Skip to main content

Advertisement

SpringerLink
Log in

Non-viral pathogens of infectious diarrhoea post-allogeneic stem cell transplantation are associated with graft-versus-host disease

  • Original Article
  • Published:
Annals of Hematology Aims and scope Submit manuscript

Abstract

Infectious diarrhoea is common post-allogeneic haematopoietic stem-cell transplantation (alloHSCT). While the epidemiology of Clostridioides difficile infection (CDI) post-alloHSCT has been described, the impact of other diarrhoeal pathogens is uncertain. We reviewed all alloHSCT between 2017 and 2022 at a single large transplant centre; 374 patients were identified and included. The 1-year incidence of infectious diarrhoea was 23%, divided into viral (13/374, 3%), CDI (65/374, 17%) and other bacterial infections (16/374, 4%). There was a significant association between infectious diarrhoea within 1 year post-transplant and the occurrence of severe acute lower gastrointestinal graft-versus-host disease (GVHD, OR = 4.64, 95% CI 2.57–8.38, p < 0.001) and inferior GVHD-free, relapse-free survival on analysis adjusted for age, donor type, stem cell source and T-cell depletion (aHR = 1.64, 95% CI = 1.18–2.27, p = 0.003). When the classes of infectious diarrhoea were compared to no infection, bacterial (OR = 6.38, 95% CI 1.90–21.40, p = 0.003), CDI (OR = 3.80, 95% CI 1.91–7.53, p < 0.001) and multiple infections (OR = 11.16, 95% CI 2.84–43.92, p < 0.001) were all independently associated with a higher risk of severe GI GVHD. Conversely, viral infections were not (OR = 2.98, 95% CI 0.57–15.43, p = 0.20). Non-viral infectious diarrhoea is significantly associated with the development of GVHD. Research to examine whether the prevention of infectious diarrhoea via infection control measures or modulation of the microbiome reduces the incidence of GVHD is needed.

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
Fig. 2
Fig. 3

Similar content being viewed by others

Data availability

The dataset generated and analysed during the current study is available from the corresponding author upon reasonable request.

References

  1. Kolb HJ, Mittermüller J, Clemm C, Holler E, Ledderose G, Brehm G, Heim M, Wilmanns W (1990) Donor leukocyte transfusions for treatment of recurrent chronic myelogenous leukemia in marrow transplant patients. Blood 76(12):2462–2465

    Article  CAS  PubMed  Google Scholar 

  2. Jagasia M, Arora M, Flowers MED, Chao NJ, McCarthy PL, Cutler CS, Urbano-Ispizua A, Pavletic SZ, Haagenson MD, Zhang M-J, Antin JH, Bolwell BJ, Bredeson C, Cahn J-Y, Cairo M, Gale RP, Gupta V, Lee SJ, Litzow M, Weisdorf DJ, Horowitz MM, Hahn T (2012) Risk factors for acute GVHD and survival after hematopoietic cell transplantation. Blood 119(1):296–307. https://doi.org/10.1182/blood-2011-06-364265

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. El-Jawahri A, Li S, Antin JH, Spitzer TR, Armand PA, Koreth J, Nikiforow S, Ballen KK, Ho VT, Alyea EP, Dey BR, McAfee SL, Glotzbecker BE, Soiffer RJ, Cutler CS, Chen Y-B (2016) Improved treatment-related mortality and overall survival of patients with grade IV acute GVHD in the modern years. Biol Blood Marrow Transplant 22(5):910–918. https://doi.org/10.1016/j.bbmt.2015.12.024

    Article  PubMed  Google Scholar 

  4. Weisdorf D, Zhang M-J, Arora M, Horowitz MM, Rizzo JD, Eapen M (2012) Graft-versus-host disease induced graft-versus-leukemia effect: greater impact on relapse and disease-free survival after reduced intensity conditioning. Biol Blood Marrow Transplant 18(11):1727–1733. https://doi.org/10.1016/j.bbmt.2012.06.014

    Article  PubMed  PubMed Central  Google Scholar 

  5. Garnett C, Apperley JF, Pavlů J (2013) Treatment and management of graft-versus-host disease: improving response and survival. Ther Adv Hematol 4(6):366–378. https://doi.org/10.1177/2040620713489842

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Hahn T, McCarthy PL Jr, Zhang MJ, Wang D, Arora M, Frangoul H, Gale RP, Hale GA, Horan J, Isola L, Maziarz RT, van Rood JJ, Gupta V, Halter J, Reddy V, Tiberghien P, Litzow M, Anasetti C, Pavletic S, Ringdén O (2008) Risk factors for acute graft-versus-host disease after human leukocyte antigen-identical sibling transplants for adults with leukemia. J Clin Oncol 26(35):5728–5734. https://doi.org/10.1200/jco.2008.17.6545

    Article  PubMed  PubMed Central  Google Scholar 

  7. Alonso CD, Treadway SB, Hanna DB, Huff CA, Neofytos D, Carroll KC, Marr KA (2012) Epidemiology and outcomes of Clostridium difficile infections in hematopoietic stem cell transplant recipients. Clin Infect Dis 54(8):1053–1063. https://doi.org/10.1093/cid/cir1035

    Article  PubMed  PubMed Central  Google Scholar 

  8. Van Praet JT, Huysman A, De Knijf E, De Buyser S, Snauwaert S, Van Droogenbroeck J, Lodewyck T, Schauwvlieghe A, Selleslag D, Reynders M (2023) Infectious diarrhea after allogeneic hematopoietic cell transplantation assessed by a multiplex polymerase chain reaction assay. Int J Infect Dis 127:17–22. https://doi.org/10.1016/j.ijid.2022.11.045

    Article  CAS  PubMed  Google Scholar 

  9. Kelly CP, LaMont JT (2008) Clostridium difficile–more difficult than ever. N Engl J Med 359(18):1932–1940. https://doi.org/10.1056/NEJMra0707500

    Article  CAS  PubMed  Google Scholar 

  10. Slimings C, Armstrong P, Beckingham WD, Bull AL, Hall L, Kennedy KJ, Marquess J, McCann R, Menzies A, Mitchell BG, Richards MJ, Smollen PC, Tracey L, Wilkinson IJ, Wilson FL, Worth LJ, Riley TV (2014) Increasing incidence of Clostridium difficile infection, Australia, 2011–2012. Med J Aust 200(5):272–276. https://doi.org/10.5694/mja13.11153

    Article  PubMed  Google Scholar 

  11. Chung S, Abou Mourad Y (2019) Clostridium difficile infection among hematopoietic stem cell transplant recipients and subsequent development of graft-versus-host disease. Blood 134:4494. https://doi.org/10.1182/blood-2019-129663

    Article  Google Scholar 

  12. Bhutani D, Jaiyeoba C, Kim S, Naylor P, Uberti JP, Ratanatharathorn V, Ayash L, Deol A, Alavi A, Revankar S, Chandrasekar P (2019) Relationship between clostridium difficile infection and gastrointestinal graft versus host disease in recipients of allogeneic stem cell transplantation. Bone Marrow Transplant 54(1):164–167. https://doi.org/10.1038/s41409-018-0270-x

    Article  CAS  PubMed  Google Scholar 

  13. Chakrabarti S, Lees A, Jones SG, Milligan DW (2000) Clostridium difficile infection in allogeneic stem cell transplant recipients is associated with severe graft-versus-host disease and non-relapse mortality. Bone Marrow Transplant 26(8):871–876. https://doi.org/10.1038/sj.bmt.1702627

    Article  CAS  PubMed  Google Scholar 

  14. Ramanathan M, Kim S, He N, Chen M, Hematti P, Abid MB, Rotz SJ, Williams KM, Lazarus HM, Wirk B, Yin DE, Kanakry CG, Perales M-A, Chemaly RF, Dandoy CE, Riches M, Ustun C (2023) The incidence and impact of clostridioides difficile infection on transplant outcomes in acute leukemia and MDS after allogeneic hematopoietic cell transplant—a CIBMTR study. Bone Marrow Transplant 58(4):360–366. https://doi.org/10.1038/s41409-022-01896-z

    Article  PubMed  Google Scholar 

  15. De La Cochetière MF, Durand T, Lalande V, Petit JC, Potel G, Beaugerie L (2008) Effect of antibiotic therapy on human fecal microbiota and the relation to the development of Clostridium difficile. Microb Ecol 56(3):395–402. https://doi.org/10.1007/s00248-007-9356-5

    Article  CAS  PubMed  Google Scholar 

  16. Sehgal K, Khanna S (2021) Gut microbiome and Clostridioides difficile infection: a closer look at the microscopic interface. Therap Adv Gastroenterol 14:1756284821994736. https://doi.org/10.1177/1756284821994736

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Rea MC, O’Sullivan O, Shanahan F, O’Toole PW, Stanton C, Ross RP, Hill C (2012) Clostridium difficile carriage in elderly subjects and associated changes in the intestinal microbiota. J Clin Microbiol 50(3):867–875. https://doi.org/10.1128/jcm.05176-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Nelson AM, Walk ST, Taube S, Taniuchi M, Houpt ER, Wobus CE, Young VB (2012) Disruption of the human gut microbiota following Norovirus infection. PLoS ONE 7(10):e48224. https://doi.org/10.1371/journal.pone.0048224

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Hoyt R, Ritchie DS, Roberts AW, Macgregor L, Curtis DJ, Szer J, Grigg AP (2008) Cyclosporin, methotrexate and prednisolone for graft-versus-host disease prophylaxis in allogeneic peripheral blood progenitor cell transplants. Bone Marrow Transplant 41(7):651–658. https://doi.org/10.1038/sj.bmt.1705955

    Article  CAS  PubMed  Google Scholar 

  20. Glucksberg H, Storb R, Fefer A, Buckner CD, Neiman PE, Clift RA, Lerner KG, Thomas ED (1974) Clinical manifestations of graft-versus-host disease in human recipients of marrow from HL-A-matched sibling donors. Transplantation 18(4):295–304. https://doi.org/10.1097/00007890-197410000-00001

    Article  CAS  PubMed  Google Scholar 

  21. Jagasia MH, Greinix HT, Arora M, Williams KM, Wolff D, Cowen EW, Palmer J, Weisdorf D, Treister NS, Cheng GS, Kerr H, Stratton P, Duarte RF, McDonald GB, Inamoto Y, Vigorito A, Arai S, Datiles MB, Jacobsohn D, Heller T, Kitko CL, Mitchell SA, Martin PJ, Shulman H, Wu RS, Cutler CS, Vogelsang GB, Lee SJ, Pavletic SZ, Flowers ME (2015) National Institutes of Health Consensus Development Project on criteria for clinical trials in chronic graft-versus-host disease: I. The (2014) Diagnosis and Staging Working Group report. Biol Blood Marrow Transplant 21(3):389-401.e381. https://doi.org/10.1016/j.bbmt.2014.12.001

    Article  Google Scholar 

  22. Yolken RH, Bishop CA, Townsend TR, Bolyard EA, Bartlett J, Santos GW, Saral R (1982) Infectious gastroenteritis in bone-marrow-transplant recipients. N Engl J Med 306(17):1009–1012. https://doi.org/10.1056/nejm198204293061701

    Article  CAS  PubMed  Google Scholar 

  23. Kelly CP (2012) Can we identify patients at high risk of recurrent Clostridium difficile infection? Clin Microbiol Infect 18(Suppl 6):21–27. https://doi.org/10.1111/1469-0691.12046

    Article  PubMed  Google Scholar 

  24. Ma GK, Brensinger CM, Wu Q, Lewis JD (2017) Increasing incidence of multiply recurrent clostridium difficile infection in the United States: a cohort study. Ann Intern Med 167(3):152–158. https://doi.org/10.7326/m16-2733

    Article  PubMed  Google Scholar 

  25. Kinnebrew MA, Lee YJ, Jenq RR, Lipuma L, Littmann ER, Gobourne A, No D, van den Brink M, Pamer EG, Taur Y (2014) Early Clostridium difficile infection during allogeneic hematopoietic stem cell transplantation. PLoS ONE 9(3):e90158. https://doi.org/10.1371/journal.pone.0090158

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Rogers WS, Westblade LF, Soave R, Jenkins SG, van Besien K, Singh HK, Walsh TJ, Small CB, Shore T, Crawford CV, Satlin MJ (2020) Impact of a multiplexed polymerase chain reaction panel on identifying diarrheal pathogens in hematopoietic cell transplant recipients. Clin Infect Dis 71(7):1693–1700. https://doi.org/10.1093/cid/ciz1068

    Article  CAS  PubMed  Google Scholar 

  27. Zeiser R (2019) Advances in understanding the pathogenesis of graft-versus-host disease. Br J Haematol 187(5):563–572. https://doi.org/10.1111/bjh.16190

    Article  PubMed  Google Scholar 

  28. Zeiser R, Blazar BR (2017) Acute graft-versus-host disease - biologic process, prevention, and therapy. N Engl J Med 377(22):2167–2179. https://doi.org/10.1056/NEJMra1609337

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Klämbt V, Wohlfeil SA, Schwab L, Hülsdünker J, Ayata K, Apostolova P, Schmitt-Graeff A, Dierbach H, Prinz G, Follo M, Prinz M, Idzko M, Zeiser R (2015) A novel function for P2Y2 in myeloid recipient-derived cells during graft-versus-host disease. J Immunol 195(12):5795–5804. https://doi.org/10.4049/jimmunol.1501357

    Article  CAS  PubMed  Google Scholar 

  30. Choi SW, Levine JE, Ferrara JL (2010) Pathogenesis and management of graft-versus-host disease. Immunol Allergy Clin North Am 30(1):75–101. https://doi.org/10.1016/j.iac.2009.10.001

    Article  PubMed  PubMed Central  Google Scholar 

  31. Fredricks DN (2019) The gut microbiota and graft-versus-host disease. J Clin Investig 129(5):1808–1817. https://doi.org/10.1172/JCI125797

    Article  PubMed  PubMed Central  Google Scholar 

  32. Lemahieu W, Maes B, Verbeke K, Rutgeerts P, Geboes K, Vanrenterghem Y (2005) Cytochrome P450 3A4 and P-glycoprotein activity and assimilation of tacrolimus in transplant patients with persistent diarrhea. Am J Transplant 5(6):1383–1391. https://doi.org/10.1111/j.1600-6143.2005.00844.x

    Article  CAS  PubMed  Google Scholar 

  33. Bekkum DWV, Roodenburg J, Heidt PJ, Waaij DVD (1974) Mitigation of secondary disease of allogeneic mouse radiation chimeras by modification of the intestinal microflora. JNCI 52(2):401–404. https://doi.org/10.1093/jnci/52.2.401

    Article  PubMed  Google Scholar 

  34. Burgos da Silva M, Ponce DM, Dai A, M. Devlin S, Gomes ALC, Moore G, Slingerland J, Shouval R, Armijo GK, DeWolf S, Fei T, Clurman A, Fontana E, Amoretti LA, Wright RJ, Andrlova H, Miltiadous O, Perales M-A, Taur Y, Peled JU, van den Brink MRM (2022) Preservation of the fecal microbiome is associated with reduced severity of graft-versus-host disease. Blood 140(22):2385–2397. https://doi.org/10.1182/blood.2021015352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Taur Y, Jenq RR, Perales M-A, Littmann ER, Morjaria S, Ling L, No D, Gobourne A, Viale A, Dahi PB, Ponce DM, Barker JN, Giralt S, van den Brink M, Pamer EG (2014) The effects of intestinal tract bacterial diversity on mortality following allogeneic hematopoietic stem cell transplantation. Blood 124(7):1174–1182. https://doi.org/10.1182/blood-2014-02-554725

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Payen M, Nicolis I, Robin M, Michonneau D, Delannoye J, Mayeur C, Kapel N, Berçot B, Butel M-J, Le Goff J, Socié G, Rousseau C (2020) Functional and phylogenetic alterations in gut microbiome are linked to graft-versus-host disease severity. Blood Adv 4(9):1824–1832. https://doi.org/10.1182/bloodadvances.2020001531

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. DeFilipp Z, Hohmann E, Jenq RR, Chen YB (2019) Fecal microbiota transplantation: restoring the injured microbiome after allogeneic hematopoietic cell transplantation. Biol Blood Marrow Transplant 25(1):e17–e22. https://doi.org/10.1016/j.bbmt.2018.10.022

    Article  CAS  PubMed  Google Scholar 

  38. Vollaard EJ, Clasener HA (1994) Colonization resistance. Antimicrob Agents Chemother 38(3):409–414. https://doi.org/10.1128/aac.38.3.409

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Kamada N, Chen GY, Inohara N, Núñez G (2013) Control of pathogens and pathobionts by the gut microbiota. Nat Immunol 14(7):685–690. https://doi.org/10.1038/ni.2608

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Smith PM, Howitt MR, Panikov N, Michaud M, Gallini CA, Bohlooly YM, Glickman JN, Garrett WS (2013) The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 341(6145):569–573. https://doi.org/10.1126/science.1241165

    Article  CAS  PubMed  Google Scholar 

  41. Donohoe DR, Garge N, Zhang X, Sun W, O’Connell TM, Bunger MK, Bultman SJ (2011) The microbiome and butyrate regulate energy metabolism and autophagy in the mammalian colon. Cell Metab 13(5):517–526. https://doi.org/10.1016/j.cmet.2011.02.018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Jenq RR, Taur Y, Devlin SM, Ponce DM, Goldberg JD, Ahr KF, Littmann ER, Ling L, Gobourne AC, Miller LC, Docampo MD, Peled JU, Arpaia N, Cross JR, Peets TK, Lumish MA, Shono Y, Dudakov JA, Poeck H, Hanash AM, Barker JN, Perales M-A, Giralt SA, Pamer EG, van den Brink MRM (2015) Intestinal blautia is associated with reduced death from graft-versus-host disease. Biol Blood Marrow Transplant 21(8):1373–1383. https://doi.org/10.1016/j.bbmt.2015.04.016

    Article  PubMed  PubMed Central  Google Scholar 

  43. Shono Y, van den Brink MRM (2018) Gut microbiota injury in allogeneic haematopoietic stem cell transplantation. Nat Rev Cancer 18(5):283–295. https://doi.org/10.1038/nrc.2018.10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Bilinski J, Grzesiowski P, Sorensen N, Madry K, Muszynski J, Robak K, Wroblewska M, Dzieciatkowski T, Dulny G, Dwilewicz-Trojaczek J, Wiktor-Jedrzejczak W, Basak GW (2017) Fecal microbiota transplantation in patients with blood disorders inhibits gut colonization with antibiotic-resistant bacteria: results of a prospective, single-center study. Clin Infect Dis 65(3):364–370. https://doi.org/10.1093/cid/cix252

    Article  CAS  PubMed  Google Scholar 

  45. Pession A, Zama D, Muratore E, Leardini D, Gori D, Guaraldi F, Prete A, Turroni S, Brigidi P, Masetti R (2021) Fecal microbiota transplantation in allogeneic hematopoietic stem cell transplantation recipients: a systematic review. J Pers Med 11 (2). https://doi.org/10.3390/jpm11020100

  46. van Lier YF, Davids M, Haverkate NJE, de Groot PF, Donker ML, Meijer E, Heubel-Moenen FCJI, Nur E, Zeerleder SS, Nieuwdorp M, Blom B, Hazenberg MD (2020) Donor fecal microbiota transplantation ameliorates intestinal graft-versus-host disease in allogeneic hematopoietic cell transplant recipients. Sci Transl Med 12 (556). https://doi.org/10.1126/scitranslmed.aaz8926

  47. Webb BJ, Brunner A, Ford CD, Gazdik MA, Petersen FB, Hoda D (2016) Fecal microbiota transplantation for recurrent Clostridium difficile infection in hematopoietic stem cell transplant recipients. Transpl Infect Dis 18(4):628–633. https://doi.org/10.1111/tid.12550

    Article  CAS  PubMed  Google Scholar 

  48. Cammarota G, Ianiro G, Tilg H, Rajilić-Stojanović M, Kump P, Satokari R, Sokol H, Arkkila P, Pintus C, Hart A, Segal J, Aloi M, Masucci L, Molinaro A, Scaldaferri F, Gasbarrini G, Lopez-Sanroman A, Link A, de Groot P, de Vos WM, Högenauer C, Malfertheiner P, Mattila E, Milosavljević T, Nieuwdorp M, Sanguinetti M, Simren M, Gasbarrini A (2017) European consensus conference on faecal microbiota transplantation in clinical practice. Gut 66(4):569–580. https://doi.org/10.1136/gutjnl-2016-313017

    Article  PubMed  Google Scholar 

  49. Shouval R, Youngster I, Geva M, Eshel A, Danylesko I, Shimoni A, Beider K, Fein JA, Sharon I, Koren O, Nagler A (2018) Repeated courses of orally administered fecal microbiota transplantation for the treatment of steroid resistant and steroid dependent intestinal acute graft vs. host disease: a pilot study (NCT 03214289). Blood 132(1):2121–2121. https://doi.org/10.1182/blood-2018-99-110270

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Clinical Haematology, Peter MacCallum Cancer Centre and Royal Melbourne Hospital, 305 Grattan St, Melbourne, VIC, 3000, Australia

    Matthew J. Rees, Alexandra Rivalland, Sarah Tan, Mingdi Xie & David Ritchie

  2. Department of Infectious Diseases, Peter MacCallum Cancer Centre, Melbourne, Australia

    Michelle K. Yong

  3. Victorian Infectious Diseases Service, Melbourne Health, Melbourne, Australia

    Michelle K. Yong

  4. Sir Peter MacCallum, Department of Oncology, University of Melbourne, Melbourne, Australia

    Michelle K. Yong

  5. National Centre for Infections in Cancer, Peter MacCallum Cancer Centre, Melbourne, Melbourne, Australia

    Michelle K. Yong

Authors
  1. Matthew J. Rees
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alexandra Rivalland
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sarah Tan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mingdi Xie
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Michelle K. Yong
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. David Ritchie
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Matthew James Rees, Michelle Yong and David Ritchie designed the study; All authors contributed data and reviewed the manuscript; Matthew James Rees analysed the data; Matthew James Rees wrote the first draft of the manuscript, and all authors read and approved the final manuscript.

Corresponding author

Correspondence to Matthew J. Rees.

Ethics declarations

Ethics approval

This retrospective study was performed in line with the principles of the Declaration of Helsinki. Approval was granted by the ethics committees of Peter MacCallum Cancer Centre and the Royal Melbourne hospital.

Competing interests

The authors declare no competing interests.

Disclosures

The authors have no disclosures.

Additional information

Publisher's Note

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

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

Rees, M.J., Rivalland, A., Tan, S. et al. Non-viral pathogens of infectious diarrhoea post-allogeneic stem cell transplantation are associated with graft-versus-host disease. Ann Hematol 103, 593–602 (2024). https://doi.org/10.1007/s00277-023-05526-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00277-023-05526-6

Keywords

Search

Navigation