Chronic Hepatitis С and Oncohematological Diseases

AUTOIMMUNE THROMBOCYTOPENIA

TV Antonova1, MS Nozhkin1, DA Lioznov1,2

1 IP Pavlov First Saint Petersburg State Medical University, 6/8 L’va Tolstogo ul., Saint Petersburg, Russian Federation, 197022

2 AA Smorodintsev Research Institute of Influenza, 15/17 Professora Popova ul., Saint Petersburg, Russian Federation, 197376

For correspondence: Prof. Tamara Vasilevna Antonova, MD, PhD, 6/8 L’va Tolstogo ul., Saint Petersburg, Russian Federation, 197022; e-mail: antonovatv28@yandex.ru

For citation: Antonova TV, Nozhkin MS, Lioznov DA. Chronic Hepatitis С and Oncohematological Diseases. Clinical oncohematology. 2023;16(1):46–53. (In Russ).

DOI: 10.21320/2500-2139-2023-16-1-46-53

ABSTRACT

This review focuses on HCV infection in oncohematological patients. High risk of hepatitis C virus (HCV) infection within this group of patients was proved by a significantly (2.0–2.5 times) higher HCV infection rate in non-Hodgkin’s lymphoma patients compared to population data. Besides, the review demonstrates the importance of HCV in the development and progression of B-cell non-Hodgkin’s lymphomas, which is confirmed by its tumorigenicity. The paper reviews the variant of seronegative (occult) hepatitis С, which is characterized by HCV RNA detected in liver tissue and peripheral blood mononuclear cells by highly sensitive reverse transcription PCR with the absence of serum HCV and HCV RNA antibodies. In this case, patients can present a source of infection. Seronegative hepatitis С is detected in donor blood in 2.2–3.4 % of cases. This infection variant is identified in 20–85 % of oncohematological patients, which needs to be further examined. Comorbid HCV infection is a potential prognostic factor in oncohematological diseases. Oncohematological patients with comorbid chronic hepatitis C (CHC) show considerably worse survival as compared with patients without it. HCV infection is associated with increased complication rates in both chemotherapy and hematopoietic stem cell transplantation (HSCT). Immunochemotherapy, on the other hand, affects CHC exacerbation and progression. High efficacy and good tolerability of direct-acting antiviral agents (DAA) in CHC therapy opened new prospects for their wide use in cases of comorbid diseases. HCV treatment in patients after HSCT still remains an issue. The guidelines for CHC treatment are predominantly formulated with a view to antiviral pre-HSCT therapy which is not always feasible in real-world clinical practice. The review contains examples of effective use of DAA drugs before or after HSCT and a case of antiviral treatment administered simultaneously with HSCT.

Keywords: hepatitis C virus, HCV infection, oncohematology, hematopoietic stem cell transplantation, immunochemotherapy, direct-acting antiviral agents.

Received: June 17, 2022

Accepted: December 10, 2022

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Статистика Plumx английский

REFERENCES

  1. Choo QL, Kuo G, Weiner AJ, et al. Isolation of a cDNA clone derived from a blood-borne non-A, non-B viral hepatitis genome. Science. 1989;244(4902):359–62. doi: 10.1126/science.2523562.
  2. Houghton M. Discovery of the hepatitis C virus. Liver Int. 2009;29(Suppl 1):82–8. doi: 10.1111/j.1478-3231.2008.01925.x.
  3. Жебрун А.Б., Калинина О.В. Вирусный гепатит С: эволюция эпидемиологического процесса, эволюция вируса. Журнал микробиологии, эпидемиологии и иммунобиологии. 2016;1:102–12. doi: 10.36233/0372-9311-2016-1-102-112.
    [Zhebrun AB, Kalinina OV. Viral hepatitis C: evolution of the epidemiologic process, evolution of the virus. Zhurnal Mikrobiologii, Epidemiologii, i Immunobiologii. 2016;1:102–12. doi: 10.36233/0372-9311-2016-1-102-112. (In Russ)]
  4. Simmonds P, Bukh J, Combet C, et al. Consensus proposals for a unified system of nomenclature of hepatitis C virus genotypes. 2005;42(4):962–73. doi: 10.1002/hep.20819.
  5. Smith DB, Bukh J, Kuiken C, et al. Expanded classification of hepatitis C virus into 7 genotypes and 67 subtypes: updated criteria and genotype assignment web resource. 2014;59(1):318–27. doi: 10.1002/hep.26744.
  6. Petruzziello A, Marigliano S, Loquercio G, et al. Global epidemiology of hepatitis C virus infection: updated information on the distribution and circulation of hepatitis C virus genotypes. World J Gastroenterol. 2016;22(34):7824–40. doi: 10.3748/wjg.v22.i34.7824.
  7. Чуланов В.П., Исаков В.А., Жданов К.В. и др. Промежуточные результаты международного многоцентрового проспективного наблюдательного исследования «MOSAIC» по оценке эпидемиологии, субъективных и экономических исходов лечения хронического вирусного гепатита С. Инфекционные болезни. 2018;16(1):5–14. doi: 20953/1729-9225-2018-1-5-14.
    [Chulanov VP, Isakov VA, Zhdanov KV, et al. Interim results of the international multicenter prospective observational study to evaluate the epidemiology, humanistic and economic outcomes of treatment for chronic hepatitis C virus (HCV) (MOSAIC). Infektsionnye bolezni. 2018;16(1):5–14. doi: 10.20953/1729-9225-2018-1-5-14. (In Russ)]
  8. Чуланов В.П., Пименов Н.Н., Мамонова Н.А. и др. Хронический гепатит С как проблема здравоохранения России сегодня и завтра. Терапевтический архив. 2015;87(11):5–10. doi: 10.17116/terarkh201587115-10.
    [Chulanov VP, Pimenov NN, Mamonova NA, et al. Chronic hepatitis C In Russia: current challenges and prospects. Terapevticheskii arkhiv. 2015;87(11):5–10. doi: 10.17116/terarkh201587115-10. (In Russ)]
  9. Федеральная служба по надзору в сфере защиты прав потребителей и благополучия человека. О состоянии санитарно-эпидемиологического благополучия населения в Российской Федерации в 2019 г.: Государственный доклад. М.: 2020. 299 с.
    [Federal Service for Surveillance on Consumer Rights Protection and Human Wellbeing. On the state of sanitary and epidemiological well-being of the population in the Russian Federation in 2019: State report. Moscow; 2020. 299 p. (In Russ)]
  10. Дземова А.А., Ганченко Р.А., Трифонова Г.Ф. и др. Хронический гепатит С в Российской Федерации после начала программы элиминации HCV-инфекции. Гепатология и гастроэнтерология. 2020;4(2):165–70. doi: 25298/2616-5546-2020-4-2-165-170.
    [Dzemova AA, Ganchenko RA, Trifonova GF, et al. Chronic hepatitis C in the Russian Federation after starting the HCV elimination program. Gepatologiya i gastroenterologiya. 2020;4(2):165–70. doi: 10.25298/2616-5546-2020-4-2-165-170. (In Russ)]
  11. Злокачественные новообразования в России в 2020 году (заболеваемость и смертность). Под ред. А.Д. Каприна, В.В. Старинского, А.О. Шахзадовой. М.: МНИОИ им. П.А. Герцена — филиал ФГБУ «НМИЦ радиологии» Минздрава России, 252 с.
    [Kaprin AD, Starinskii VV, Shakhzadova AO, eds. Zlokachestvennye novoobrazovaniya v Rossii v 2020 godu (zabolevaemost’ i smertnost’). (Malignant neoplasms In Russia in 2019 (incidence and mortality.) Moscow: MNIOI im. P.A. Gertsena — filial FGBU “NMITs radiologii” Publ.; 2021. 252 p. (In Russ)]
  12. Kawamura Y, Ikeda K, Arase Y, et al. Viral elimination reduces incidence of malignant lymphoma in patients with hepatitis. J Am Med Assoc. 2007;120(12):1034–41. doi: 10.1016/j.amjmed.2007.06.022.
  13. Su TH, Liu CJ, Tseng TC, et al. Hepatitis C viral infection increases the risk of lymphoid-neoplasms: A population-based cohort study. Hepatology. 2016;63(3):721–30. doi: 10.1002/hep.28387.
  14. Pozzato G, Mazzaro C, Maso L, et al. Hepatitis C virus and non-Hodgkin’s lymphomas: meta-analysis of epidemiology data and therapy options. World J Hepatol. 2016;8(2):107–16. doi: 10.4254/wjh.v8.i2.107.
  15. Милованова С.Ю., Лысенко Л.В., Милованова Л.Ю. и др. HCV-ассоциированная смешанная криоглобулинемия и В-клеточная неходжкинская лимфома — патогенетически связанные проблемы. Терапевтический архив. 2018;90(6):112–20. doi: 10.26442/terarkh2018906112-120.
    [Milovanova SYu, Lysenko LV, Milovanova LYu, et al. HCV-associated mixed cryoglobulinemia and B-cell non-Hodgkin’s lymphoma are pathogenetically related problems. Terapevticheskii arkhiv. 2018;90(6):112–20. doi: 10.26442/terarkh2018906112-120. (In Russ)]
  16. Minafo YA, Del Padre M, Cristofoletti C, et al. A stereotyped light chain may shape virus-specific B-cell receptors in HCV-dependent lymphoproliferative disorders. Genes Immun. 2020;21(2):131–5. doi: 10.1038/s41435-020-0093-9.
  17. Lotfi AA, Mohamed AE, Shalaby NA, et al. Occult hepatitis C virus infection in patients with malignant lymphoproliferative disorders. Int J Immunopathol Pharmacol. 2020;34:2058738420961202. doi: 10.1177/2058738420961202.
  18. Hirose S, Yamaji Y, Tsuruya K, et al. Rapid regression of B-cell non-Hodgkin’s lymphoma after eradication of hepatitis C virus by direct antiviral agents. Case Rep Gastroenterol. 2019;13(2):336–41. doi: 10.1159/000501546.
  19. Defrancesco I, Zerbi C, Rattotti S, et al. HCV infection and non-Hodgkin lymphomas: an evolving story. Clin Exp Med. 2020;20(3):321–8. doi: 10.1007/s10238-020-00615-6.
  20. Pozzato G, Mazzaro C, Gattei V. Hepatitis C virus-associated non-Hodgkin lymphomas: the endless history. Minerva Medica. 2021;112(2):215–27. doi: 10.23736/S0026-4806.20.07184-0.
  21. Сaсoub P, Comarmond C, Vieira M, et al. HCV-related lymphoproliferative disorders in the direct-acting antiviral era: From mixed cryoglobulinaemia to B-cell lymphoma. J Hepatol. 2021;76(1):174–85. doi: 10.1016/j.jhep.2021.09.023.
  22. Zhang M, Gao F, Peng L, et al. Distinct clinical features and prognostic factors in Hepatitis C virus-associated Non-Hodgkin’s lymphoma: a systematic review and meta-analysis. Cancer Cell Int. 2021;21(1):524. doi: 10.1186/s12935-021-02230-1.
  23. Ножкин М.С. Клинико-лабораторная характеристика течения хронического гепатита С у онкогематологических больных: Автореф. дис.… канд. мед. наук. СПб., 2021. 17 с.
    [Nozhkin MS. Kliniko-laboratornaya kharakteristika techeniya khronicheskogo gepatita C u onkogematologicheskikh bolnykh. (Clinical and laboratory characteristics of the course of chronic hepatitis C in oncohematological ) [dissertation] Saint Petersburg; 2021. 17 р. (In Russ)]
  24. Arico M, Maggiore G, Silini E, et al. Hepatitis C virus infection in children treated for acute lymphoblastic leukemia. Blood. 1994;84(9):2919–22.
  25. Meir H, Balawi I, Nayel H, et al. Hepatitis dysfunction in children with acute lymphoblastic leukemia remission: relation to hepatitis infection. Med Pediatr Oncol. 2001;36(4):469–73. doi: 10.1002/mpo.1111.
  26. Шардаков В.И., Назарова Е.Л., Сухорукова Э.Е. и др. Характеристика иммунного ответа у онкогематологических больных, имеющих хронический гепатит С. Вятский медицинский вестник. 2020;65(1):62–7.
    [Shardakov VI, Nazarova EL, Sukhorukova EE, et al. Characterization of the immune response in oncohematological patients with chronic hepatitis C. Vyatskii meditsinskii vestnik. 2020;65(1):62–7. (In Russ)]
  27. Torres HA, Davila M. Reactivation of hepatitis B virus and hepatitis C virus in patients with cancer. Nat Rev Clin Oncol. 2012;9(3):156–66. doi: 10.1038/nrclinonc.2012.1.
  28. Шаницына С.Е., Бурневич Э.З., Никулкина Е.Н. и др. Факторы риска неблагоприятного прогноза хронического гепатита С. Терапевтический архив. 2019;91(2):59–66. doi: 10.26442/00403660.2019.02.000082.
    [Shchanitcyna SE, Burnevich EZ, Nikulkina EN, et al. Risk factors of unfavorable prognosis of chronic hepatitis C. Terapevticheskii arkhiv. 2019;91(2):59–66. doi: 10.26442/00403660.2019.02.000082. (In Russ)]
  29. Mahale P, Kontoyiannis DP, Chemaly RF, et al. Acute exacerbation and reactivation of chronic hepatitis C virus infection in cancer patients. J Hepatol. 2021;57(6):1177–85. doi: 10.1016/j.jhep.2012.07.031.
  30. Nosotti L, D’Andrea M, Pitidis A, et al. Hepatitis C virus infection prevalence and liver dysfunction in a cohort of B-cell non-Hodgkin’s lymphoma patients treated with immunochemotherapy. Scand J Infect Dis. 2012;44(1):70–3. doi: 10.3109/00365548.2011.611819.
  31. Новик А.А. Возможности трансплантации костного мозга и стволовых кроветворных клеток в терапии гематологических и онкологических заболеваний. Вестник Национального медико-хирургического центра им. Н.И. Пирогова. 2006;1(1):58–63.
    [Novik AA. Possibilities for bone marrow and hematopoietic stem cell transplantation in the treatment of hematological and oncological diseases. Vestnik Natsionalnogo mediko-khirurgicheskogo tsentra im. N.I. Pirogova. 2006;1(1):58–63. (In Russ)]
  32. Mahmoud HK, Fathy GM, Elhaddad A, et al. Hematopoietic Stem Cell Transplantation in Egypt: Challenges and Opportunities. Mediterr J Hematol Infect Dis. 2020;12(1):e2020023. doi: 10.4084/MJHID.2020.023.
  33. Levitsky D, Sorrell MF. Hepatic complications of hematopoietic cell transplantation. Curr Gastroenterol Rep. 2007;9(1):60–5. doi: 10.1007/s11894-008-0022-y.
  34. Abdelbary H, Magdy R, Moussa M, et al. Liver disease during and after hematopoietic stem cell transplantation in adults: a single-center Egyptian experience. J Egypt Natl Canc Inst. 2020;32(1):11. doi: 10.1186/s43046-020-0020-1.
  35. Kaito S, Doki N, Hishima T, et al. Progressive hepatic cirrhosis early after allogeneic hematopoietic stem cell transplantation in a patient with chronic hepatitis C infection. Turk J Hematol. 2019;36(2):130–3. doi: 10.4274/tjh.galenos.2019.2018.0224.
  36. Castillo I, Rodriguez-Inigo E, Bartolome J, et al. Hepatitis C virus replicates in peripheral blood mononuclear cells of patients with occult hepatitis C virus infection. 2005;54(5):682–5. doi: 10.1136/gut.2004.057281.
  37. Castillo I, Bartolome J, Quiroga JA, et al. Long-term virological follow up of patients with occult hepatitis C virus infection. Liver Int. 2011;31(10):1519–24. doi: 10.1111/j.1478-3231.2011.02613.x.
  38. Вишневская Т.В., Масалова О.В., Альховский С.В. и др. Выявление маркеров репликации вируса гепатита С в мононуклеарных клетках периферической крови больных хроническим гепатитом С. Медицинская иммунология. 2008;10(4–5):397–404. doi: 10.15789/1563-0625-2008-4-5-397-404.
    [Vishnevskaya TV, Massalova OV, Alkhovsky SV, et al. Detection of hepatitis C virus-specific replication markers in peripheral blood mononuclears from the patients with chronic hepatitis C. Medical immunology. 2008;10(4–5):397–404. doi: 10.15789/1563-0625-2008-4-5-397-404. (In Russ)]
  39. Quiroga JA, Castillo I, Llorente S, et al. Identification of serologically silent latent hepatitis C viral infection by detecting an immunoglobulin G antibody to the dominant epitope of the HCV core peptide. J Hepatol. 2009;50(2):256–63. doi: 10.1016/j.jhep.2008.08.021.
  40. Carreno V, Bartolome J, Castillo I, et al. New perspectives in occult hepatitis C virus infection. World J Gastroenterol. 2012;18(23):2887–94. doi: 10.3748/wjg.v18.i23.2887.
  41. De Marco L, Gillio-Tos A, Fiano V, et al. Occult HCV infection: an unexpected finding in a population unselected for hepatic disease. PLoS One. 2009;4(12):e8128. doi: 10.1371/journal.pone.0008128.
  42. Lin H, Chen X, Zhu S, et al. Prevalence of Occult Hepatitis C Virus Infection among Blood Donors in Jiangsu, China. Intervirology. 2016;59(4):204–10. doi: 10.1159/000455854.
  43. Martinez-Rodriguez ML, Uribe-Noguez LA, Arroyo-Anduiza CI, et al. Prevalence and risk factors of Occult Hepatitis C infections in blood donors from Mexico City. PLoS One. 2018;13(10):e0205659. doi: 10.1371/journal.pone.0205659.
  44. Austria A, Wu GY. Occult Hepatitis C Virus Infection: A Review. J Clin Transl Hepatol. 2018;6(2):155–60. doi: 10.14218/JCTH.2017.00053.
  45. Helaly GF, Elsheredy AG, El Basset Mousa AA, et al. Seronegative and occult hepatitis C virus infections in patients with hematological disorders. Arch Virol. 2017;162(1):63–6. doi: 10.1007/s00705-016-3049-7.
  46. Mahrous S, Baraka A, Fathy М, Fayez М. Seronegative and latent hepatitis C viral infections in patients with acute and chronic myeloid leukemia. Egypt J Hosp Med. 2022;86(1):470–6. doi: 10.21608/ejhm.2022.213795.
  47. Yousif MM, Elsadek Fakhr A, Morad EA, et al. Prevalence of occult hepatitis C virus infection in patients who achieved sustained virologic response to direct-acting antiviral agents. Infez Med. 2018;26(3):237–43.
  48. Mazzaro C, Quartuccio L, Adinolfi LE. Review of extrahepatic manifestations of chronic hepatitis C viral infection and the effects of direct-acting antiviral therapy. Viruses. 2021;13(11):2249. doi: 10.3390/v13112249.
  49. Sarakko DM, Marzano A, Rizzetto M. Therapy of chronic viral hepatitis: light at the end of the tunnel? 2022;10(3):534. doi: 10.3390/biomedicines10030534.
  50. Нурмухаметова Е.А., Блохина Н.П., Тихонова Н.Ю. Противовирусная терапия хронического гепатита С: многолетний опыт реальной клинической практики. Инфекционные болезни. 2021;19(3):43–57. doi: 10.20953/1729-9225-2021-3-43-57.
    [Nurmukhametova EA, Blokhina NP, Tikhonova NYu. Antiviral therapy for chronic hepatitis C: many years of real clinical experience. Infektsionnye bolezni. 2021;19(3):43–57. doi: 10.20953/1729-9225-2021-3-43-57. (In Russ)]
  51. Rabaan AA, Al-Ahmed SH, Bazzi AM, et al. Overview of hepatitis C infection, molecular biology and new treatment. J Infect Public Health. 2020;13(5):773–83. doi: 10.1016/j.jiph.2019.11.015.
  52. Fontana RJ, Brown RS, Moreno-Zamora A, et al. Daclatasvir in combination with sofosbuvir or simeprevir in liver transplant recipients with severe recurrent hepatitis C infection. Liver Transpl. 2016;22(4):446–58. doi: 10.1002/lt.24416.
  53. Michot JM, Canioni D, Driss H, et al. Antiviral therapy is associated with a better survival in patients with hepatitis C virus and B-cell non-Hodgkin lymphomas, ANRS HC-13 lympho-C study. Am J Hematol. 2015;90(3):197–203. doi: 10.1002/ajh.23889.
  54. Frigeni M, Besson C, Visco C, et al. Interferon-free compared to interferon-based antiviral regimens as first-line therapy B-cell lymphoproliferative disorders associated with hepatitis C virus infection. Leukemia. 2020;34(5):1462–6. doi: 10.1038/s41375-019-0687-2.
  55. Pinana JL, Serra MА, Hernandez-Boluda JC, et al. Successful treatment of hepatitis C virus infection with sofosbuvir and simeprevir in the early phase of an allogeneic stem cell transplant. Transpl Infect Dis. 2016;18(1):89–92. doi: 10.1111/tid.12474.
  56. Rauwolf K, Herbruggen H, Zollner S, et al. Durable control of hepatitis C through interferon-free antiviral combination therapy immediately prior to allogeneic haematopoietic stem cell transplantation. J Viral. 2019;26(4):454–8. doi: 10.1111/jvh.13046.
  57. Onodera K, Onishi Y, Inoue J, et al. Second direct-acting antiviral therapy for hepatitis C virus infection after umbilical cord blood transplantation: A case report. J Infect Chemother. 2021;27(8):1230–3. doi: 10.1016/j.jiac.2021.02.002.
  58. Iftikhar R, Ahmad P, de Latour R, et al. Special issues related to the diagnosis and management of acquired aplastic anemia in countries with restricted resources, a report on behalf of the Eastern Mediterranean blood and marrow transplantation (EMBMT) group and severe aplastic anemia working party of the European Society for blood and marrow transplantation (SAAWP of EBMT). Bone Marrow Transplant. 2021;56(10):2518–32. doi: 10.1038/s41409-021-01332-8.
  59. Cunningham HE, Shea TC, Grgic T, Lachiewicz AM. Successful treatment of hepatitis C virus infection with direct-acting antivirals during hematopoietic cell transplant. Transpl Infect Dis. 2019;21(3):е13091. doi: 10.1111/tid.13091.
  60. Кичатова В.С., Кюрегян К.К. Современный взгляд на резистентность к препаратам прямого противовирусного действия при лечении вирусного гепатита С. Инфекционные болезни: новости, мнения, обучение. 2019;8(2):64–71. doi: 10.24411/2305-3496-2019-12009.
    [Kichatova VS, Kuregyan KK. Modern view on resistance to direct antiviral drugs in the treatment of viral hepatitis C: analytical review. Infektsionnye bolezni: novosti, mneniya, obuchenie. 2019;8(2):64–71. doi: 10.24411/2305-3496-2019-12009. (In Russ)]
  61. Глобальная стратегия сектора здравоохранения по вирусному гепатиту 2016–2021 гг. На пути к ликвидации вирусного гепатита. Женева: ВОЗ, 2016. 52 с.
    [Global health sector strategy on viral hepatitis 2016–2021. Towards ending viral hepatitis. Geneva: WHO Publ.; 52 p. (In Russ)]
  62. Михайлов М.И., Ющук Н.Д., Малинникова Е.Ю. и др. Проект программы по контролю и ликвидации вирусных гепатитов как проблемы общественного здоровья в Российской Федерации. Инфекционные болезни: новости, мнения, обучение. 2018;7(2):52–8. doi:24411/2305-3496-2018-12005.
    [Mikhaylov MI, Yushchuk ND, Malinnikova EYu, et al. The design of the program for control and elimination of viral hepatitis as public health problem in the Russian Federation. Infektsionnye bolezni: novosti, mneniya, obuchenie. 2018;7(2):52–8. doi: 10.24411/2305-3496-2018-12005. (In Russ)]