Allogeneic hematopoietic cell transplantation, the microbiome, and graft-versus-host disease

References

• Pasquini M, Wang Z, Horowitz MM, Gale RP. Report from the Center for International Blood and Marrow Transplant Research (CIBMTR): current uses and outcomes of hematopoietic cell transplants for blood and bone marrow disorders. Clin Transpl. 2013;2013:187–13.
   Google Scholar
• D’Souza A, Fretham C, Lee SJ, Arora M, Brunner J, Chhabra S, Devine S, Eapen M, Hamadani M, Hari P, et al. Current use of and trends in hematopoietic cell transplantation in the United States. Biol Blood Marrow Transplant. 2020 Aug;26(8):e177–e182. doi:10.1016/j.bbmt.2020.04.013.
   PubMed Web of Science ®Google Scholar
• Penack O, Peczynski C, Mohty M, Yakoub-Agha I, Styczynski J, Montoto S, Duarte RF, Kröger N, Schoemans H, Koenecke C, et al. How much has allogeneic stem cell transplant-related mortality improved since the 1980s? A retrospective analysis from the EBMT. Blood Adv. 2020 Dec 22;4(24):6283–6290. doi:10.1182/bloodadvances.2020003418.
   PubMed Web of Science ®Google Scholar
• Gifford G, Gilroy N, Dyer G, Shouval R, Waters NR, Gomes ALC, Zuanelli Brambilla C, Fei T, Devlin SM, Nguyen CL, et al. The experience of survival following allogeneic haematopoietic stem cell transplantation in New South Wales, Australia. Bone Marrow Transplantation. 2016 Oct;51(10):1361–1368. doi:10.1038/bmt.2016.135.
   PubMed Web of Science ®Google Scholar
• Wolff D, Bardak J, Edinger M, Klinger-Schindler U, Holler E, Lawitschka A, Schoemans H, Herr W, Kröger N, Ayuk Ayuketang F. Evaluation of the Cost of survivorship care after allogeneic hematopoeitic stem cell transplantation-an analysis of 2 German transplantation centers. Front Public Health. 2020;8:572470. doi:10.3389/fpubh.2020.572470.
   PubMed Web of Science ®Google Scholar
• Westin JR, Saliba RM, De Lima M, Alousi A, Hosing C, Qazilbash MH, Khouri IF, Shpall EJ, Anderlini P, Rondon G, et al. Steroid-Refractory Acute GVHD: predictors and Outcomes. Adv Hematol. 2011;2011:601953. doi:10.1155/2011/601953.
   PubMedGoogle Scholar
• Zeiser R, Blazar BR. Acute graft-versus-host disease - Biologic process, prevention, and therapy. N Engl J Med. 2017 Nov 30;377(22):2167–2179. doi:10.1056/NEJMra1609337.
   PubMed Web of Science ®Google Scholar
• Jenq RR, van den Brink MRM. van den Brink MR. Allogeneic haematopoietic stem cell transplantation: individualized stem cell and immune therapy of cancer. Nat Rev Cancer. 2010 Mar;10(3):213–221. doi:10.1038/nrc2804.
   PubMed Web of Science ®Google Scholar
• Zeiser R, Blazar BR. Pathophysiology of chronic graft-versus-host disease and therapeutic targets. N Engl J Med. 2017 Dec 28;377(26):2565–2579. doi:10.1056/NEJMra1703472.
   PubMed Web of Science ®Google Scholar
• Fowler DH. Shared biology of GVHD and GVT effects: potential methods of separation. Crit Rev Oncol Hematol. 2006 Mar;57(3):225–244. doi:10.1016/j.critrevonc.2005.07.001.
   PubMed Web of Science ®Google Scholar
• Rooks MG, Garrett WS. Gut microbiota, metabolites and host immunity. Nat Rev Immunol. 2016 May 27;16(6):341–352. doi:10.1038/nri.2016.42.
   PubMed Web of Science ®Google Scholar
• Miller TL, Wolin MJ. Pathways of acetate, propionate, and butyrate formation by the human fecal microbial flora. Appl Environ Microbiol. 1996 May;62(5):1589–1592. doi:10.1128/aem.62.5.1589-1592.1996.
   PubMed Web of Science ®Google Scholar
• Smith PM, Howitt MR, Panikov N, Michaud M, Gallini CA, Bohlooly-Y M, Glickman JN, Garrett WS. The microbial metabolites, short-chain fatty acids, regulate colonic T reg cell homeostasis. Science. 2013 Aug 2;341(6145):569–573. doi:10.1126/science.1241165.
   PubMed Web of Science ®Google Scholar
• Sun M, Wu W, Chen L, Yang W, Huang X, Ma C, Chen F, Xiao Y, Zhao Y, Ma C. Microbiota-derived short-chain fatty acids promote Th1 cell IL-10 production to maintain intestinal homeostasis. Nat Commun. 2018 Sep 3;9(1):3555. doi:10.1038/s41467-018-05901-2.
   PubMed Web of Science ®Google Scholar
• Yang W, Yu T, Huang X, Bilotta AJ, Xu L, Lu Y, Sun J, Pan F, Zhou J, Zhang W, et al. Intestinal microbiota-derived short-chain fatty acids regulation of immune cell IL-22 production and gut immunity. Nat Commun. 2020 Sep 8;11(1):4457. doi:10.1038/s41467-020-18262-6.
   PubMed Web of Science ®Google Scholar
• Kim M, Qie Y, Park J, Kim CH. Gut microbial metabolites fuel host antibody responses. Cell Host Microbe. 2016 Aug 10;20(2):202–214. doi:10.1016/j.chom.2016.07.001.
   PubMed Web of Science ®Google Scholar
• Gaudier E, Jarry A, Blottiere HM, de Coppet P, Buisine MP, Aubert JP, Laboisse C, Cherbut C, Hoebler C. Butyrate specifically modulates MUC gene expression in intestinal epithelial goblet cells deprived of glucose. Am J Physiol Gastrointest Liver Physiol. 2004 Dec;287(6):G1168–74. doi:10.1152/ajpgi.00219.2004.
   PubMed Web of Science ®Google Scholar
• Willemsen LE, Koetsier MA, van Deventer SJ, van Tol EA. Short chain fatty acids stimulate epithelial mucin 2 expression through differential effects on prostaglandin E(1) and E(2) production by intestinal myofibroblasts. Gut 2003 Oct;52(10):1442–1447. doi:10.1136/gut.52.10.1442.
   PubMed Web of Science ®Google Scholar
• Ruff WE, Greiling TM, Kriegel MA. Host-microbiota interactions in immune-mediated diseases. Nat Rev Microbiol. 2020 Sep;18(9):521–538. doi:10.1038/s41579-020-0367-2.
   PubMed Web of Science ®Google Scholar
• Taur Y, Xavier JB, Lipuma L, Ubeda C, Goldberg J, Gobourne A, Lee YJ, Dubin KA, Socci ND, Viale A. Intestinal domination and the risk of bacteremia in patients undergoing allogeneic hematopoietic stem cell transplantation. Clin Infect Dis. 2012 Oct;55(7):905–914. doi:10.1093/cid/cis580.
   PubMed Web of Science ®Google Scholar
• Jenq RR, Ubeda C, Taur Y, Menezes CC, Khanin R, Dudakov JA, Liu C, West ML, Singer NV, Equinda MJ, et al. Regulation of intestinal inflammation by microbiota following allogeneic bone marrow transplantation. J Exp Med. 2012 May 7;209(5):902–910. doi:10.1084/jem.20112408.
   Web of Science ®Google Scholar
• Taur Y, Jenq RR, Perales M-A, Littmann ER, Morjaria S, Ling L, No D, Gobourne A, Viale A, Dahi PB, et al. The effects of intestinal tract bacterial diversity on mortality following allogeneic hematopoietic stem cell transplantation. Blood. 2014 Aug 14;124(7):1174–1182. doi:10.1182/blood-2014-02-554725.
   PubMed Web of Science ®Google Scholar
• Peled JU, Gomes ALC, Devlin SM, Littmann ER, Taur Y, Sung AD, Weber D, Hashimoto D, Slingerland AE, Slingerland JB, et al. Microbiota as predictor of mortality in allogeneic hematopoietic-cell transplantation. N Engl J Med. 2020 Feb 27;382(9):822–834. doi:10.1056/NEJMoa1900623.
   PubMed Web of Science ®Google Scholar
• Hulsdunker J, Ottmuller KJ, Neeff HP, Koyama M, Gao Z, Thomas OS, Follo M, Al-Ahmad A, Prinz G, Duquesne S, et al. Neutrophils provide cellular communication between ileum and mesenteric lymph nodes at graft-versus-host disease onset. Blood. 2018 Apr 19;131(16):1858–1869. doi:10.1182/blood-2017-10-812891.
   PubMed Web of Science ®Google Scholar
• Khuat LT, Le CT, Pai CS, Shields-Cutler RR, Holtan SG, Rashidi A, Parker SL, Knights D, Luna JI, Dunai C, et al. Obesity induces gut microbiota alterations and augments acute graft-versus-host disease after allogeneic stem cell transplantation. Sci Transl Med. 2020 Nov 25;12(571). doi:10.1126/scitranslmed.aay7713
   PubMed Web of Science ®Google Scholar
• Schroeder BO, Backhed F. Signals from the gut microbiota to distant organs in physiology and disease. Nat Med. 2016 Oct 6;22(10):1079–1089. doi:10.1038/nm.4185.
   PubMed Web of Science ®Google Scholar
• Hino A, Fukushima K, Kusakabe S, Ueda T, Sudo T, Fujita J, Motooka D, Takeda AK, Shinozaki NO, Watanabe S, et al. Prolonged gut microbial alterations in post-transplant survivors of allogeneic haematopoietic stem cell transplantation. Br J Haematol. 2022 Dec 5; doi:10.1111/bjh.18574.
   PubMedGoogle Scholar
• Rashidi A, Ebadi M, Rehman TU, Elhusseini H, Halaweish HF, Kaiser T, Holtan SG, Khoruts A, Weisdorf DJ, Staley C, et al. Lasting shift in the gut microbiota in patients with acute myeloid leukemia. Blood Adv. 2022 Jun 14;6(11):3451–3457. doi:10.1182/bloodadvances.2021006783.
   PubMed Web of Science ®Google Scholar
• Rashidi A, Kaiser T, Graiziger C, Holtan SG, Rehman TU, Weisdorf DJ, Dunny GM, Khoruts A, Staley C. Gut dysbiosis during antileukemia chemotherapy versus allogeneic hematopoietic cell transplantation. Cancer. 2020 Apr 1;126(7):1434–1447. doi:10.1002/cncr.32641.
   PubMed Web of Science ®Google Scholar
• Montassier E, Gastinne T, Vangay P, Al-Ghalith GA, Bruley Des Varannes S, Massart S, Moreau P, Potel G, de La Cochetière MF, Batard E. Chemotherapy-driven dysbiosis in the intestinal microbiome. Aliment Pharmacol Ther. 2015 Sep;42(5):515–528. doi:10.1111/apt.13302.
   PubMed Web of Science ®Google Scholar
• Galloway-Pena JR, Shi Y, Peterson CB, Sahasrabhojane P, Gopalakrishnan V, Brumlow CE, Daver NG, Alfayez M, Boddu PC, Khan MAW, et al. Gut microbiome signatures are predictive of infectious risk following induction therapy for acute Myeloid Leukemia. Clin Infect Dis. 2020 Jun 24;71(1):63–71. doi:10.1093/cid/ciz777.
   PubMed Web of Science ®Google Scholar
• van Vliet MJ, Tissing WJ, Dun CA, Meessen N, Kamps W, de Bont E, Harmsen H. Chemotherapy treatment in pediatric patients with acute myeloid leukemia receiving antimicrobial prophylaxis leads to a relative increase of colonization with potentially pathogenic bacteria in the gut. Clin Infect Dis. 2009 Jul 15;49(2):262–270. doi:10.1086/599346.
   PubMed Web of Science ®Google Scholar
• Zwielehner J, Lassl C, Hippe B, Pointner A, Switzeny OJ, Remely M, Kitzweger E, Ruckser R, Haslberger AG. Changes in human fecal microbiota due to chemotherapy analyzed by TaqMan-PCR, 454 sequencing and PCR-DGGE fingerprinting. PLoS One. 2011;6(12):e28654. doi:10.1371/journal.pone.0028654.
   PubMed Web of Science ®Google Scholar
• Biagi E, Zama D, Nastasi C, Consolandi C, Fiori J, Rampelli S, Turroni S, Centanni M, Severgnini M, Peano C, et al. Gut microbiota trajectory in pediatric patients undergoing hematopoietic SCT. Bone Marrow Transplantation. 2015 Jul;50(7):992–998. doi:10.1038/bmt.2015.16.
   PubMed Web of Science ®Google Scholar
• Gerassy-Vainberg S, Blatt A, Danin-Poleg Y, Gershovich K, Sabo E, Nevelsky A, Daniel S, Dahan A, Ziv O, Dheer R, et al. Radiation induces proinflammatory dysbiosis: transmission of inflammatory susceptibility by host cytokine induction. Gut. 2018 Jan;67(1):97–107. doi:10.1136/gutjnl-2017-313789.
   PubMed Web of Science ®Google Scholar
• Shouval R, Waters NR, Gomes ALC, Zuanelli Brambilla C, Fei T, Devlin SM, Nguyen CL, Markey KA, Dai A, Slingerland JB, et al. Conditioning regimens are associated with distinct patterns of microbiota injury in allogeneic hematopoietic cell transplantation. Clin Cancer Res. 2023 Jan 4;29(1):165–173. doi:10.1158/1078-0432.CCR-22-1254.
   PubMed Web of Science ®Google Scholar
• Cray P, Sheahan BJ, Dekaney CM. Secretory sorcery: paneth cell control of intestinal repair and homeostasis. Cell Mol Gastroenterol Hepatol. 2021;12(4):1239–1250. doi:10.1016/j.jcmgh.2021.06.006.
   PubMed Web of Science ®Google Scholar
• Norona J, Apostolova P, Schmidt D, Ihlemann R, Reischmann N, Taylor G, Köhler N, de Heer J, Heeg S, Andrieux G, et al. Glucagon-like peptide 2 for intestinal stem cell and Paneth cell repair during graft-versus-host disease in mice and humans. Blood. 2020 Sep 17;136(12):1442–1455. doi:10.1182/blood.2020005957.
   PubMed Web of Science ®Google Scholar
• Tamburini FB, Andermann TM, Tkachenko E, Senchyna F, Banaei N, Bhatt AS. Precision identification of diverse bloodstream pathogens in the gut microbiome. Nat Med. 2018 Dec;24(12):1809–1814. doi:10.1038/s41591-018-0202-8.
   PubMed Web of Science ®Google Scholar
• Weber D, Jenq RR, Peled JU, Taur Y, Hiergeist A, Koestler J, Dettmer K, Weber M, Wolff D, Hahn J, et al. Microbiota disruption induced by early use of broad-spectrum antibiotics is an independent risk factor of outcome after allogeneic stem cell transplantation. Biol Blood Marrow Tr. 2017 May;23(5):845–852. doi:10.1016/j.bbmt.2017.02.006.
   PubMed Web of Science ®Google Scholar
• Ubeda C, Taur Y, Jenq RR, Equinda MJ, Son T, Samstein M, Viale A, Socci ND, van den Brink MRM, Kamboj M, et al. Vancomycin-resistant Enterococcus domination of intestinal microbiota is enabled by antibiotic treatment in mice and precedes bloodstream invasion in humans. J Clin Invest. 2010 Dec;120(12):4332–4341. doi:10.1172/JCI43918.
   PubMed Web of Science ®Google Scholar
• Falony G, Joossens M, Vieira-Silva S, Wang J, Darzi Y, Faust K, Kurilshikov A, Bonder MJ, Valles-Colomer M, Vandeputte D, et al. Population-level analysis of gut microbiome variation. Science. 2016 Apr 29;352(6285):560–564. doi:10.1126/science.aad3503.
   PubMed Web of Science ®Google Scholar
• Zhernakova A, Kurilshikov A, Bonder MJ, Tigchelaar EF, Schirmer M, Vatanen T, Mujagic Z, Vila AV, Falony G, Vieira-Silva S, et al. Population-based metagenomics analysis reveals markers for gut microbiome composition and diversity. Science. 2016 Apr 29;352(6285):565–569. doi:10.1126/science.aad3369.
   PubMed Web of Science ®Google Scholar
• Dominguez-Bello MG, Costello EK, Contreras M, Magris M, Hidalgo G, Fierer N, Knight R. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci U S A. 2010 Jun 29;107(26):11971–11975. doi:10.1073/pnas.1002601107.
   PubMed Web of Science ®Google Scholar
• Ley RE, Peterson DA, Gordon JI. Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell. 2006 Feb 24;124(4):837–848. doi:10.1016/j.cell.2006.02.017.
   PubMed Web of Science ®Google Scholar
• Swarte JC, Li Y, Hu S, Björk JR, Gacesa R, Vich Vila A, Douwes RM, Collij V, Kurilshikov A, Post A, et al. Gut microbiome dysbiosis is associated with increased mortality after solid organ transplantation. Sci Transl Med. 2022 Aug 31;14(660):eabn7566. doi:10.1126/scitranslmed.abn7566.
   PubMed Web of Science ®Google Scholar
• Schluter J, Peled JU, Taylor BP, Markey KA, Smith M, Taur Y, Niehus R, Staffas A, Dai A, Fontana E, et al. The gut microbiota is associated with immune cell dynamics in humans. Nature. 2020 Dec;588(7837):303–307. doi:10.1038/s41586-020-2971-8.
   PubMed Web of Science ®Google Scholar
• Miltiadous O, Waters NR, Andrlova H, Dai A, Nguyen CL, Burgos da Silva M, Lindner S, Slingerland J, Giardina P, Clurman A, et al. Early intestinal microbial features are associated with CD4 T-cell recovery after allogeneic hematopoietic transplant. Blood. 2022 May 5;139(18):2758–2769. doi:10.1182/blood.2021014255.
   PubMed Web of Science ®Google Scholar
• Kolodziejczyk AA, Zheng D, Elinav E. Diet-microbiota interactions and personalized nutrition. Nat Rev Microbiol. 2019 Dec;17(12):742–753. doi:10.1038/s41579-019-0256-8.
   PubMed Web of Science ®Google Scholar
• Johnson AJ, Vangay P, Al-Ghalith GA, Hillmann BM, Ward TL, Shields-Cutler RR, Kim AD, Shmagel AK, Syed AN, Walter J, et al. Daily sampling reveals personalized diet-microbiome associations in humans. Cell Host Microbe. 2019 Jun 12;25(6):789–802 e5. doi:10.1016/j.chom.2019.05.005.
   PubMed Web of Science ®Google Scholar
• Kyle UG, Chalandon Y, Miralbell R, Karsegard VL, Hans D, Trombetti A, Rizzoli R, Helg C, Pichard C. Longitudinal follow-up of body composition in hematopoietic stem cell transplant patients. Bone Marrow Transplant. 2005 Jun;35(12):1171–1177. doi:10.1038/sj.bmt.1704996.
   PubMed Web of Science ®Google Scholar
• D’Amico F, Biagi E, Rampelli S, Fiori J, Zama D, Soverini M, Barone M, Leardini D, Muratore E, Prete A, et al. Enteral nutrition in pediatric patients undergoing hematopoietic SCT promotes the recovery of gut microbiome homeostasis. Nutrients. 2019 Dec 4;11(12):doi:10.3390/nu11122958
   Web of Science ®Google Scholar
• Andersen S, Staudacher H, Weber N, Kennedy G, Varelias A, Banks M, Bauer J. Pilot study investigating the effect of enteral and parenteral nutrition on the gastrointestinal microbiome post-allogeneic transplantation. Br J Haematol. 2020 Feb;188(4):570–581. doi:10.1111/bjh.16218.
   PubMed Web of Science ®Google Scholar
• Beckerson J, Szydlo RM, Hickson M, Mactier CE, Innes AJ, Gabriel IH, Palanicawandar R, Kanfer EJ, Macdonald DH, Milojkovic D, et al. Impact of route and adequacy of nutritional intake on outcomes of allogeneic haematopoietic cell transplantation for haematologic malignancies. Clin Nutr. 2019 Apr;38(2):738–744. doi:10.1016/j.clnu.2018.03.008.
   PubMed Web of Science ®Google Scholar
• Gonzales F, Bruno B, Alarcon Fuentes M, De Berranger E, Guimber D, Behal H, Gandemar V, Spiegel A, Sirvent A, Yakoub-Agha I, et al. Better early outcome with enteral rather than parenteral nutrition in children undergoing MAC allo-SCT. Clin Nutr. 2018 Dec;37(6Pt A):2113–2121. doi:10.1016/j.clnu.2017.10.005.
   PubMedGoogle Scholar
• Shono Y. Van den Brink MRM. Gut microbiota injury in allogeneic haematopoietic stem cell transplantation. Nat Rev Cancer. 2018 May;18(5):283–295. doi:10.1038/nrc.2018.10.
   PubMed Web of Science ®Google Scholar
• Schloig S, Arumugam M, Sunagawa S, Mitreva M, Tap J, Zhu A, Waller A, Mende DR, Kultima JR, Martin J, et al. Genomic variation landscape of the human gut microbiome. Nature. 2013 Jan 3;493(7430):45–50. doi:10.1038/nature11711.
   PubMed Web of Science ®Google Scholar
• Van Tyne D, Gilmore MS. Friend turned foe: evolution of enterococcal virulence and antibiotic resistance. Annu Rev Microbiol. 2014;68(1):337–356. doi:10.1146/annurev-micro-091213-113003.
   PubMedGoogle Scholar
• Geva-Zatorsky N, Sefik E, Kua L, Pasman L, Tan TG, Ortiz-Lopez A, Yanortsang TB, Yang L, Jupp R, Mathis D, et al. Mining the human gut microbiota for immunomodulatory organisms. Cell. 2017 Feb 23;168(5):928–943 e11. doi:10.1016/j.cell.2017.01.022.
   PubMed Web of Science ®Google Scholar
• Steck N, Hoffmann M, Sava IG, Kim SC, Hahne H, Tonkonogy SL, Mair K, Krueger D, Pruteanu M, Shanahan F, et al. Enterococcus faecalis metalloprotease compromises epithelial barrier and contributes to intestinal inflammation. Gastroenterology. 2011 Sep;141(3):959–971. doi:10.1053/j.gastro.2011.05.035.
   PubMed Web of Science ®Google Scholar
• Molina MA, Diaz AM, Hesse C, Ginter W, Gentilini MV, Nuñez GG, Canellada AM, Sparwasser T, Berod L, Castro MS, et al. Immunostimulatory effects triggered by Enterococcus faecalis CECT7121 probiotic strain involve activation of dendritic cells and interferon-gamma production. PLoS One. 2015;10(5):e0127262. doi:10.1371/journal.pone.0127262.
   PubMed Web of Science ®Google Scholar
• Kim SC, Tonkonogy SL, Albright CA, Tsang J, Balish EJ, Braun J, Huyke MM, Sartor RB. Variable phenotypes of enterocolitis in interleukin 10-deficient mice monoassociated with two different commensal bacteria. Gastroenterology. 2005 Apr;128(4):891–906. doi:10.1053/j.gastro.2005.02.009.
   PubMed Web of Science ®Google Scholar
• Stein-Thoeringer CK, Nichols KB, Lazrak A, Docampo MD, Slingerland AE, Slingerland JB, Clurman AG, Armijo G, Gomes ALC, Shono Y, et al. Lactose drives Enterococcus expansion to promote graft-versus-host disease. Science. 2019 Nov 29;366(6469):1143–1149. doi:10.1126/science.aax3760.
   PubMed Web of Science ®Google Scholar
• van den Bogert B, Meijerink M, Zoetendal EG, Wells JM, Kleerebezem M. Immunomodulatory properties of Streptococcus and Veillonella isolates from the human small intestine microbiota. PLoS One. 2014;9(12):e114277. doi:10.1371/journal.pone.0114277.
   PubMed Web of Science ®Google Scholar
• Tang X, Kudo Y, Baker JL, LaBonte S, Jordan PA, McKinnie SMK, Guo J, Huan T, Moore BS, Edlund A, et al. Cariogenic streptococcus mutans produces tetramic acid strain-specific antibiotics that impair commensal colonization. ACS Infect Dis. 2020 Apr 10;6(4):563–571. doi:10.1021/acsinfecdis.9b00365.
   PubMed Web of Science ®Google Scholar
• Kulkarni S, Powles R, Treleaven J, Riley U, Singhal S, Horton C, Sirohi B, Bhagwati N, Meller S, Saso R, et al. Chronic graft versus host disease is associated with long-term risk for pneumococcal infections in recipients of bone marrow transplants. Blood. 2000 Jun 15;95(12):3683–3686. doi:10.1182/blood.V95.12.3683.
   PubMed Web of Science ®Google Scholar
• Engelhard D, Cordonnier C, Shaw PJ, Parkalli T, Guenther C, Martino R, Dekker AW, Prentice HG, Gustavsson A, Nurnberger W, et al. Early and late invasive pneumococcal infection following stem cell transplantation: a European Bone Marrow Transplantation survey. Br J Haematol. 2002 May;117(2):444–450. doi:10.1046/j.1365-2141.2002.03457.x.
   PubMed Web of Science ®Google Scholar
• Aguilar-Guisado M, Jimenez-Jambrina M, Espigado I, Rovira M, Martino R, Oriol A, Borrell N, Ruiz I, Martín-Dávila P, de la Cámara R, et al. Pneumonia in allogeneic stem cell transplantation recipients: a multicenter prospective study. Clin Transplant. 2011 Nov-Dec;25(6):E629–38. doi:10.1111/j.1399-0012.2011.01495.x.
   PubMed Web of Science ®Google Scholar
• Ubeda C, Bucci V, Caballero S, Djukovic A, Toussaint NC, Equinda M, Lipuma L, Gobourne A, No D, Taur Y, et al. Intestinal microbiota containing Barnesiella species cures vancomycin-resistant Enterococcus faecium colonization. Infect Immun. 2013 Mar;81(3):965–973. doi:10.1128/IAI.01197-12.
   PubMed Web of Science ®Google Scholar
• Jenq RR, Taur Y, Devlin SM, Ponce DM, Goldberg JD, Ahr KF, Littmann ER, Ling L, Gobourne AC, Miller LC, et al. Intestinal Blautia Is Associated with Reduced Death from Graft-versus-Host Disease. Biol Blood Marrow Tr. 2015 Aug;21(8):1373–1383. doi:10.1016/j.bbmt.2015.04.016.
   PubMed Web of Science ®Google Scholar
• Bhattacharyya A, Hanafi LA, Sheih A, Golob JL, Srinivasan S, Boeckh MJ, Pergam S, Mahmood S, Baker KK, Gooley TA, et al. Graft-derived reconstitution of mucosal-associated invariant T Cells after allogeneic hematopoietic cell transplantation. Biol Blood Marrow Transplant. 2018 Feb;24(2):242–251. doi:10.1016/j.bbmt.2017.10.003.
   PubMed Web of Science ®Google Scholar
• Andrlova H, Miltiadous O, Kousa AI, Dai A, DeWolf S, Violante S, Park H-Y, Janaki-Raman S, Gardner R, El Daker S, et al. MAIT and Vdelta2 unconventional T cells are supported by a diverse intestinal microbiome and correlate with favorable patient outcome after allogeneic HCT. Sci Transl Med. 2022 May 25;14(646):eabj2829. doi:10.1126/scitranslmed.abj2829.
   PubMed Web of Science ®Google Scholar
• Atarashi K, Tanoue T, Oshima K, Suda W, Nagano Y, Nishikawa H, Fukuda S, Saito T, Narushima S, Hase K, et al. Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota. Nature. 2013 Aug 8;500(7461):232–236. doi:10.1038/nature12331.
   PubMed Web of Science ®Google Scholar
• Mathewson ND, Jenq R, Mathew AV, Koenigsknecht M, Hanash A, Toubai T, Oravecz-Wilson K, Wu S-R, Sun Y, Rossi C, et al. Gut microbiome-derived metabolites modulate intestinal epithelial cell damage and mitigate graft-versus-host disease. Nat Immunol. 2016 May;17(5):505–513. doi:10.1038/ni.3400.
   PubMed Web of Science ®Google Scholar
• Payen M, Nicolis I, Robin M, Michonneau D, Delannoye J, Mayeur C, Kapel N, Berçot B, Butel M-J, Le Goff J, et al. Functional and phylogenetic alterations in gut microbiome are linked to graft-versus-host disease severity. Blood Adv. 2020 May 12;4(9):1824–1832. doi:10.1182/bloodadvances.2020001531.
   PubMed Web of Science ®Google Scholar
• Markey KA, Schluter J, Gomes ALC, Littmann, ER, Pickard, AJ, Taylor, BP , Giardana PA, Weber D, Dai A, Docampo MD, et al. The microbe-derived short-chain fatty acids butyrate and propionate are associated with protection from chronic GVHD. Blood. 2020 Jul 2;136(1):130–136. doi:10.1182/blood.2019003369.
   PubMed Web of Science ®Google Scholar
• Weber D, Hiergeist A, Weber M, Dettmer K, Wolff D, Hahn J, Herr W, Gessner A, Holler E. Detrimental effect of broad-spectrum antibiotics on intestinal microbiome diversity in patients after allogeneic stem cell transplantation: lack of commensal sparing antibiotics. Clin Infect Dis. 2019 Apr 8;68(8):1303–1310. doi:10.1093/cid/ciy711.
   PubMed Web of Science ®Google Scholar
• Shono Y, Docampo MD, Peled JU, Perobelli SM, Velardi E, Tsai JJ, Slingerland AE, Smith OM, Young LF, Gupta J. Increased GVHD-related mortality with broad-spectrum antibiotic use after allogeneic hematopoietic stem cell transplantation in human patients and mice. Sci Transl Med. 2016 May 18;8(339):339ra71. doi:10.1126/scitranslmed.aaf2311.
   PubMed Web of Science ®Google Scholar
• Weber D, Oefner PJ, Dettmer K, Hiergeist A, Koestler J, Gessner A, Weber M, Stämmler F, Hahn J, Wolff D, et al. Rifaximin preserves intestinal microbiota balance in patients undergoing allogeneic stem cell transplantation. Bone Marrow Transplant. 2016 Aug;51(8):1087–1092. doi:10.1038/bmt.2016.66.
   PubMed Web of Science ®Google Scholar
• de Gunzburg J, Ghozlane A, Ducher A, Le Chatelier E, Duval X, Ruppé E, Armand-Lefevre L, Sablier-Gallis F, Burdet C, Alavoine L, et al. Protection of the human gut microbiome from antibiotics. J Infect Dis. 2018 Jan 30;217(4):628–636. doi:10.1093/infdis/jix604.
   PubMed Web of Science ®Google Scholar
• Kaleko M, Bristol JA, Hubert S, Parsley T, Widmer G, Tzipori S, Subramanian P, Hasan N, Koski P, Kokai-Kun J, et al. Development of SYN-004, an oral beta-lactamase treatment to protect the gut microbiome from antibiotic-mediated damage and prevent Clostridium difficile infection. Anaerobe. 2016 Oct;41:58–67. doi:10.1016/j.anaerobe.2016.05.015.
   PubMed Web of Science ®Google Scholar
• Lehar SM, Pillow T, Xu M, Staben L, Kajihara KK, Vandlen R, DePalatis L, Raab H, Hazenbos WL, Hiroshi Morisaki J, et al. Novel antibody-antibiotic conjugate eliminates intracellular S. aureus. Nature. 2015 Nov 19;527(7578):323–328. doi:10.1038/nature16057.
   PubMed Web of Science ®Google Scholar
• Bikard D, Euler CW, Jiang W, Nussenzweig PM, Goldberg GW, Duportet X, Fischetti VA, Marraffini LA. Exploiting CRISPR-Cas nucleases to produce sequence-specific antimicrobials. Nat Biotechnol. 2014 Nov;32(11):1146–1150. doi:10.1038/nbt.3043.
   PubMed Web of Science ®Google Scholar
• Makki K, Deehan EC, Walter J, Backhed F. The impact of dietary fiber on gut microbiota in host health and disease. Cell Host Microbe. 2018 Jun 13;23(6):705–715. doi:10.1016/j.chom.2018.05.012.
   PubMed Web of Science ®Google Scholar
• De Vrese M, Schrezenmeir J. Probiotics, prebiotics, and synbiotics. Adv Biochem Eng Biotechnol. 2008;111:1–66. doi:10.1007/10_2008_097.
   PubMed Web of Science ®Google Scholar
• Gerbitz A, Schultz M, Wilke A, Linde H-J, Scholmerich J, Andreesen R, Holler E. Probiotic effects on experimental graft-versus-host disease: let them eat yogurt. Blood. 2004 Jun 1;103(11):4365–4367. doi:10.1182/blood-2003-11-3769.
   PubMed Web of Science ®Google Scholar
• Gorshein E, Wei C, Ambrosy S, Budney S, Vivas J, Shenkerman A, Manago J, McGrath MK, Tyno A, Lin Y. Lactobacillus rhamnosus GG probiotic enteric regimen does not appreciably alter the gut microbiome or provide protection against GVHD after allogeneic hematopoietic stem cell transplantation. Clin Transplant. 2017;31(5):May. doi:10.1111/ctr.12947.
   Web of Science ®Google Scholar
• Salminen MK, Rautelin H, Tynkkynen S, Poussa T, Saxelin M, Valtonen V, Jarvinen A. Lactobacillus bacteremia, clinical significance, and patient outcome, with special focus on probiotic L. rhamnosus GG. Clin Infect Dis. 2004 Jan 1;38(1):62–69. doi:10.1086/380455.
   PubMed Web of Science ®Google Scholar
• Robin F, Paillard C, Marchandin H, Demeocq F, Bonnet R, Hennequin C. Lactobacillus rhamnosus meningitis following recurrent episodes of bacteremia in a child undergoing allogeneic hematopoietic stem cell transplantation. J Clin Microbiol. 2010 Nov;48(11):4317–4319. doi:10.1128/JCM.00250-10.
   PubMed Web of Science ®Google Scholar
• Vahabnezhad E, Mochon AB, Wozniak LJ, Ziring DA. Lactobacillus bacteremia associated with probiotic use in a pediatric patient with ulcerative colitis. J Clin Gastroenterol. 2013 May-Jun;47(5):437–439. doi:10.1097/MCG.0b013e318279abf0.
   PubMed Web of Science ®Google Scholar
• Mehta A, Rangarajan S, Borate U. A cautionary tale for probiotic use in hematopoietic SCT patients-Lactobacillus acidophilus sepsis in a patient with mantle cell lymphoma undergoing hematopoietic SCT. Bone Marrow Transplant. 2013 Mar;48(3):461–462. doi:10.1038/bmt.2012.153.
   PubMed Web of Science ®Google Scholar
• Ambesh P, Stroud S, Franzova E, Gotesman J, Sharma K, Wolf L, Kamholz S. Recurrent lactobacillus bacteremia in a patient with leukemia. J Investig Med High Impact Case Rep. 2017 Oct-Dec;5(4):2324709617744233. doi:10.1177/2324709617744233.
   Google Scholar
• Suez J, Zmora N, Zilberman-Schapira G, Mor U, Dori-Bachash M, Bashiardes S, Zur M, Regev-Lehavi D, Ben-Zeev Brik R, Federici S. Post-antibiotic gut mucosal microbiome reconstitution is impaired by probiotics and improved by autologous FMT. Cell. 2018 Sep 6;174(6):1406–1423 e16. doi:10.1016/j.cell.2018.08.047.
   PubMed Web of Science ®Google Scholar
• Cooper TE, Scholes-Robertson N, Craig JC, Hawley CM, Howell M, Johnson DW, Teixeira-Pinto A, Jaure A, Wong G. Synbiotics, prebiotics and probiotics for solid organ transplant recipients. Cochrane Database Syst Rev. 2022 Sep 20;9(9):CD014804. doi:10.1002/14651858.CD014804.pub2.
   PubMedGoogle Scholar
• Simms-Waldrip TR, Sunkersett G, Coughlin LA, Savani MR, Arana C, Kim J, Kim M, Zhan X, Greenberg DE, Xie Y. Antibiotic-induced depletion of anti-inflammatory clostridia is associated with the development of graft-versus-host disease in pediatric stem cell transplantation patients. Biol Blood Marrow Transplant. 2017 May;23(5):820–829. doi:10.1016/j.bbmt.2017.02.004.
   PubMed Web of Science ®Google Scholar
• Kim SG, Becattini S, Moody TU, Shliaha PV, Littmann ER, Seok R, Gjonbalaj M, Eaton V, Fontana E, Amoretti L, et al. Microbiota-derived lantibiotic restores resistance against vancomycin-resistant Enterococcus. Nature. 2019 Aug;572(7771):665–669. doi:10.1038/s41586-019-1501-z.
   PubMed Web of Science ®Google Scholar
• Eiseman B, Silen W, Bascom GS, Kauvar AJ. Fecal enema as an adjunct in the treatment of pseudomembranous enterocolitis. Surgery. 1958 Nov;44(5):854–859.
   PubMed Web of Science ®Google Scholar
• Van Nood E, Dijkgraaf MG, Keller JJ, Fuentes S, Zoetendal EG, de Vos WM, Visser CE, Kuijper EJ, Bartelsman JFWM, Tijssen JGP. Duodenal infusion of donor feces for recurrent clostridium difficile. N Engl J Med. 2013 May 30;368(22):2145. doi:10.1056/NEJMc1303919.
   PubMedGoogle Scholar
• DeFilipp Z, Peled JU, Li S, Mahabamunuge J, Dagher Z, Slingerland AE, Del Rio C, Valles B, Kempner ME, Smith M, et al. Third-party fecal microbiota transplantation following allo-HCT reconstitutes microbiome diversity. Blood Adv. 2018 Apr 10;2(7):745–753. doi:10.1182/bloodadvances.2018017731.
   PubMed Web of Science ®Google Scholar
• Taur Y, Coyte K, Schluter J, Robilotti E, Figueroa C, Gjonbalaj M, Littmann ER, Ling L, Miller L, Gyaltshen Y, et al. Reconstitution of the gut microbiota of antibiotic-treated patients by autologous fecal microbiota transplant. Sci Transl Med. 2018 Sep 26;10(460). doi:10.1126/scitranslmed.aap9489
   PubMed Web of Science ®Google Scholar
• Spindelboeck W, Schulz E, Uhl B, Kashofer K, Aigelsreiter A, Zinke-Cerwenka W, Mulabecirovic A, Kump PK, Halwachs B, Gorkiewicz G, et al. Repeated fecal microbiota transplantations attenuate diarrhea and lead to sustained changes in the fecal microbiota in acute, refractory gastrointestinal graft- versus -host-disease. Haematologica. 2017 May;102(5):e210–e213. doi:10.3324/haematol.2016.154351.
   PubMed Web of Science ®Google Scholar
• Kaito S, Toya T, Yoshifuji K, Kurosawa S, Inamoto K, Takeshita K, Suda W, Kakihana K, Honda K, Hattori M, et al. Fecal microbiota transplantation with frozen capsules for a patient with refractory acute gut graft-versus-host disease. Blood Adv. 2018 Nov 27;2(22):3097–3101. doi:10.1182/bloodadvances.2018024968.
   PubMed Web of Science ®Google Scholar
• Qi X, Li X, Zhao Y, Wu X, Chen F, Ma X, Zhang F, Wu D. Treating steroid refractory intestinal acute graft-vs.-host disease with fecal microbiota transplantation: a pilot study. Front Immunol. 2018;9:2195. doi:10.3389/fimmu.2018.02195.
   PubMed Web of Science ®Google Scholar
• van Lier YF, Davids M, Haverkate NJE, de Groot PF, Donker ML, Meijer E, Heubel-Moenen FCJI, Nur E, Zeerleder SS, Nieuwdorp M, et al. 2020 Aug 12. Donor fecal microbiota transplantation ameliorates intestinal graft-versus-host disease in allogeneic hematopoietic cell transplant recipients. Sci Transl Med.12(556). doi:10.1126/scitranslmed.aaz8926
   PubMed Web of Science ®Google Scholar
• DeFilipp Z, Bloom PP, Torres Soto M, Mansour MK, Sater MRA, Huntley MH, Turbett S, Chung RT, Chen YB, Hohmann EL, et al. Drug-resistant E. coli bacteremia transmitted by fecal microbiota transplant. N Engl J Med. 2019 Nov 21;381(21):2043–2050. doi:10.1056/NEJMoa1910437.
   PubMed Web of Science ®Google Scholar
• Bilinski J, Lis K, Tomaszewska A, Pechcinska A, Grzesiowski P, Dzieciatkowski T, Walesiak A, Gierej B, Ziarkiewicz-Wroblewska B, Tyszka M, et al. Eosinophilic gastroenteritis and graft-versus-host disease induced by transmission of Norovirus with fecal microbiota transplant. Transpl Infect Dis. 2020 Jun 23;e13386. doi:10.1111/tid.13386.
   Web of Science ®Google Scholar
• Cammarota G, Ianiro G, Kelly CR, Mullish BH, Allegretti JR, Kassam Z, Putignani L, Fischer M, Keller JJ, Costello SP, et al. International consensus conference on stool banking for faecal microbiota transplantation in clinical practice. Gut. 2019 Dec;68(12):2111–2121. doi:10.1136/gutjnl-2019-319548.
   PubMed Web of Science ®Google Scholar
• Gibson GR, Hutkins R, Sanders ME, Prescott SL, Reimer RA, Salminen SJ, Scott K, Stanton C, Swanson KS, Cani PD, et al. Expert consensus document: the International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nat Rev Gastroenterol Hepatol. 2017 Aug;14(8):491–502. doi:10.1038/nrgastro.2017.75.
   PubMed Web of Science ®Google Scholar
• Tsilingiri K, Rescigno M. Postbiotics: what else? Benef Microbes. 2013 Mar 1;4(1):101–107. doi:10.3920/BM2012.0046.
   PubMed Web of Science ®Google Scholar
• Riwes M, Reddy P. Short chain fatty acids: postbiotics/metabolites and graft versus host disease colitis. Semin Hematol. 2020 Jan;57(1):1–6. doi:10.1053/j.seminhematol.2020.06.001.
   PubMed Web of Science ®Google Scholar
• Iyama S, Sato T, Tatsumi H, Hashimoto A, Tatekoshi A, Kamihara Y, Horiguchi H, Ibata S, Ono K, Murase K, et al. Efficacy of enteral supplementation enriched with glutamine, fiber, and oligosaccharide on mucosal injury following hematopoietic stem cell transplantation. Case Rep Oncol. 2014 Sep;7(3):692–699. doi:10.1159/000368714.
   PubMedGoogle Scholar
• Yoshifuji K, Inamoto K, Kiridoshi Y, Takeshita K, Sasajima S, Shiraishi Y, Yamashita Y, Nisaka Y, Ogura Y, Takeuchi R, et al. Prebiotics protect against acute graft-versus-host disease and preserve the gut microbiota in stem cell transplantation. Blood Adv. 2020 Oct 13;4(19):4607–4617. doi:10.1182/bloodadvances.2020002604.
   PubMed Web of Science ®Google Scholar
• Andermann TM, Fouladi F, Tamburini FB, Sahaf B, Tkachenko E, Greene C, Buckley MT, Brooks EF, Hedlin H, Arai S, et al. A fructo-oligosaccharide prebiotic is well tolerated in adults undergoing allogeneic hematopoietic stem cell transplantation: a phase I dose-escalation trial. Transplant Cell Ther. 2021 Nov;27(11):932e1–932 e11. doi:10.1016/j.jtct.2021.07.009.
   Google Scholar