood Marrow Transplant. 2011;17:1004–11.

    Article  CAS  Google Scholar 

  20. Ho VT, Weller E, Lee SJ, Alyea EP, Antin JH, Soiffer RJ. Prognostic factors for early severe pulmonary complications after hematopoietic stem cell transplantation. Biol blood Marrow Transplant. 2001;7:223–30.

    Article  CAS  Google Scholar 

  21. Mawardi H, Elad S, Correa ME, Stevenson K, Woo SB, Almazrooa S, et al. Oral epithelial dysplasia and squamous cell carcinoma following allogeneic hematopoietic stem cell transplantation: clinical presentation and treatment outcomes. Bone Marrow Transplant. 2011;46:884.

    Article  CAS  Google Scholar 

  22. Shah AT, Wu E, Wein RO. Oral squamous cell carcinoma in post-transplant patients. Am J Otolaryngol. 2013;34:176–9.

    Article  Google Scholar 

  23. Chang G, John Orav E, McNamara T, Tong MY, Antin JH. Depression, cigarette smoking, and hematopoietic stem cell transplantation outcome. Cancer. 2004;101:782–9.

    Article  Google Scholar 

  24. Mo X, Zhang X, Xu L, Wang Y, Yan C, Chen H, et al. Late-onset severe pneumonia after allogeneic hematopoietic stem cell transplantation: prognostic factors and treatments. Transplant Infect Dis. 2016;18:492–503.

    Article  CAS  Google Scholar 

  25. Goodchild M, Nargis N, d’Espaignet ET. Global economic cost of smoking-attributable diseases. Tob Control. 2018;27:58–64.

    Article  Google Scholar 

  26. Mehdi A, Rybicki L, Mossad S, Yurch M, Sekeres M, Gerds AT, et al. Impact of cigarette smoking on survival after myeloablative allogeneic hematopoietic stem cell transplantation and contribution of invasive fungal infection. Bone Marrow Transplant. 2017;52:1665.

    Article  CAS  Google Scholar 

  27. Stenehjem JS, Smeland KB, Murbraech K, Holte H, Kvaløy SO, Wethal T, et al. Obstructive and restrictive pulmonary dysfunction in long-term lymphoma survivors after high-dose therapy with autologous stem cell transplantation. Acta Oncol. 2018;57:773–81.

    Article  Google Scholar 

  28. Jacob L, Freyn M, Kalder M, Dinas K, Kostev K. Impact of tobacco smoking on the risk of developing 25 different cancers in the UK: a retrospective study of 422,010 patients followed for up to 30 years. Oncotarget . 2018;9:17420.

    Article  Google Scholar 

  29. Zhou X, Nonnemaker J, Sherrill B, Gilsenan AW, Coste F, West R. Attempts to quit smoking and relapse: factors associated with success or failure from the ATTEMPT cohort study. Addict Behav. 2009;34:365–73.

    Article  Google Scholar 

  30. National comprehensive cancer network (NCCN). Clinical Practice Guidelines in Oncology (NCCN Guidelines®) for Smoking Cessation (2015). https://www.nccn.org/professionals/physician_gls/pdf/smoking.pdf. Accessed 18 Jan 2018.

  31. American Society of Clinical Oncology (ASCO). Tobacco cessation guide (2012). https://www.asco.org/sites/new-www.asco.org/files/content-files/blog-release/documents/tobacco-cessation-guide.pdf. Accessed 21 January 2018.

  32. United States Preventive Services Task Force (USPSTF). Tobacco smoking cessation published recommendation (2015). https://www.uspreventiveservicestaskforce.org/Page/Document/UpdateSummaryFinal/tobacco-use-in-adults-and-pregnant-women-counseling-and-interventions1. Accessed 21 Jan 2018.

  33. http://tgapp.asbmt.org/#/article-content-recommended-screening-page. Accessed 8 Dec 2018.

  34. Schlemmer F, Chevret S, Lorillon G, De Bazelaire C, Peffault de Latour R, Meignin V, et al. Late-onset noninfectious interstitial lung disease after allogeneic hematopoietic stem cell transplantation. Respir Med. 2014;108:1525–33.

    Article  Google Scholar 

  35. Santo Tomas LH, Loberiza FR,Jr, Klein JP, Layde PM, Lipchik RJ, Rizzo JD. et al. Risk factors for bronchiolitis obliterans in allogeneic hematopoietic stem-cell transplantation for leukemia. Chest . 2005;128:153–61.

    Article  Google Scholar 

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SKH and MA wrote the first draft of the manuscript. All authors contributed substantially to the conception, acquisition, analysis, and interpretation of the data for the work.

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Correspondence to Shahrukh K. Hashmi.

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Abufarhaneh, M., Ehlers, S.L., Burns, L.J. et al. Effects of smoking on outcomes of hematopoietic cell transplantation: a systemic review and future directions. Bone Marrow Transplant 54, 1382–1390 (2019). https://doi.org/10.1038/s41409-019-0485-5

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