The survival rates of patients undergoing allogeneic hematopoietic stem cell transplantation (HSCT) have improved. However, HSCT can induce significant long-term complications. Therefore, we investigated the late complications and risk factors for quality of life (QOL) post-HSCT.
We retrospectively analyzed 67 adult survivors over 2 years after HSCT between 2015 and 2018 at Ulsan University Hospital, Ulsan, Korea. The survey data including FACT-BMT, Hospital Anxiety and Depression Scale, and NCCN Distress Thermometer were collected as patient-reported outcomes using a tablet PC during a routine practice of survivorship clinic.
The median age was 46 years. The most common symptom was fatigue (80.6%). Younger age (< 60 years), acute lymphoblastic leukemia (ALL), chronic graft-versus-host disease (GVHD), and immunosuppressant use were significantly associated with worse QOL and depression. Additionally, younger survivors (< 60 years) showed significantly more fatigue and anxiety compared with elderly survivors (≥ 60 years). Female sex was significantly associated with lower physical well-being and higher distress than male sex.
Younger patients (< 60 years), female, ALL, chronic GVHD, and continuous immunosuppressant use were significant risk factors for worse QOL and depression. Hence, creating a more active survivorship care plan after HSCT, specifically for these patients, is required.
This is a preview of subscription content, log in to check access.
Buy single article
Instant access to the full article PDF.
Price includes VAT for USA
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
This is the net price. Taxes to be calculated in checkout.
Allogeneic hematopoietic stem cell transplantation
Quality of life
Functional Assessment of Cancer Therapy-Bone Marrow Transplantation
Bone Marrow Transplantation Subscale
Hospital Anxiety and Depression Scale
- NCCN DT:
National Comprehensive Cancer Network’s Distress Thermometer
Brief Pain Inventory
Acute myeloid leukemia
Acute lymphoblastic leukemia
Reduced intensity conditioning
Total Outcome Index
Majhail NS, Farnia SH, Carpenter PA, Champlin RE, Crawford S, Marks DI, Omel JL, Orchard PJ, Palmer J, Saber W, Savani BN, Veys PA, Bredeson CN, Giralt SA, LeMaistre CF (2015) Indications for autologous and allogeneic hematopoietic cell transplantation: guidelines from the American Society for Blood and Marrow Transplantation. Biol Blood Marrow Transplant 21:1863–1869. https://doi.org/10.1016/j.bbmt.2015.07.032
Martin PJ, Counts GW Jr, Appelbaum FR, Lee SJ, Sanders JE, Deeg HJ, Flowers MED, Syrjala KL, Hansen JA, Storb RF, Storer BE (2010) Life expectancy in patients surviving more than 5 years after hematopoietic cell transplantation. J Clin Oncol 28:1011–1016. https://doi.org/10.1200/JCO.2009.25.6693
Wingard JR, Majhail NS, Brazauskas R, Wang Z, Sobocinski KA, Jacobsohn D, Sorror ML, Horowitz MM, Bolwell B, Rizzo JD, Socié G (2011) Long-term survival and late deaths after allogeneic hematopoietic cell transplantation. J Clin Oncol 29:2230–2239. https://doi.org/10.1200/JCO.2010.33.7212
Syrjala KL, Martin PJ, Lee SJ (2012) Delivering care to long-term adult survivors of hematopoietic cell transplantation. J Clin Oncol 30:3746–3751. https://doi.org/10.1200/JCO.2012.42.3038
Majhail NS (2017) Long-term complications after hematopoietic cell transplantation. Hematol Oncol Stem Cell Ther 10:220–227. https://doi.org/10.1016/j.hemonc.2017.05.009
Savani BN, Griffith ML, Jagasia S, Lee SJ (2011) How I treat late effects in adults after allogeneic stem cell transplantation. Blood 117:3002–3009. https://doi.org/10.1182/blood-2010-10-263095
Matthes-Martin S, Potschger U, Barr R et al (2012) Costs and cost-effectiveness of allogeneic stem cell transplantation in children are predictable. Biol Blood Marrow Transplant 18:1533–1539. https://doi.org/10.1016/j.bbmt.2012.04.002
Inamoto Y, Valdes-Sanz N, Ogawa Y et al (2019) Ocular graft-versus-host disease after hematopoietic cell transplantation: expert review from the Late Effects and Quality of Life Working Committee of the Center for International Blood and Marrow Transplant Research and Transplant Complications Working Party of the European Society of Blood and Marrow Transplantation. Biol Blood Marrow Transplant 25:e46–e54. https://doi.org/10.1016/j.bbmt.2018.11.021
Kurosawa S, Yamaguchi T, Oshima K, Yanagisawa A, Fukuda T, Kanamori H, Mori T, Takahashi S, Kondo T, Kohno A, Miyamura K, Umemoto Y, Teshima T, Taniguchi S, Yamashita T, Inamoto Y, Kanda Y, Okamoto S, Atsuta Y (2019) Resolved versus active chronic graft-versus-host disease: impact on post-transplantation quality of life. Biol Blood Marrow Transplant 25:1851–1858. https://doi.org/10.1016/j.bbmt.2019.05.016
Hayakawa J, Miyamura D, Kimura SI, Gomyo A, Tamaki M, Akahoshi Y, Harada N, Ugai T, Kusuda M, Kameda K, Wada H, Ishihara Y, Kawamura K, Sakamoto K, Sato M, Terasako-Saito K, Kikuchi M, Nakasone H, Kako S, Kanda Y (2019) Negative impact of chronic graft-versus-host disease and glucocorticoid on the recovery of physical function after allogeneic hematopoietic stem cell transplantation. Bone Marrow Transplant 54:994–1003. https://doi.org/10.1038/s41409-018-0365-4
Zajac-Spychala O, Pieczonka A, Baranska M, Wachowiak J (2019) Long-term recipient health-related quality of life and donor-recipient relationship following sibling pediatric hematopoietic stem cell transplantation. Biol Blood Marrow Transplant 26:401–406. https://doi.org/10.1016/j.bbmt.2019.10.009
Agh T, Csanadi M, Voko Z, Webb T, Jeyakumaran D, Trudeau J, Sengupta N, Schain F, Mattsson J (2019) Humanistic burden of patients with chronic graft-versus-host disease - systematic literature review of health-related quality of life and functional status. Expert Rev Hematol 12:295–309. https://doi.org/10.1080/17474086.2019.1602036
Gupta V, Panzarella T, Li L, Khan J, Sharma A, Lipton JH, Kuruvilla J, Messner H, Alibhai SMH (2012) A prospective study comparing the outcomes and health-related quality of life in adult patients with myeloid malignancies undergoing allogeneic transplantation using myeloablative or reduced-intensity conditioning. Biol Blood Marrow Transplant 18:113–124. https://doi.org/10.1016/j.bbmt.2011.05.022
Andersson I, Ahlberg K, Stockelberg D, Brune M, Persson LO (2009) Health-related quality of life in patients undergoing allogeneic stem cell transplantation after reduced intensity conditioning versus myeloablative conditioning. Cancer Nurs 32:325–334. https://doi.org/10.1097/NCC.0b013e31819b5c81
Yoo H, Lee K, Lee J, Eremenco S, Choi S, Kim H, Lee J (2006) Korean translation and validity of FACT-BMT version 4 and the quality of life in allogeneic bone marrow transplantation patients. Qual Life Res 15:559–564. https://doi.org/10.1007/s11136-005-1769-3
McQuellon RP, Russell GB, Cella DF, Craven BL, Brady M, Bonomi A, Hurd DD (1997) Quality of life measurement in bone marrow transplantation: development of the Functional Assessment of Cancer Therapy-Bone Marrow Transplant (FACT-BMT) scale. Bone Marrow Transplant 19:357–368. https://doi.org/10.1038/sj.bmt.1700672
Zigmond AS, Snaith RP (1983) The hospital anxiety and depression scale. Acta Psychiatr Scand 67:361–370. https://doi.org/10.1111/j.1600-0447.1983.tb09716.x
Oh SMMK, Park DB (1999) A study on the standardization of the hospital anxiety and depression scale for Koreans:a comparison of normal, depressed and anxious groups. J Korean Neuropsychiatr Assoc 38:289–296
Network NCC (2013) NCCN clinical practice guidelines in oncology: distress management version 1.
Yun YH, Wang XS, Lee JS, Roh JW, Lee CG, Lee WS, Lee KS, Bang SM, Mendoza TR, Cleeland CS (2005) Validation study of the Korean version of the brief fatigue inventory. J Pain Symptom Manag 29:165–172. https://doi.org/10.1016/j.jpainsymman.2004.04.013
Butt Z, Wagner LI, Beaumont JL, Paice JA, Peterman AH, Shevrin D, von Roenn JH, Carro G, Straus JL, Muir JC, Cella D (2008) Use of a single-item screening tool to detect clinically significant fatigue, pain, distress, and anorexia in ambulatory cancer practice. J Pain Symptom Manag 35:20–30. https://doi.org/10.1016/j.jpainsymman.2007.02.040
Kumar A, Mhaskar AR, Reljic T, Mhaskar RS, Kharfan-Dabaja MA, Anasetti C, Mohty M, Djulbegovic B (2012) Antithymocyte globulin for acute-graft-versus-host-disease prophylaxis in patients undergoing allogeneic hematopoietic cell transplantation: a systematic review. Leukemia 26:582–588. https://doi.org/10.1038/leu.2011.349
Bhatia S, Francisco L, Carter A, Sun CL, Baker KS, Gurney JG, McGlave PB, Nademanee A, O'Donnell M, Ramsay NKC, Robison LL, Snyder D, Stein A, Forman SJ, Weisdorf DJ (2007) Late mortality after allogeneic hematopoietic cell transplantation and functional status of long-term survivors: report from the bone marrow transplant survivor study. Blood 110:3784–3792. https://doi.org/10.1182/blood-2007-03-082933
Clavert A, Peric Z, Brissot E, Malard F, Guillaume T, Delaunay J, Dubruille V, le Gouill S, Mahe B, Gastinne T, Blin N, Harousseau JL, Moreau P, Milpied N, Mohty M, Chevallier P (2017) Late complications and quality of life after reduced-intensity conditioning allogeneic stem cell transplantation. Biol Blood Marrow Transplant 23:140–146. https://doi.org/10.1016/j.bbmt.2016.10.011
Bevans MF, Marden S, Leidy NK, Soeken K, Cusack G, Rivera P, Mayberry H, Bishop MR, Childs R, Barrett AJ (2006) Health-related quality of life in patients receiving reduced-intensity conditioning allogeneic hematopoietic stem cell transplantation. Bone Marrow Transplant 38:101–109. https://doi.org/10.1038/sj.bmt.1705406
Bonifazi F, Solano C, Wolschke C, Sessa M, Patriarca F, Zallio F, Nagler A, Selleri C, Risitano AM, Messina G, Bethge W, Herrera P, Sureda A, Carella AM, Cimminiello M, Guidi S, Finke J, Sorasio R, Ferra C, Sierra J, Russo D, Benedetti E, Milone G, Benedetti F, Heinzelmann M, Pastore D, Jurado M, Terruzzi E, Narni F, Völp A, Ayuk F, Ruutu T, Kröger N (2019) Acute GVHD prophylaxis plus ATLG after myeloablative allogeneic haemopoietic peripheral blood stem-cell transplantation from HLA-identical siblings in patients with acute myeloid leukaemia in remission: final results of quality of life and long-term outcome analysis of a phase 3 randomised study. Lancet Haematol 6:e89–e99. https://doi.org/10.1016/S2352-3026(18)30214-X
D'Souza A ZX (2016) Current uses and outcomes of hematopoietic stem cell transplantation (HCT): CIBMTR summary slides.
Schumacher A, Sauerland C, Silling G, Berdel WE, Stelljes M, Koch R (2017) Development of quality of life in patients undergoing allogeneic stem cell transplantation with regard to anxiety, depression and resilience. Bone Marrow Transplant 52:1334–1337. https://doi.org/10.1038/bmt.2017.123
Sivertsen H, Bjorklof GH, Engedal K, Selbaek G, Helvik AS (2015) Depression and quality of life in older persons: a review. Dement Geriatr Cogn Disord 40:311–339. https://doi.org/10.1159/000437299
Mohammed J, Smith SR, Burns L, Basak G, Aljurf M, Savani BN, Schoemans H, Peric Z, Chaudhri NA, Chigbo N, Alfred A, Bakhsh H, Salooja N, Chris Chim A, Hashmi SK (2019) Role of physical therapy before and after hematopoietic stem cell transplantation: white paper report. Biol Blood Marrow Transplant 25:e191–e198. https://doi.org/10.1016/j.bbmt.2019.01.018
Prieto JM, Atala J, Blanch J, Carreras E, Rovira M, Cirera E, Espinal A, Gasto C (2005) Role of depression as a predictor of mortality among cancer patients after stem-cell transplantation. J Clin Oncol 23:6063–6071. https://doi.org/10.1200/jco.2005.05.751
Dirou S, Chambellan A, Chevallier P, Germaud P, Lamirault G, Gourraud PA, Perrot B, Delasalle B, Forestier B, Guillaume T, Peterlin P, Garnier A, Magnan A, Blanc FX, Lemarchand P (2018) Deconditioning, fatigue and impaired quality of life in long-term survivors after allogeneic hematopoietic stem cell transplantation. Bone Marrow Transplant 53:281–290. https://doi.org/10.1038/s41409-017-0057-5
Morishita S, Kaida K, Yamauchi S, Wakasugi T, Ikegame K, Ogawa H, Domen K (2017) Relationship of physical activity with physical function and health-related quality of life in patients having undergone allogeneic haematopoietic stem-cell transplantation. Eur J Cancer Care (Engl):26. https://doi.org/10.1111/ecc.12669
Carlson LE, Smith D, Russell J, Fibich C, Whittaker T (2006) Individualized exercise program for the treatment of severe fatigue in patients after allogeneic hematopoietic stem-cell transplant: a pilot study. Bone Marrow Transplant 37:945–954. https://doi.org/10.1038/sj.bmt.1705343
Bosnak Guclu M, Bargi G, Sucak GT (2019) Impairments in dyspnea, exercise capacity, physical activity and quality of life of allogeneic hematopoietic stem cell transplantation survivors compared with healthy individuals: a cross sectional study. Physiother Theory Pract 8:1–12. https://doi.org/10.1080/09593985.2019.1594473
San Juan AF, Chamorro-Vina C, Moral S et al (2008) Benefits of intrahospital exercise training after pediatric bone marrow transplantation. Int J Sports Med 29:439–446. https://doi.org/10.1055/s-2007-965571
Bogg TF, Broderick C, Shaw P, Cohn R, Naumann FL (2015) Feasibility of an inpatient exercise intervention for children undergoing hematopoietic stem cell transplant. Pediatr Transplant 19:925–931. https://doi.org/10.1111/petr.12614
Walrath M, Bacon C, Foley S, Fung HC (2015) Gastrointestinal side effects and adequacy of enteral intake in hematopoietic stem cell transplant patients. Nutr Clin Pract 30:305–310. https://doi.org/10.1177/0884533614547084
Goldenberg M, Danovitch I, IsHak WW (2014) Quality of life and smoking. Am J Addict 23:540–562. https://doi.org/10.1111/j.1521-0391.2014.12148.x
This work was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education, Science and Technology (NRF-2017R1C1B5015107), and it was also supported by the Ulsan University Hospital Research Grant (UUH-2019-06).
Conflict of interest
The authors declare that they have no conflict of interest.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
About this article
Cite this article
Cheon, J., Lee, Y.J., Jo, J. et al. Late complications and quality of life assessment for survivors receiving allogeneic hematopoietic stem cell transplantation. Support Care Cancer (2020). https://doi.org/10.1007/s00520-020-05572-0
- Allogeneic hematopoietic cell transplantation
- Late complications
- Quality of life
- Hospital Anxiety and Depression Scale