Особенности Т-клеточного иммунного ответа у пациентов с онкогематологическими заболеваниями после перенесенной инфекции SARS-CoV-2 и вакцинации

Введение.  Онкогематологические больные являются одной из наиболее уязвимых групп для инфекционных заболеваний. Нарушения работы иммунной системы, вызванные заболеванием и/или его терапией, негативно влияют на длительность и тяжесть инфекции, приводят к повышенному риску смерти и снижают эффективность вакцинации. Однако компенсаторные механизмы, позволяющие иммунокомпрометированным больным бороться с вирусной инфекцией, не до конца изучены.

Цель: систематизировать знания о формировании иммунного ответа у онкогематологических больных с нарушениями гуморального или клеточного звена.

Основные сведения. Проведен анализ особенностей Т-клеточного иммунного ответа у  онкогематологических больных. Обсуждено, как разнообразие репертуара Т-клеточных рецепторов может влиять на эффективную элиминацию и защиту от заражения вирусом SARS-CoV-2.

1. Wood W.A., Neuberg D.S., Thompson J.C., et al. Outcomes of patients with hematologic malignancies and COVID-19: a report from the ASH Research Collaborative Data Hub. Blood Adv. 2020; 4: 5966–75. DOI: 10.1182/bloodadvances.2020003170.

2. Dhodapkar M.V., Dhodapkar K.M., Ahmed R. Viral Immunity and Vaccines in Hematologic Malignancies: Implications for COVID-19. Blood Cancer Discov. 2021; 2: 9–12. DOI: 10.1158/2643-3230.BCD-20-0177.

3. Aleshina O.A., Zakurdaeva K., Vasileva A.N., et al. Clinical Outcomes in Patients With COVID-19 and Hematologic Disease. Clin Lymphoma Myeloma Leuk. 2023; 23: 589–98. DOI: 10.1016/j.clml.2023.04.002.

4. Bange E.M., Han N.A., Wileyto P., et al. CD8+ T cells contribute to survival in patients with COVID-19 and hematologic cancer. Nat Med. 2021; 27: 1280–9. DOI: 10.1038/s41591-021-01386-7.

5. Gur I, Giladi A., Isenberg Y.N., Neuberger A., Stern A. COVID-19 in Patients with Hematologic Malignancies: Clinical Manifestations, Persistence, and Immune Response. Acta Haematol. 2022; 145: 297–309. DOI: 10.1159/000523872.

6. Fendler A., Au L., Shepherd S.T.C., et al. Functional antibody and T cell immunity following SARS-CoV-2 infection, including by variants of concern, in patients with cancer: the CAPTURE study. Nat Cancer. 2021; 2: 1321–37. DOI: 10.1038/s43018-021-00275-9.

7. Abdul-Jawad S., Bau L., Alaguthurai T., et al. Acute Immune Signatures and Their Legacies in Severe Acute Respiratory Syndrome Coronavirus-2 Infected Cancer Patients. Cancer Cell. 2021; 39: 257–75.e6. DOI: 10.1016/j.ccell.2021.01.001.

8. Kuderer N.M., Choueiri T.K., Shah D.P., et al. Clinical impact of COVID-19 on patients with cancer (CCC19): a cohort study. Lancet. 2020; 395: 1907–18.

9. Shin D.H., Gillard A., Van Wieren A., et al. Remission of liquid tumors and SARS-CoV-2 infection: A literature review. Mol Ther Oncolytics. 2022; 26: 135–40. DOI: 10.1016/j.omto.2022.06.006.

10. Meo C., Palma G., Bruzzese F., et al. Spontaneous cancer remission after COVID-19: insights from the pandemic and their relevance for cancer treatment. J Transl Med. 2023; 21: 273. DOI: 10.1186/s12967-023-04110-w.

11. Zornikova K.V., Sheetikov S.A., Rusinov A.Y., et al. Architecture of the SARSCoV-2-specific T cell repertoire. Front Immunol. 2023; 14: 1070077. DOI: 10.3389/fimmu.2023.1070077.

12. Xu J., Li X., Yuan N., et al. T cell receptor β repertoires in patients with COVID-19 reveal disease severity signatures. Front Immunol. 2023; 14: 1190844. DOI: 10.3389/fimmu.2023.1190844.

13. Park J.J., Lee K.A.V., Lam S.Z., et al. Machine learning identifies T cell receptor repertoire signatures associated with COVID-19 severity. Commun Biol. 2023; 6: 1–13. DOI: 10.1038/s42003-023-04447-4.

14. Galson J.D., Schaetzle S., Bashford-Rogers R.J.M., et al. Deep Sequencing of B Cell Receptor Repertoires From COVID-19 Patients Reveals Strong Convergent Immune Signatures. Front Immunol. 2020; 11:605170. DOI: 10.3389/fimmu.2020.605170.

15. Farmanbar A., Kneller R., Firouzi S. RNA sequencing identifies clonal structure of T-cell repertoires in patients with adult T-cell leukemia/lymphoma. npj Genom Med. 2019; 4: 1–9. DOI: 10.1038/s41525-019-0084-9.

16. Vardi A., Agathangelidis A., Stalika E., et al. Antigen Selection Shapes the T-cell Repertoire in Chronic Lymphocytic Leukemia. Clin Cancer Res. 2016; 22: 167–74. DOI: 10.1158/1078-0432.CCR-14-3017.

17. Wang X., Chen Y., Li Z., et al. Single‐Cell RNA‐Seq of T Cells in B‐ALL Patients Reveals an Exhausted Subset with Remarkable Heterogeneity. Adv Sci. 2021; 8: 2101447. DOI: 10.1002/advs.202101447.

18. Keane C., Gould C., Jones K., et al. The T-cell Receptor Repertoire Influences the Tumor Microenvironment and Is Associated with Survival in Aggressive B-cell Lymphoma. Clin Cancer Res. 2017; 23: 1820–28. DOI: 10.1158/1078-0432.CCR-16-1576.

19. Liu X., Venkataraman G., Lin J., et al. Highly clonal regulatory T-cell population in follicular lymphoma — inverse correlation with the diversity of CD8+ T cells. Oncoimmunology. 2015; 4: e1002728. DOI: 10.1080/2162402X.2014.1002728.

20. Rieken J., Bernard V., Witte H.M., et al. Exhaustion of tumour‐infiltrating T‐cell receptor repertoire diversity is an age‐dependent indicator of immunological fitness independently predictive of clinical outcome in Burkitt lymphoma. Br J Haematol. 2021; 193: 138–49. DOI: 10.1111/bjh.17083.

21. Iyer A., Hennessey D., Gniadecki R. Clonotype pattern in T-cell lymphomas map the cell of origin to immature lymphoid precursors. Blood Adv. 2022; 6: 2334–45. DOI: 10.1182/bloodadvances.2021005884.

22. Jiang W., Zhou S., Li J., et al. The BCR repertoire comparison, lymphoma typing model and OS predicted model in 5 different pathological lymphomas: T-LBL/ALL, PTCL-NOS, B-MCL, B-FL, and DLBCL. JCO. 2020; 38: 8059. DOI: 10.1200/JCO.2020.38.15_suppl.8059.

23. Zhang J., Hu X., Wang J., et al. Immune receptor repertoires in pediatric and adult acute myeloid leukemia. Genome Med. 2019; 11: 73. DOI: 10.1186/s13073-019-0681-3.

24. Fozza C., Longinotti M. T-cell receptor repertoire usage in hematologic malignancies. Crit Rev Oncol Hematol. 2013; 86: 201–11. DOI: 10.1016/j.critrevonc.2012.11.005.

25. Hellerstein M. What are the roles of antibodies versus a durable, high quality T-cell response in protective immunity against SARS-CoV-2? Vaccine: X. 2020; 6: 100076. DOI: 10.1016/j.jvacx.2020.100076.

26. Vilar-Compte D., Shah DP, Vanichanan J., et al. Influenza in Patients with Hematological Malignancies: Experience at Two Comprehensive Cancer Centers. J Med Virol. 2018; 90: 50–60. DOI: 10.1002/jmv.24930.

27. Marchesi F., Pimpinelli F., Ensoli F., Mengarelli A. Cytomegalovirus infection in hematologic malignancy settings other than the allogeneic transplant. Hematol Oncol. 2018; 36: 381–91. DOI: 10.1002/hon.2453.

28. Manna A., Pronzato P., Cordani S., Canessa P. CMV infection and pneumonia in hematological malignancies. J Infect Chemother. 2003; 9: 265–67. DOI: 10.1007/s10156-003-0251-9.

29. Atkins S., He F. Chemotherapy and Beyond. Infect Dis Clin North Am. 2019; 33: 289–309. DOI: 10.1016/j.idc.2019.01.001.

30. Busca A. Viral infections in patients with hematological malignancies. Leukemia Suppl. 2012; 1: S24–5. DOI: 10.1038/leusup.2012.15.

31. Wade J.C. Viral Infections in Patients with Hematological Malignancies. Hematology. 2006: 368–74. DOI: 10.1182/asheducation-2006.1.368.

32. Sato K., Igarashi S., Tsukada N., et al. Cytomegalovirus infection in patients with malignant lymphomas who have not received hematopoietic stem cell transplantation. BMC Cancer. 2022; 22: 944. DOI: 10.1186/s12885-022-10008-5.

33. Shimizu K., Iyoda T., Sanpei A., et al. Identification of TCR repertoires in functionally competent cytotoxic T cells cross-reactive to SARS-CoV-2. Commun Biol. 2021; 4: 1–13. DOI: 10.1038/s42003-021-02885-6.

34. Mallajosyula V., Ganjavi C., Chakraborty S., et al. CD8 + T cells specific for conserved coronavirus epitopes correlate with milder disease in patients with COVID-19. Sci Immunol. 2021; 6: eabg5669. DOI: 10.1126/sciimmunol.abg5669.

35. DiLillo D.J., Weinberg J.B., Yoshizaki A., et al. Chronic lymphocytic leukemia and regulatory B cells share IL-10 competence and immunosuppressive function. Leukemia. 2013; 27: 170–82. DOI: 10.1038/leu.2012.165.

36. D’Arena G., Laurenti L., Minervini M.M., et al. Regulatory T-cell number is increased in chronic lymphocytic leukemia patients and correlates with progressive disease. Leuk Res. 2011; 35: 363–8. DOI: 10.1016/j.leukres.2010.08.010.

37. Lyudovyk O., Kim J.Y., Qualls D., et al. Impaired humoral immunity is associated with prolonged COVID-19 despite robust CD8 T cell responses. Cancer Cell. 2022; 40: 738–53.e5. DOI: 10.1016/j.ccell.2022.05.013.

38. Bilich T., Roerden M., Maringer Y., et al. Preexisting and Post–COVID-19 Immune Responses to SARS-CoV-2 in Patients with Cancer. Cancer Discov. 2021; 11: 1982–95. DOI: 10.1158/2159-8290.CD-21-0191.

39. Baden L.R., El Sahly H.M., Essink B., et al. Efficacy and Safety of the mRNA-1273 SARS-CoV-2 Vaccine. N Engl J Med. 2021; 384: 403–16. DOI: 10.1056/NEJMoa2035389.

40. Thakkar A., Gonzalez-Lugo J.D., Goradia N., et al. Seroconversion rates following COVID-19 vaccination among patients with cancer. Cancer Cell. 2021; 39: 1081–90.e2. DOI: 10.1016/j.ccell.2021.06.002.

41. Fendler A., Shepherd S.T.C., Au L., et al. Adaptive immunity and neutralizing antibodies against SARS-CoV-2 variants of concern following vaccination in patients with cancer: The CAPTURE study. Nat Cancer. 2021; 2: 1321–37. DOI: 10.1038/s43018-021-00274-w.

42. Peeters M., Verbruggen L., Teuwen L., et al. Reduced humoral immune response after BNT162b2 coronavirus disease 2019 messenger RNA vaccination in cancer patients under antineoplastic treatment. ESMO Open. 2021; 6: 100274. DOI: 10.1016/j.esmoop.2021.100274.

43. Chung A., Banbury B., Vignali M., et al. Antibody and T‐cell responses by ultra‐deep T‐cell receptor immunosequencing after COVID ‐19 vaccination in patients with plasma cell dyscrasias. Br J Haematol. 2022; 199: 520–8. DOI: 10.1111/bjh.18434.

44. Uaprasert N., Pitakkitnukun P., Tangcheewinsirikul N., et al. Immunogenicity and risks associated with impaired immune responses following SARS-CoV-2 vaccination and booster in hematologic malignancy patients: an updated meta-analysis. Blood Cancer J. 2022; 12: 1–13. DOI: 10.1038/s41408-022-00776-5.

45. Nguyen T.H.O., Rowntree L.C., Allen L.F., et al. Robust SARS-CoV-2 T cell responses with common TCRαβ motifs toward COVID-19 vaccines in patients with hematological malignancy impacting B cells. Cell Rep Med. 2023; 4: 101017. DOI: 10.1016/j.xcrm.2023.101017.

46. Greenberger L.M., Saltzman L.A., Gruenbaum L.M., et al. Anti-spike Tcell and Antibody Responses to SARS-CoV-2 mRNA Vaccines in Patients with Hematologic Malignancies. Blood Cancer Discov. 2022; 3: 481–9. DOI: 10.1158/2643-3230.BCD-22-0077.

47. Marasco V., Carniti C., Guidetti A. et.al. T-cell immune response after mRNA SARS-CoV-2 vaccines is frequently detected also in the absence of seroconversion in patients with lymphoid malignancies. Br J Haematol. 2022; 196(3): 548–58. DOI: 10.1111/bjh.17877.

48. Keppler-Hafkemeyer A., Greil C., Wratil P.R., et al. Potent high-avidity neutralizing antibodies and T cell responses after COVID-19 vaccination in individuals with B cell lymphoma and multiple myeloma. Nat Cancer. 2023; 4: 81–95. DOI: 10.1038/s43018-022-00502-x.

49. Goel S., Griffiths E.A., Segal B., et al. Antigen-Specific T-Cell Repertoire Responses Following COVID-19 Vaccination Are Intact in Majority of Patients with B-Cell Lymphoid Malignancies on Active Therapy. Blood. 2023; 142: 5714. DOI: 10.1182/blood-2023-190914.

50. Painter M.M., Mathew D., Goel R.R., et al. Rapid induction of antigen-specific CD4+ T cells is associated with coordinated humoral and cellular immunity to SARS-CoV-2 mRNA vaccination. Immunity. 2021; 54: 2133–42.e3. DOI: 10.1016/j.immuni.2021.08.001.

51. Alimam S., Ann Timms J., Harrison C.N., et al. Altered immune response to the annual influenza A vaccine in patients with myeloproliferative neoplasms. Br J Haematol. 2021; 193: 150–4. DOI: 10.1111/bjh.17096.

52. Mariotti J., Spina F., Carniti C., et al. Long‐term patterns of humoral and cellular response after vaccination against influenza A (H1N1) in patients with hematologic malignancies. Eur J Haematol. 2012; 89: 111–9. DOI: 10.1111/j.1600-0609.2012.01793.x.

53. Touizer E, Alrubayyi A., Rees-Spear C., et al. Failure to seroconvert after two doses of BNT162b2 SARS-CoV-2 vaccine in a patient with uncontrolled HIV. Lancet HIV. 2021;8:e317–8. DOI: 10.1016/S2352-3018(21)00099-0.

54. Kamar N., Abravanel F., Marion O., et al. Three Doses of an mRNA Covid-19 Vaccine in Solid-Organ Transplant Recipients. N Engl J Med. 2021; 385: 661–2. DOI: 10.1056/NEJMc2108861.

55. Gao Y., Cai C., Wullimann D., et al. Immunodeficiency syndromes differentially impact the functional profile of SARS-CoV-2-specific T cells elicited by mRNA vaccination. Immunity. 2022; 55: 1732–46.e5. DOI: 10.1016j.immuni.2022.07.005.

56. Brown R.D., Pope B., Murray A., et al. Dendritic cells from patients with myeloma are numerically normal but functionally defective as they fail to up-regulate CD80 (B7-1) expression after huCD40LT stimulation because of inhibition by transforming growth factor-β1 and interleukin-10. Blood. 2001; 98:2992–8. DOI: 10.1182/blood.V98.10.2992.

57. Ramasamy K., Sadler R., Jeans S., et a. Immune response to COVID ‐19 vaccination is attenuated by poor disease control and antimyeloma therapy with vaccine driven divergent T‐cell response. Br J Haematol. 2022; 197: 293. DOI: 10.1111/bjh.18066.

58. Abdul-Jawad S., Beatson R., Lechmere T., et al. BNT162b2 COVID-19 and ChAdOx1 nCoV-19 vaccination in patients with myelodysplastic syndromes. Haematologica. 2022; 107: 1181–4. DOI: 10.3324/haematol.2021.280337.

59. Chuleerarux N., Manothummetha K., Moonla C., et al. Immunogenicity of SARS-CoV-2 vaccines in patients with multiple myeloma: a systematic review and meta-analysis. Blood Adv. 2022; 6: 6198–207. DOI: 10.1182/bloodadvances.2022008530.

60. Pfannes R., Pierzchalski A., Maddalon A., et al. Characterization of postvaccination SARS-CoV-2 T cell subtypes in patients with different hematologic malignancies and treatments. Front Immunol. 2023; 14. DOI: 10.3389/fimmu.2023.1087996.

61. En.le J.C., Campe J., Schwenger A., et al. Severe impairment of T-cell responses to BNT162b2 immunization in patients with multiple myeloma. Blood. 2022; 139: 137–42. DOI: 10.1182/blood.2021013429.

62. Booth S., Willan J., Wong H., et al. Regional outcomes of severe acute respiratory syndrome coronavirus 2 infection in hospitalised patients with haematological malignancy. Eur J Haematol 2020; 105: 476–83. DOI: 10.1111/ejh.13469.

63. Солопова Г.Г., Цыганова Е.В., Кондрашова А.В. и др. Особенности течения новой коронавирусной инфекции COVID-19 у детей с онкологическими, онкогематологическими и тяжелыми иммунологическими заболеваниями. Опыт НМИЦ ДГОИ им. Дмитрия Рогачева. Вопросы гематологии/онкологии и иммунопатологии в педиатрии. 2021; 20(4): 89-99. DOI: 10.24287/1726-1708-2021-20-4-89-99.

64. Akatsuka Y., Cerveny C., Hansen J.A. T cell receptor clonal diversity following allogeneic marrow grafting. Human Immunol. 1996; 48: 125–34. DOI: 10.1016/0198-8859(96)00082-1.

65. Bomberger C., Singh-Jairam M., Rodey G., et al. Lymphoid Reconstitution After Autologous PBSC Transplantation With FACS-Sorted CD34+ Hematopoietic Progenitors. Blood. 1998; 91: 2588–600. DOI: 10.1182/blood.V91.7.2588.

66. Roux E., Helg C., Dumont-Girard F., et al. Analysis of T-Cell Repopulation After Allogeneic Bone Marrow Transplantation: Significant Differences Between Recipients of T-Cell Depleted and Unmanipulated Grafts. Blood. 1996; 87: 3984–92. DOI: 10.1182/blood.V87.9.3984.bloodjournal8793984.

67. Sugita K., Soiffer R.J., Murray C., et al. The phenotype and reconstitution of immunoregulatory T cell subsets after T cell-depleted allogeneic and autologous bone marrow transplantation. Transplantation. 1994; 57: 1465–73.

68. Dumont-Girard F., Roux E., van Lier R.A., et al. Reconstitution of the T-Cell Compartment After Bone Marrow Transplantation: Restoration of the Repertoire by Thymic Emigrants. Blood. 1998; 92: 4464–71. DOI: 10.1182/blood.V92.11.4464.

69. Keever C.A., Small T.N., Flomenberg N., et al. Immune Reconstitution Following Bone Marrow Transplantation: Comparison of Recipients of T-Cell Depleted Marrow With Recipients of Conventional Marrow Grafts. Blood. 1989; 73: 1340–50. DOI: 10.1182/blood.V73.5.1340.1340.

70. Porman S.J., Nocker P., Gallagher M., et al. Pattern of T cell reconstitution following allogeneic bone marrow transplantation for acute hematological malignancy. Transplantation. 1982; 34: 96. DOI: 10.1097/00007890-198208000-00007.

71. Small T.N., Papadopoulos E.B., Boulad F., et al. Comparison of Immune Reconstitution After Unrelated and Related T-Cell–Depleted Bone Marrow Transplantation: Effect of Patient Age and Donor Leukocyte Infusions. Blood. 1999; 93: 467–80. DOI: 10.1182/blood.V93.2.467.

72. Park B.G., Park C-J, Jang S., et al. Reconstitution of lymphocyte subpopulations after hematopoietic stem cell transplantation: comparison of hematologic malignancies and donor types in event-free patients. Leuk Res. 2015; 39: 1334–41. DOI: 10.1016/j.leukres.2015.09.010.

73. Abdel-Azim H., Elshoury A., Mahadeo K.M., et al. Humoral Immune Reconstitution Kinetics after Allogeneic Hematopoietic Stem Cell Transplantation in Children: A Maturation Block of IgM Memory B Cells May Lead to Impaired Antibody Immune Reconstitution. Biol Blood Marrow Transplant. 2017; 23: 1437–46. DOI: 10.1016/j.bbmt.2017.05.005.

74. Mushtaq M.U., Shahzad M., Chaudhary S.G., et al. Impact of SARS-CoV-2 in Hematopoietic Stem Cell Transplantation and Chimeric Antigen Receptor T Cell Therapy Recipients. Transplant Cell Ther. 2021; 27: 796.e1-e7. DOI: 10.1016/j.jtct.2021.07.005.

75. Fox T.A., Kirkwood A.A., Enfield L., et al. Low seropositivity and suboptimal neutralisation rates in patients fully vaccinated against COVID‐19 with B‐cell malignancies. Br J Haematol. 2021; 195: 706–9. DOI: 10.1111/bjh.17836.

76. Abbas H.A., Hao D., Tomczak K., et al. Single cell T cell landscape and T cell receptor repertoire profiling of AML in context of PD-1 blockade therapy. Nat Commun. 2021; 12: 6071. DOI: 10.1038/s41467-021-26282-z.

77. Kagamu H., Kitano S., Yamaguchi O., et al. CD4+ T-cell Immunity in the Peripheral Blood Correlates with Response to Anti-PD-1 Therapy. Cancer Immunol Res. 2020; 8: 334–44. DOI: 10.1158/2326-6066.CIR-19-0574.

78. Robilotti E.V., Babady N.E., Mead P.A., et al. Determinants of Severity in Cancer Patients with COVID-19 Illness. Nat Med. 2020; 26: 1218–23. DOI: 10.1038/s41591-020-0979-0.

79. Chari A., Samur M.K., Martinez-Lopez J., et al. Clinical features associated with COVID-19 outcome in multiple myeloma: first results from the International Myeloma Society data set. Blood. 2020; 136: 3033–40. DOI: 10.1182/blood.2020008150.

80. Lin W-L, Nguyen T-H-Y, Wu L-M, et al. Anticancer Therapy and Mortality of Adult Patients with Hematologic Malignancy and COVID-19: A Systematic Review and Meta-Analysis. Life. 2023; 13: 381. DOI: 10.3390/life13020381.

81. Liu H., Yang D., Chen X., et al. The effect of anticancer treatment on cancer patients with COVID‐19: A systematic review and meta‐analysis. Cancer Med. 2020; 10: 1043–56. DOI: 10.1002/cam4.3692.

82. Dulery R., Lamure S., Delord M., et al. Prolonged in‐hospital stay and higher mortality after Covid‐19 among patients with non‐Hodgkin lymphoma treated with B‐cell depleting immunotherapy. Am J Hematol. 2021; 96: 934–44. DOI: 10.1002/ajh.26209.

83. Booth S., Curley H.M., Varnai C., et al. Key findings from the UKCCMP cohort of 877 patients with haematological malignancy and COVID‐19: disease control as an important factor relative to recent chemotherapy or anti‐CD20 therapy. Br J Haematol. 2022; 196: 892–901. DOI: 10.1111/bjh.17937.

84. Basquiera A.L., Garcia M.J., Martinez Rolon J., et al. Clinical characteristics and evolution of hematological patients and COVID-19 in Argentina: a report from the Argentine Society of Hematology. Medicina. 2021; 81: 536–45. DOI: 10.21203/rs.3.rs-162289/v1.

85. Bange E., Han N., Wileyto E.P., et al. CD8 T cells compensate for impaired humoral immunity in COVID-19 patients with hematologic cancer. Nat Med. 2021; 27: 1280–9 . DOI: 10.1038/s41591-021-01386-7.

86. Jarisch A., Wiercinska E., Huenecke S., et al. Immune Responses to SARSCoV-2 Vaccination in Young Patients with Anti-CD19 Chimeric Antigen Receptor T Cell-Induced B Cell Aplasia. Transplant Cell Ther. 2022; 28: 366.e1–e7. DOI: 10.1016/j.jtct.2022.04.017.

87. Atanackovic D., Luetkens T., Omili D., et al. Vaccine-induced T-cell responses against SARS-CoV-2 and its Omicron variant in patients with B cell–depleted lymphoma after CART therapy. Blood. 2022; 140: 152–6. DOI: 10.1182/blood.2022016175.

88. Parvathaneni K., Torres-Rodriguez K., Meng W., et al. SARS-CoV-2 Spike-Specific T-Cell Responses in Patients With B-Cell Depletion Who Received Chimeric Antigen Receptor T-Cell Treatments. JAMA Oncol. 2022; 8: 164. DOI: 10.1001/jamaoncol.2021.6030.

89. Atanackovic D., Kreitman R.J., Cohen J., et al. T cell responses against SARSCoV-2 and its Omicron variant in a patient with B cell lymphoma after multiple doses of a COVID-19 mRNA vaccine. J Immunother Cancer. 2022; 10: e004953. DOI: 10.1136/jitc-2022-004953.

90. Riise J., Meyer S., Blaas I., et al. Rituximab‐treated patients with lymphoma develop strong CD8 T‐cell responses following COVID ‐19 vaccination. Br J Haematol. 2022; 197: 697–708. DOI: 10.1111/bjh.18149.

91. Nucci M., Anaissie E. Infections in Patients with Multiple Myeloma in the Era of High‐Dose Therapy and Novel Agents. Clin Infect Dis. 2009; 49: 1211–25. DOI: 10.1086/605664.

92. Seggewiss R., Einsele H. Immune reconstitution after allogeneic transplantation and expanding options for immunomodulation: an update. Blood. 2010; 115: 3861–68. DOI: 10.1182/blood-2009-12-234096.

93. Rieger C.T., Liss B., MellinghoffS., et al. Anti-infective vaccination strategies in patients with hematologic malignancies or solid tumors—Guideline of the Infectious Diseases Working Party (AGIHO) of the German Society for Hematology and Medical Oncology (DGHO). Ann Oncol. 2018; 29: 1354–65. DOI: 10.1093/annonc/mdy117.

94. Ullmann A.J., Schmidt-Hieber M., Bertz H., et al. Infectious diseases in allogeneic haematopoietic stem cell transplantation: prevention and prophylaxis strategy guidelines 2016. Ann Hematol. 2016; 95: 1435–55. DOI: 10.1007/s00277-016-2711-1.

95. Hata A., Asanuma H., Rinki M., et al. Use of an Inactivated Varicella Vaccine in Recipients of Hematopoietic-Cell Transplants. N Engl J Med. 2002; 347: 26–34. DOI: 10.1056/NEJMoa013441.

96. Lindemann M., Klisanin V., Thummler L. et al . Humoral and Cellular Vaccination Responses against SARS-CoV-2 in Hematopoietic Stem Cell Transplant Recipients. Vaccine. 2021; 9: 1075. DOI: 10.3390/vaccines9101075.

97. Миронова Д.А., Васильева В.А., Дроков М.Ю. и др. Инфекция COVID-19 у больных, перенесших трансплантацию аллогенных гемопоэтических стволовых клеток. Гематология и трансфузиология. 2024;69(1):8–19. DOI: 10.35754/0234-5730-2024-69-1-8-19.

98. Sharma A., Bhatt N.S., St Martin A., et al. Clinical characteristics and outcomes of COVID-19 in haematopoietic stem-cell transplantation recipients: an observational cohort study. The Lancet Haematol. 2021; 8: e185–93. DOI: 10.1016/S2352-3026(20)30429-4.

99. Hill J.A., Martens M.J., Young J-A.H., et al. SARS-CoV-2 vaccination in the fi rst year after allogeneic hematopoietic cell transplant: a prospective, multicentre, observational study. eClinicalMedicine. 2023; 59: 101983. DOI: 10.1016/j.eclinm.2023.101983.

100. Pradier A., Mamez A.C., Stephan C., et al. T cell receptor sequencing reveals reduced clonal breadth of T-cell responses against SARS-CoV-2 after natural infection and vaccination in allogeneic hematopoietic stem cell transplant recipients. Ann Oncol. 2022; 33: 1333–5. DOI: 10.1016/j.annonc.2022.09.153.

101. VanOudenhove J., Liu Y., Nelakanti R., et al. Impact of Memory T Cells on SARS-COV-2 Vaccine Response in Hematopoietic Stem Cell Transplant. BioRxiv. 2023.10.26.564259. DOI: 10.1101/2023.10.26.564259.

102. Federico L., Tvedt T.H.A., Gainullin M., et al. Robust spike-specifi c CD4+ and CD8+ T cell responses in SARS-CoV-2 vaccinated hematopoietic cell transplantation recipients: a prospective, cohort study. Front Immunol. 2023; 14: 1210899. DOI: 10.3389/fimmu.2023.1210899.

103. Lazaro Del Campo P., De Paz Arias R., Ramirez Lopez A., et al. No transmission of SARS-CoV-2 in a patient undergoing allogeneic hematopoietic cell transplantation from a matched-related donor with unknown COVID-19. Transfus Apher Sci. 2020; 59: 102921. DOI: 10.1016/j.transci.2020.102921.

104. Leclerc M., Fourati S., Menouche D., et al. Allogeneic haematopoietic stem cell transplantation from SARS-CoV-2 positive donors. Lancet Haematol. 2021;8:e167–9. DOI: 10.1016/S2352-3026(21)00025-9.

105. Anurathapan U., Apiwattanakul N., Pakakasama S., et al. Hematopoietic stem cell transplantation from an infected SARS-CoV2 donor sibling. Bone Marrow Transplant. 2020; 55: 2359–60. DOI: 10.1038/s41409-020-0969-3.

106. Cho H.J., Koo J.W., Roh S.K., et al. COVID-19 transmission and blood transfusion: A case report. J Infect Public Health. 2020; 13: 1678–9. DOI: 10.1016/j.jiph.2020.05.001.

107. Katz L.M. Is SARS‐CoV ‐2 transfusion transmitted? Transfusion. 2020; 60: 1111–4. DOI: 10.1111/trf.15831.

108. Langhi D.M., De Souza R.C., Barros M., et al. SARS-COV-2: is it a risk for blood transfusion? Hematol Transfus Cell Ther. 2022; 44: 100–3. DOI: 10.1016/j.htct.2021.08.001.

109. Pannu S.R., Cardone M., Doraiswamy M., et al. SARS-CoV-2 IgG Seroconversion After Convalescent Plasma Transfusion Does Not Improve Hospital Outcomes in COVID-19. Chest Crit Care. 2024; 100048. DOI: 10.1016/j.chstcc.2024.100048.

110. La Rosa C., Chiuppesi F., Park Y., et al. Functional SARS-CoV-2-specific T cells of donor origin in allogeneic stem cell transplant recipients of a T-cell-replete infusion: A prospective observational study. Front Immunol. 2023; 14: 1114131. DOI: 10.3389/fimmu.2023.1114131.

111. La Rosa C., Chiuppesi F., Park Y., et al. Adoptive transfer of functional SARSCOV-2-specific immunity from donor graft to hematopoietic stem cell transplant recipients. Am J Hematol. 2022; 97: E404–7. DOI: 10.1002/ajh.26691.

112. Passamonti F., Cattaneo C., Arcaini L., et al. Clinical characteristics and risk factors associated with COVID-19 severity in patients with haematological malignancies in Italy: a retrospective, multicentre, cohort study. Lancet Haematol. 2020; 7: e737–45. DOI: 10.1016/S2352-3026(20)30251-9.

113. Pagano L., Salmanton-Garcia J., Marchesi F., et al. COVID-19 infection in adult patients with hematological malignancies: a European Hematology Association Survey (EPICOVIDEHA). J Hematol Oncol. 2021; 14: 168. DOI: 10.1186/s13045-021-01177-0.

114. Garcia-Suarez .J, De La Cruz J., Cedillo A., et al. Impact of hematologic malignancy and type of cancer therapy on COVID-19 severity and mortality: lessons from a large population-based registry study. J Hematol Oncol. 2020; 13: 133. DOI: 10.1186/s13045-020-00970-7.

115. Ribera J-M, Morgades M., Coll R., et al. Frequency, Clinical Characteristics and Outcome of Adults With Acute Lymphoblastic Leukemia and COVID 19 Infection in the First vs. Second Pandemic Wave in Spain. Clin Lymphoma Myeloma Leuk. 2021; 21: e801–9. DOI: 10.1016/j.clml.2021.06.024.

116. Azhdari Tehrani H., Ramezaninejad S., Mardani M., et al. Hematologic malignancies and COVID-19 infection: A monocenter retrospective study. Health SciRep 2022; 5: e638. DOI: 10.1002/hsr2.638.

117. Fox T.A., Troy-Barnes E., Kirkwood A.A., et al. Clinical outcomes and risk factors for severe COVID-19 in patients with haematological disorders receiving chemo- or immunotherapy. Br J Haematol 2020; 191: 194–206. DOI: 10.1111/bjh.17027.

118. Palanques-Pastor T., Megias-Vericat J.E., Martinez P., et al. Characteristics, clinical outcomes, and risk factors of SARS-COV-2 infection in adult acute myeloid leukemia patients: experience of the PETHEMA group. Leuk Lymphoma. 2021; 62: 2928–38. DOI: 10.1080/10428194.2021.1948031.

119. Stahl M., Narendra V., Jee J., et al. Neutropenia in adult acute myeloid leukemia patients represents a powerful risk factor for COVID-19 related mortality. Leuk Lymphoma. 2021; 62: 1940–8. DOI: 10.1080/10428194.2021.1885664.

120. Buyuktas D., Acar K., Sucak G., et al. COVID-19 infection in patients with acute leukemia; Istanbul experience. Am J Blood Res. 2021; 11: 427–37.

121. Mato A.R., Roeker L.E., Lamanna N., et al. Outcomes of COVID-19 in patients with CLL: a multicenter international experience. Blood. 2020; 136: 1134–43. DOI: 10.1182/blood.2020006965.

122. Scarfo L., Chatzikonstantinou T., Rigolin G.M., et al. COVID-19 severity and mortality in patients with chronic lymphocytic leukemia: a joint study by ERIC, the European Research Initiative on CLL, and CLL Campus. Leukemia. 2020; 34: 2354–63. DOI: 10.1038/s41375-020-0959-x.

123. Chatzikonstantinou T., Kapetanakis A., Scarfo L., et al. COVID-19 severity and mortality in patients with CLL: an update of the international ERIC and Campus CLL study. Leukemia. 2021; 35: 3444–54. DOI: 10.1038/s41375-021-01450-8.

124. Herishanu Y., Perry C. COVID-19 in patients with CLL: how can we change the odds? Blood. 2021; 138: 1652–3. DOI: 10.1182/blood.2021013286.

125. Blixt L., Bogdanovic G., Buggert M., et al. Covid-19 in patients with chronic lymphocytic leukemia: clinical outcome and B- and T-cell immunity during 13 months in consecutive patients. Leukemia. 2022; 36: 476–81. DOI: 10.1038/s41375-021-01424-w.

126. Visco C., Marcheselli L., Mina R., et al. A prognostic model for patients with lymphoma and COVID-19: a multicentre cohort study. Blood Adv. 2022; 6: 327–38. DOI: 10.1182/bloodadvances.2021005691.

127. Mehta V., Goel S., Kabarriti R., et al. Case Fatality Rate of Cancer Patients with COVID-19 in a New York Hospital System. Cancer Discov. 2020; 10: 935–41. DOI: 10.1158/2159-8290.CD-20-0516.

128. Lee L.Y.W., Cazier J-B, Angelis V., et al. COVID-19 mortality in patients with cancer on chemotherapy or other anticancer treatments: a prospective cohort study. Lancet. 2020; 395: 1919–26. DOI: 10.1016/S0140-6736(20)31173-9.

129. Lee L.Y.W., Cazier J-B, Starkey T., et al. COVID-19 prevalence and mortality in patients with cancer and the effect of primary tumour subtype and patient demographics: a prospective cohort study. Lancet Oncol. 2020; 21: 1309–16. DOI: 10.1016/S1470-2045(20)30442-3.

130. Lamure S., Dulery R., Di Blasi R., et al. Determinants of outcome in COVID-19 hospitalized patients with lymphoma: A retrospective multicentric cohort study. EClinicalMedicine. 2020; 27: 100549. DOI: 10.1016/j.eclinm.2020.100549.

131. Wang B., Van Oekelen O., Mouhieddine T.H., et al. A tertiary center experience of multiple myeloma patients with COVID-19: lessons learned and the path forward. J Hematol Oncol. 2020; 13: 94. DOI: 10.1186/s13045-020-00934-x.

132. Mossuto S., Attardi E., Alesiani F., et al. SARS CoV2 in Myelodysplastic Syndromes: A Snapshot From Early Italian Experience. HemaSphere. 2020; 4: e483. DOI: 10.1097/HS9.0000000000000483.

133. Dai M., Liu D., Liu M., et al. Patients with Cancer Appear More Vulnerable to SARS-CoV-2: A Multicenter Study during the COVID-19 Outbreak. Cancer Discov. 2020; 10: 783–91. DOI: 10.1158/2159-8290.CD-20-0422.

134. Wu M., Liu S., Wang C., et al. Risk factors for mortality among lung cancer patients with covid-19 infection: A systematic review and meta-analysis. PLoS ONE. 2023; 18: e0291178. DOI: 10.1371/journal.pone.0291178.

135. Spanjaart A.M., Ljungman P., De La Camara R., et al. Poor outcome of patients with COVID-19 after CAR T-cell therapy for B-cell malignancies: results of a multicenter study on behalf of the European Society for Blood and Marrow Transplantation (EBMT) Infectious Diseases Working Party and the European Hematology Association (EHA) Lymphoma Group. Leukemia. 2021; 35: 3585–8. DOI: 10.1038/s41375-021-01466-0.

136. Busca A., Salmanton-Garcia J., Corradini P., et al. COVID-19 and CAR T cells: a report on current challenges and future directions from the EPICOVIDEHA survey by EHA-IDWP. Blood Adv. 2022; 6: 2427–33. DOI: 10.1182/bloodadvances.2021005616.

137. Pinana J.L., Martino R., Garcia-Garcia I., et al. Risk factors and outcome of COVID-19 in patients with hematological malignancies. Exp Hematol Oncol. 2020; 9: 21. DOI: 10.1186/s40164-020-00177-z.

138. Strasfeld L. COVID-19 and HSCT (Hematopoietic stem cell transplant). Best Pract Res Clin Haematol. 2022; 35: 101399. DOI: 10.1016/j.beha.2022.101399.

139. Zaki A., Soomar S.M., Khan D.H., et al. Outcomes of COVID-19 infection in patients with hematological malignancies- A multicenter analysis from Pakistan. PLoS ONE. 2022; 17: e0267139. DOI: 10.1371/journal.pone.0267139.

140. Lee C.M., Choe P.G., Kang C.K., et al. Impact of T-Cell Engagers on COVID-19–Related Mortality in B-Cell Lymphoma Patients Receiving B-Cell Depleting Therapy. Cancer Res Treat. 2024; 56: 324–33. DOI: 10.4143/crt.2023.738.

141. Levavi H., Lancman G., Gabrilove J. Impact of rituximab on COVID-19 outcomes. Ann Hematol. 2021; 100: 2805–12. DOI: 10.1007/s00277-021-04662-1.