Viral reactivations and associated outcomes in the context of immune reconstitution after pediatric hematopoietic cell transplantation

Journal of Allergy and Clinical Immunology

Volumn 140, Issue 6, 2017, Pages 1643-1650.e9

  Admiraal, Rick ^a   de Koning, Coco C H ^a   Lindemans, Caroline A ^a   Bierings, Marc B ^a   Wensing, Annemarie M J ^a   Versluys, A Birgitta ^a   Wolfs, Tom F W ^a   Nierkens, Stefan ^a   Boelens, Jaap Jan ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

clinical outcomes; hematopoietic cell transplantation; immune reconstitution; Viral reactivations

Indexed keywords

CIDOFOVIR; CYCLOSPORIN A; FOSCARNET; GANCICLOVIR; METHOTREXATE; PREDNISOLONE; RITUXIMAB;

ADENOVIRIDAE; ADENOVIRUS INFECTION; ADOLESCENT; ADULT; ALLOGENEIC HEMATOPOIETIC CELL TRANSPLANTATION; ALLOTRANSPLANTATION; ARTICLE; B LYMPHOCYTE; BK VIRUS; CD3+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL TRANSPLANTATION; CHILD; CLINICAL OUTCOME; COHORT ANALYSIS; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTION; EPSTEIN BARR VIRUS; EPSTEIN BARR VIRUS INFECTION; EVENT FREE SURVIVAL; FEMALE; FOLLOW UP; GRAFT FAILURE; GRAFT VERSUS HOST REACTION; HAZARD RATIO; HERPES VIRUS INFECTION; HUMAN; HUMAN HERPESVIRUS 6; IMMUNE RECONSTITUTION; IMMUNITY; MAJOR CLINICAL STUDY; MALE; MORTALITY; MULTIVARIATE ANALYSIS; NATURAL KILLER CELL; NONRELAPSE MORTALITY; OVERALL SURVIVAL; PRIORITY JOURNAL; PROPORTIONAL HAZARDS MODEL; RETROSPECTIVE STUDY; VIRUS LOAD; VIRUS REACTIVATION; HEMATOPOIETIC STEM CELL TRANSPLANTATION; INFANT; POSTOPERATIVE COMPLICATION; PRESCHOOL CHILD; SURVIVAL ANALYSIS; VIROLOGY; VIRUS ACTIVATION; YOUNG ADULT;

ADOLESCENT; ADULT; CHILD; CHILD, PRESCHOOL; FOLLOW-UP STUDIES; GRAFT VS HOST DISEASE; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMANS; IMMUNE RECONSTITUTION; INFANT; POSTOPERATIVE COMPLICATIONS; RETROSPECTIVE STUDIES; SURVIVAL ANALYSIS; VIRUS ACTIVATION; YOUNG ADULT;

EID: 85019097525     PISSN: 00916749     EISSN: 10976825     Source Type: Journal    
DOI: 10.1016/j.jaci.2016.12.992     Document Type: Article

References (34)

1. Bülmann, L., Buser, A.S., Cantoni, N., Gerull, S., Tichelli, A., Gratwohl, A., et al. Lymphocyte subset recovery and outcome after T-cell replete allogeneic hematopoietic SCT. Bone Marrow Transplant 46 (2011), 1357–1362.
2. Bartelink, I.H., Belitser, S.V., Knibbe, C.A., Danhof, M., de Pagter, A.J., Egberts, T.C., et al. Immune reconstitution kinetics as an early predictor for mortality using various hematopoietic stem cell sources in children. Biol Blood Marrow Transplant 19 (2013), 305–313.
3. Berger, M., Figari, O., Bruno, B., Raiola, A., Dominietto, A., Fiorone, M., et al. Lymphocyte subsets recovery following allogeneic bone marrow transplantation (BMT): CD4+ cell count and transplant-related mortality. Bone Marrow Transplant 41 (2008), 55–62.
4. Ritter, J., Seitz, V., Balzer, H., Gary, R., Lenze, D., Moi, S., et al. Donor CD4 T cell diversity determines virus reactivation in patients after HLA-matched allogeneic stem cell transplantation. Am J Transplant 15 (2015), 2170–2179.
5. Fedele, R., Martino, M., Garreffa, C., Messina, G., Console, G., Princi, D., et al. The impact of early CD4+ lymphocyte recovery on the outcome of patients who undergo allogeneic bone marrow or peripheral blood stem cell transplantation. Blood Transfus 10 (2012), 174–180.
6. Kim, D.H., Sohn, S.K., Won, D.I., Lee, N.Y., Suh, J.S., Lee, K.B., Rapid helper T-cell recovery above 200 × 106/L at 3 months correlates to successful transplant outcomes after allogeneic stem cell transplantation. Bone Marrow Transplant 37 (2006), 1119–1128.
7. Pourgheysari, B., Piper, K.P., McLarnon, A., Arrazi, J., Bruton, R., Clark, F., et al. Early reconstitution of effector memory CD4+ CMV-specific T cells protects against CMV reactivation following allogeneic SCT. Bone Marrow Transplant 43 (2009), 853–861.
8. Broers, A.E., van der Holt, R., van Esser, J.W., Gratama, J.-W., Henzen-Logmans, S., Kuenen-Boumeester, V., et al. Increased transplant-related morbidity and mortality in CMV-seropositive patients despite highly effective prevention of CMV disease after allogeneic T-cell-depleted stem cell transplantation. Blood 95 (2000), 2240–2245.
9. Chiesa, R., Gilmour, K., Qasim, W., Adams, S., Worth, A.J., Zhan, H., et al. Omission of in vivo T-cell depletion promotes rapid expansion of naive CD4+ cord blood lymphocytes and restores adaptive immunity within 2 months after unrelated cord blood transplant. Br J Haematol 156 (2012), 656–666.
10. Hiwarkar, P., Gaspar, H.B., Gilmour, K., Jagani, M., Chiesa, R., Bennett-Rees, N., et al. Impact of viral reactivations in the era of pre-emptive antiviral drug therapy following allogeneic haematopoietic SCT in paediatric recipients. Bone Marrow Translant 48 (2013), 803–806.
11. Glucksberg, H., Storb, R., Fefer, A., Buckner, C.D., Neiman, P.E., Clift, R.A., et al. Clinical manifestations of graft-versus-host disease in human recipients of marrow from HL-A-matched sibling donors. Transplantation 18 (1974), 295–304.
12. Shulman, H.M., Sullivan, K.M., Weiden, P.L., McDonald, G.B., Striker, G.E., Sale, G.E., et al. Chronic graft-versus-host syndrome in man. A long-term clinicopathologic study of 20 Seattle patients. Am J Med 69 (1980), 204–217.
13. Peters, S.G., Afessa, B., Acute lung injury after hematopoietic stem cell transplantation. Clin Chest Med 26 (2005), 561–569.
14. Admiraal, R., van Kesteren, C., Jol-van der Zijde, C.M., Lankester, A.C., Bierings, M.B., Egberts, T.C.G., et al. Association between anti-thymocyte globulin exposure and CD4+ immune reconstitution in paediatric haemopoietic cell transplantation: a multicentre, retrospective pharmacodynamic cohort analysis. Lancet Haematol 2 (2015), e194–e203.
15. Boeckh, M., Leisenring, W., Riddell, S.R., Bowden, R.A., Huang, M.L., Myerson, D., et al. Late cytomegalovirus disease and mortality in recipients of allogeneic hematopoietic stem cell transplants: importance of viral load and T-cell immunity. Blood 101 (2003), 407–414.
16. Servais, S., Lengline, E., Porcher, R., Carmagnat, M., Peffault de Latour, R., Robin, M., et al. Long-term immune reconstitution and infection burden after mismatched hematopoietic stem cell transplantation. Biol Blood Marrow Transpl 20 (2014), 507–517.
17. Bruno, B., Gooley, T., Hackman, R.C., Davis, C., Corey, L., Boeckh, M., Adenovirus infection in hematopoietic stem cell transplantation: effect of ganciclovir and impact on survival. Biol Blood Marrow Transplant 9 (2003), 341–352.
18. Auger, S., Orsini, M., Céballos, P., Fegueux, N., Kanouni, T., Caumes, B., et al. Controlled Epstein-Barr virus reactivation after allogeneic transplantation is associated with improved survival. Eur J Haematol 92 (2014), 421–428.
19. Gotoh, M., Yoshizawa, S., Katagiri, S., Suguro, T., Asano, M., Kitahara, T., et al. Human herpesvirus 6 reactivation on the 30th day after allogeneic hematopoietic stem cell transplantation can predict grade 2-4 acute graft-versus-host disease. Transpl Infect Dis 16 (2014), 440–449.
20. de Pagter, P.J., Schuurman, R., Keukens, L., Schutten, M., Cornelissen, J.J., van Baarle, D., et al. Human herpes virus 6 reactivation: important predictor for poor outcome after myeloablative, but not non-myeloablative allo-SCT. Bone Marrow Transpl 48 (2013), 1460–1464.
21. Zerr, D.M., Corey, L., Kim, H.W., Huang, M.L., Nguy, L., Boeckh, M., Clinical outcomes of human herpesvirus 6 reactivation after hematopoietic stem cell transplantation. Clin Infect Dis 40 (2005), 932–940.
22. Violago, L., Jin, Z., Bhatia, M., Rustia, E., Kung, A.L., Foca, M.D., et al. Human herpesvirus-6 viremia is not associated with poor clinical outcomes in children following allogeneic hematopoietic cell transplantation. Pediatr Transplant 19 (2015), 737–744.
23. Jaskula, E., Dlubek, D., Sedzimirska, M., Duda, D., Tarnowska, A., Lange, A., Reactivations of cytomegalovirus, human herpes virus 6, and Epstein-Barr virus differ with respect to risk factors and clinical outcome after hematopoietic stem cell transplantation. Transplant Proc 42 (2010), 3273–3276.
24. Green, M.L., Leisenring, W.M., Xie, H., Walter, R.B., Mielcarek, M., Sandmaier, B.M., et al. CMV reactivation after allogeneic HCT and relapse risk: evidence for early protection in acute myeloid leukemia. Blood 122 (2013), 1316–1324.
25. Schmidt-Hieber, M., Labopin, M., Beelen, D., Volin, L., Ehninger, G., Finke, J., et al. CMV serostatus still has an important prognostic impact in de novo acute leukemia patients after allogeneic stem cell transplantation: a report from the Acute Leukemia Working Party of EBMT. Blood 122 (2013), 3359–3364.
26. Teira, P., Battiwalla, M., Ramanathan, M., Barrett, A.J., Ahn, K.W., Chen, M., et al. Early cytomegalovirus reactivation remains associated with increased transplant related mortality in the current era: a CIBMTR analysis. Blood 127 (2016), 2427–2438.
27. Gilis, L., Morisset, S., Billaud, G., Ducastelle-Leprêtre, S., Labussière-Wallet, H., Nicolini, F.E., et al. High burden of BK virus-associated hemorrhagic cystitis in patients undergoing allogeneic hematopoietic stem cell transplantation. Bone Marrow Transplant 49 (2014), 664–670.
28. Admiraal, R., Lindemans, C.A., van Kesteren, C., Bierings, M.B., Versluys, A.B., Nierkens, S., et al. Excellent T-cell reconstitution and survival provided ATG exposure is low or absent after pediatric cord blood transplantation. Blood 128 (2016), 2734–2741.
29. de Koning, C., Nierkens, S., Boelens, J.J., Strategies before, during, and after hematopoietic cell transplantation to improve T-cell immune-reconstitution. Blood 128 (2016), 2607–2615.
30. Velardi, E., Tsai, J.J., Holland, A.M., Wertheimer, T., Yu, V.W., Zakrzewski, J.L., et al. Sex steroid blockade enhances thymopoiesis by modulating Notch signaling. J Exp Med 211 (2014), 2341–2349.
31. Nadal, E., Fowler, A., Kanfer, E., Apperley, J., Goldman, J., Dazzi, F., Adjuvant interleukin-2 therapy for patients refractory to donor lymphocyte infusions. Exp Hematol 32 (2004), 218–223.
32. Seggewiss, R., Einsele, H., Hematopoietic growth factors including keratinocyte growth factor in allogeneic and autologous stem cell transplantation. Semin Hematol 44 (2007), 203–211.
33. Perruccio, K., Bonifazi, P., Topini, F., Tosti, A., Bozza, S., Aloisi, T., et al. Thymosin alpha1 to harness immunity to pathogens after haploidentical hematopoietic transplantation. Ann N Y Acad Sci 1194 (2010), 153–161.
34. Nierkens, S., Lankester, A.C., Egeler, R.M., Bader, P., Locatelli, F., Pulsipher, M.A., et al. Challenges in the harmonization of immune monitoring studies and trial design for cell-based therapies in the context of hematopoietic cell transplantation for pediatric cancer patients. Cytotherapy 17 (2015), 1667–1674.