1887

Abstract

Foetal response to hepatitis B viral infection is still unknown. The mechanisms of persistent infection that occurs more often in mother-to-child transmission than adult transmission are also unclear. Various aspects of the environmental factors that accelerate or inhibit infection and the cytokine responses are associated with the persistence of infection. Several studies showed that the cytokine poor immune response in immaturity causes the persistence of the infection. However, some reports suggested that a mature immune response was the cause of this persistent infection. This review comprehensively summarized the reports from , as well as clinical reports regarding the responses of the foetuses of hepatitis B infected mothers to the micro-organism. The mechanism of more opportunities to be persistently infected via the mother-to-child transmission route is also summarized and discussed. Since there are limited clinical reports at this time, this review will provide evidence for future studies regarding the intrauterine infection mechanism and foetal response to hepatitis B virus to elucidate the mechanisms responsible for mother-to-child transmission. This understanding may lead to effective interventions to control mother-to-child hepatitis B infection in the future.

Funding
This study was supported by the:
  • The Thailand Research Fund (Award DPG6280003)
    • Principle Award Recipient: TheeraTongsong
  • Chiang Mai University Research Fund (Award CMU-2564)
    • Principle Award Recipient: TheeraTongsong
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/content/journal/jmm/10.1099/jmm.0.001455
2021-11-15
2021-12-04
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References

  1. WHO Guidelines for the prevention, care and treatment of persons with chronic hepatitis b infection World Health Organization; 2015
    [Google Scholar]
  2. Beasley RP, Hwang LY, Lee GC, Lan CC, Roan CH et al. Prevention of perinatally transmitted hepatitis B virus infections with hepatitis B immune globulin and hepatitis B vaccine. Lancet 1983; 2:1099–1102 [View Article] [PubMed]
    [Google Scholar]
  3. McMahon BJ, Alward WL, Hall DB, Heyward WL, Bender TR et al. Acute hepatitis B virus infection: relation of age to the clinical expression of disease and subsequent development of the carrier state. J Infect Dis 1985; 151:599–603 [View Article] [PubMed]
    [Google Scholar]
  4. Degli Esposti S, Shah D. Hepatitis B in pregnancy: challenges and treatment. Gastroenterol Clin North Am 2011; 40:355–372 [View Article] [PubMed]
    [Google Scholar]
  5. Zhang SL, Yue YF, Bai GQ, Shi L, Jiang H. Mechanism of intrauterine infection of hepatitis B virus. World J Gastroenterol 2004; 10:437–438 [View Article] [PubMed]
    [Google Scholar]
  6. Chen Y, Wang L, Xu Y, Liu X, Li S et al. Role of maternal viremia and placental infection in hepatitis B virus intrauterine transmission. Microbes Infect 2013; 15:409–415 [View Article] [PubMed]
    [Google Scholar]
  7. Lin HH, Lee TY, Chen DS, Sung JL, Ohto H et al. Transplacental leakage of HBeAg-positive maternal blood as the most likely route in causing intrauterine infection with hepatitis B virus. J Pediatr 1987; 111:877–881 [View Article] [PubMed]
    [Google Scholar]
  8. Wong VC, Lee AK, Ip HM. Transmission of hepatitis B antigens from symptom free carrier mothers to the fetus and the infant. Br J Obstet Gynaecol 1980; 87:958–965 [View Article] [PubMed]
    [Google Scholar]
  9. Milich DR, Jones JE, Hughes JL, Price J, Raney AK et al. Is a function of the secreted hepatitis B e antigen to induce immunologic tolerance in utero?. Proc Natl Acad Sci U S A 1990; 87:6599–6603 [View Article] [PubMed]
    [Google Scholar]
  10. Publicover J, Gaggar A, Nishimura S, Van Horn CM, Goodsell A et al. Age-dependent hepatic lymphoid organization directs successful immunity to hepatitis B. J Clin Invest 2013; 123:3728–3739 [View Article] [PubMed]
    [Google Scholar]
  11. Andrade BB, Santos CJN, Camargo LM, Souza-Neto SM, Reis-Filho A et al. Hepatitis B infection is associated with asymptomatic malaria in the Brazilian Amazon. PLoS One 2011; 6:e19841 [View Article] [PubMed]
    [Google Scholar]
  12. Thursz MR, Kwiatkowski D, Torok ME, Allsopp CE, Greenwood BM et al. Association of hepatitis B surface antigen carriage with severe malaria in Gambian children. Nat Med 1995; 1:374–375 [View Article] [PubMed]
    [Google Scholar]
  13. Kennedy PTF, Sandalova E, Jo J, Gill U, Ushiro-Lumb I et al. Preserved T-cell function in children and young adults with immune-tolerant chronic hepatitis B. Gastroenterology 2012; 143:637–645 [View Article] [PubMed]
    [Google Scholar]
  14. Kuipery A, Gehring AJ, Isogawa M. Mechanisms of HBV immune evasion. Antiviral Res 2020; 179:104816 [View Article] [PubMed]
    [Google Scholar]
  15. Maini MK, Gehring AJ. The role of innate immunity in the immunopathology and treatment of HBV infection. J Hepatol 2016; 64:S60–S70 [View Article] [PubMed]
    [Google Scholar]
  16. Hong M, Bertoletti A. Tolerance and immunity to pathogens in early life: insights from HBV infection. Semin Immunopathol 2017; 39:643–652 [View Article] [PubMed]
    [Google Scholar]
  17. Maruyama T, McLachlan A, Iino S, Koike K, Kurokawa K et al. The serology of chronic hepatitis B infection revisited. J Clin Invest 1993; 91:2586–2595 [View Article] [PubMed]
    [Google Scholar]
  18. Bertoletti A, Ferrari C. nate and adaptive immune responses in chronic hepatitis B virus infections: towards restoration of immune control of viral infection. Gut 2012; 61:1754–1764 [View Article] [PubMed]
    [Google Scholar]
  19. Miller D, Motomura K, Garcia-Flores V, Romero R, Gomez-Lopez N. Innate lymphoid cells in the maternal and fetal compartments. Front Immunol 2018; 9:2396 [View Article] [PubMed]
    [Google Scholar]
  20. Chang R-Q, Zhou W-J, Li D-J, Li M-Q. Innate lymphoid cells at the maternal-fetal interface in human pregnancy. Int J Biol Sci 2020; 16:957–969 [View Article] [PubMed]
    [Google Scholar]
  21. Lin H, Mosmann TR, Guilbert L, Tuntipopipat S, Wegmann TG. Synthesis of T helper 2-type cytokines at the maternal-fetal interface. J Immunol 1993; 151:4562–4573 [PubMed]
    [Google Scholar]
  22. King A, Allan DS, Bowen M, Powis SJ, Joseph S et al. HLA-E is expressed on trophoblast and interacts with CD94/NKG2 receptors on decidual NK cells. Eur J Immunol 2000; 30:1623–1631 [View Article] [PubMed]
    [Google Scholar]
  23. Li C, Houser BL, Nicotra ML, Strominger JL. HLA-G homodimer-induced cytokine secretion through HLA-G receptors on human decidual macrophages and natural killer cells. Proc Natl Acad Sci U S A 2009; 106:5767–5772 [View Article] [PubMed]
    [Google Scholar]
  24. van der Meer A, Lukassen HGM, van Lierop MJC, Wijnands F, Mosselman S et al. Membrane-bound HLA-G activates proliferation and interferon-gamma production by uterine natural killer cells. Mol Hum Reprod 2004; 10:189–195 [View Article] [PubMed]
    [Google Scholar]
  25. LeMaoult J, Krawice-Radanne I, Dausset J, Carosella ED. HLA-G1-expressing antigen-presenting cells induce immunosuppressive CD4+ T cells. Proc Natl Acad Sci U S A 2004; 101:7064–7069 [View Article] [PubMed]
    [Google Scholar]
  26. Steinman RM. Decisions about dendritic cells: past, present, and future. Annu Rev Immunol 2012; 30:1–22 [View Article] [PubMed]
    [Google Scholar]
  27. Blois SM, Ilarregui JM, Tometten M, Garcia M, Orsal AS et al. A pivotal role for galectin-1 in fetomaternal tolerance. Nat Med 2007; 13:1450–1457 [View Article] [PubMed]
    [Google Scholar]
  28. Kämmerer U, Eggert AO, Kapp M, McLellan AD, Geijtenbeek TBH et al. Unique appearance of proliferating antigen-presenting cells expressing DC-SIGN (CD209) in the decidua of early human pregnancy. Am J Pathol 2003; 162:887–896 [View Article] [PubMed]
    [Google Scholar]
  29. Mold JE, Michaëlsson J, Burt TD, Muench MO, Beckerman KP et al. Maternal alloantigens promote the development of tolerogenic fetal regulatory T cells in utero. Science 2008; 322:1562–1565 [View Article] [PubMed]
    [Google Scholar]
  30. Marleau AM, Greenwood JD, Wei Q, Singh B, Croy BA. Chimerism of murine fetal bone marrow by maternal cells occurs in late gestation and persists into adulthood. Lab Invest 2003; 83:673–681 [View Article] [PubMed]
    [Google Scholar]
  31. Takahata Y, Nomura A, Takada H, Ohga S, Furuno K et al. CD25+CD4+ T cells in human cord blood: an immunoregulatory subset with naive phenotype and specific expression of forkhead box p3 (Foxp3) gene. Exp Hematol 2004; 32:622–629 [View Article] [PubMed]
    [Google Scholar]
  32. Publicover J, Goodsell A, Nishimura S, Vilarinho S, Wang Z et al. IL-21 is pivotal in determining age-dependent effectiveness of immune responses in a mouse model of human hepatitis B. J Clin Invest 2011; 121:1154–1162 [View Article] [PubMed]
    [Google Scholar]
  33. Sirilert S, Khamrin P, Kumthip K, Malasao R, Maneekarn N et al. Placental infection of hepatitis B virus among Thai pregnant women: Clinical risk factors and its association with fetal infection. Prenat Diagn 2020; 40:380–386 [View Article] [PubMed]
    [Google Scholar]
  34. Li F, Wang X, Men K, Xu D, Yan Y et al. Receptivity of human choriocarcinoma JEGIII cells and isolated trophoblast cells to hepatitis B virus infection and enhancement by tumor necrosis factor alpha. Jpn J Infect Dis 2007; 60:167–172 [PubMed]
    [Google Scholar]
  35. Wang X-P, Li F-J, Xu D-Z, Yan Y-P, Men K et al. Uptake of hepatitis B virus into choriocarcinoma cells in the presence of proinflammatory cytokine tumor necrosis factor-alpha. Am J Obstet Gynecol 2004; 191:1971–1978 [View Article] [PubMed]
    [Google Scholar]
  36. Bhat P, Anderson DA. Hepatitis B virus translocates across a trophoblastic barrier. J Virol 2007; 81:7200–7207 [View Article] [PubMed]
    [Google Scholar]
  37. Kumar M, Sharma Y, Bandi S, Gupta S. Endogenous antiviral microRNAs determine permissiveness for hepatitis B virus replication in cultured human fetal and adult hepatocytes. J Med Virol 2015; 87:1168–1183 [View Article] [PubMed]
    [Google Scholar]
  38. Xun Y-H, Zhang Y-J, Pan Q-C, Mao R-C, Qin Y-L et al. Metformin inhibits hepatitis B virus protein production and replication in human hepatoma cells. J Viral Hepat 2014; 21:597–603 [View Article] [PubMed]
    [Google Scholar]
  39. Tian T, Sun D, Wang P, Wang H, Bai X et al. Roles of Toll-like Receptor 7 and 8 in Prevention of Intrauterine Transmission of Hepatitis B Virus. Cell Physiol Biochem 2015; 37:445–453 [View Article] [PubMed]
    [Google Scholar]
  40. Sato S, Li K, Kameyama T, Hayashi T, Ishida Y et al. The RNA sensor RIG-I dually functions as an innate sensor and direct antiviral factor for hepatitis B virus. Immunity 2015; 42:123–132 [View Article] [PubMed]
    [Google Scholar]
  41. Cai D, Li J, Zeng Y, Li Y, Ren H. A study on the anti-HBV effect of dendritic cell from human umbilical cord blood. Zhonghua Gan Zang Bing Za Zhi 2007; 15:88–91 [PubMed]
    [Google Scholar]
  42. van Montfoort N, van der Aa E, van den Bosch A, Brouwers H, Vanwolleghem T et al. Hepatitis B Virus Surface Antigen Activates Myeloid Dendritic Cells via a Soluble CD14-Dependent Mechanism. J Virol 2016; 90:6187–6199 [View Article] [PubMed]
    [Google Scholar]
  43. Tian Y, Kuo C-F, Akbari O, Ou J-H. Maternal-Derived Hepatitis B Virus e Antigen Alters Macrophage Function in Offspring to Drive Viral Persistence after Vertical Transmission. Immunity 2016; 44:1204–1214 [View Article] [PubMed]
    [Google Scholar]
  44. Wang H-Y, Chien M-H, Huang H-P, Chang H-C, Wu C-C et al. Distinct hepatitis B virus dynamics in the immunotolerant and early immunoclearance phases. J Virol 2010; 84:3454–3463 [View Article] [PubMed]
    [Google Scholar]
  45. Arck PC, Hecher K. Fetomaternal immune cross-talk and its consequences for maternal and offspring’s health. Nat Med 2013; 19:548–556 [View Article] [PubMed]
    [Google Scholar]
  46. Beasley RP, Trepo C, Stevens CE, Szmuness W. The e antigen and vertical transmission of hepatitis B surface antigen. Am J Epidemiol 1977; 105:94–98 [View Article] [PubMed]
    [Google Scholar]
  47. Chen S-C, Toy M, Yeh JM, Wang J-D, Resch S. Cost-effectiveness of augmenting universal hepatitis B vaccination with immunoglobin treatment. Pediatrics 2013; 131:e1135–43 [View Article] [PubMed]
    [Google Scholar]
  48. Isaacs D, Kilham HA, Alexander S, Wood N, Buckmaster A et al. Ethical issues in preventing mother-to-child transmission of hepatitis B by immunisation. Vaccine 2011; 29:6159–6162 [View Article] [PubMed]
    [Google Scholar]
  49. Wiseman E, Fraser MA, Holden S, Glass A, Kidson BL et al. Perinatal transmission of hepatitis B virus: an Australian experience. Med J Aust 2009; 190:489–492 [View Article] [PubMed]
    [Google Scholar]
  50. Zou H, Chen Y, Duan Z, Zhang H, Pan C. Virologic factors associated with failure to passive-active immunoprophylaxis in infants born to HBsAg-positive mothers. J Viral Hepat 2012; 19:e18–25 [View Article] [PubMed]
    [Google Scholar]
  51. Wen W-H, Chang M-H, Zhao L-L, Ni Y-H, Hsu H-Y et al. Mother-to-infant transmission of hepatitis B virus infection: significance of maternal viral load and strategies for intervention. J Hepatol 2013; 59:24–30 [View Article] [PubMed]
    [Google Scholar]
  52. Zhang L, Gui X, Wang B, Ji H, Yisilafu R et al. A study of immunoprophylaxis failure and risk factors of hepatitis B virus mother-to-infant transmission. Eur J Pediatr 2014; 173:1161–1168 [View Article] [PubMed]
    [Google Scholar]
  53. Liu C-P, Zeng Y-L, Zhou M, Chen L-L, Hu R et al. Factors associated with mother-to-child transmission of hepatitis B virus despite immunoprophylaxis. Intern Med 2015; 54:711–716 [View Article] [PubMed]
    [Google Scholar]
  54. Schillie S, Walker T, Veselsky S, Crowley S, Dusek C et al. Outcomes of infants born to women infected with hepatitis B. Pediatrics 2015; 135:e1141–7 [View Article] [PubMed]
    [Google Scholar]
  55. EASL Clinical Practice Guidelines on the management of hepatitis B virus infection. J Hepatol 2017; 67:370–398 [View Article] [PubMed]
    [Google Scholar]
  56. Terrault NA, Lok ASF, McMahon BJ, Chang K-M, Hwang JP et al. Update on prevention, diagnosis, and treatment of chronic hepatitis B: AASLD 2018 hepatitis B guidance. Hepatology 2018; 67:1560–1599 [View Article] [PubMed]
    [Google Scholar]
  57. Sarin SK, Kumar M, Lau GK, Abbas Z, Chan HLY et al. Asian-Pacific clinical practice guidelines on the management of hepatitis B: a 2015 update. Hepatol Int 2016; 10:1–98 [View Article] [PubMed]
    [Google Scholar]
  58. Lee C, Gong Y, Brok J, Boxall EH, Gluud C. Effect of hepatitis B immunisation in newborn infants of mothers positive for hepatitis B surface antigen: systematic review and meta-analysis. BMJ 2006; 332:328–336 [View Article] [PubMed]
    [Google Scholar]
  59. Scheid A, Borriello F, Pietrasanta C, Christou H, Diray-Arce J et al. Adjuvant effect of bacille calmette-guérin on hepatitis B vaccine immunogenicity in the preterm and term newborn. Front Immunol 2018; 9:29 [View Article] [PubMed]
    [Google Scholar]
  60. Dauby N, Alonso-Vega C, Suarez E, Flores A, Hermann E et al. Maternal infection with trypanosoma cruzi and congenital Chagas disease induce a trend to a type 1 polarization of infant immune responses to vaccines. PLoS Negl Trop Dis 2009; 3:e571 [View Article] [PubMed]
    [Google Scholar]
  61. Malhotra I, LaBeaud AD, Morris N, McKibben M, Mungai P et al. Cord blood antiparasite interleukin 10 as a risk marker for compromised vaccine immunogenicity in early childhood. J Infect Dis 2018; 217:1426–1434 [View Article] [PubMed]
    [Google Scholar]
  62. Zhu Q, Ge Y, Gu S, Yu H, Wang J et al. Relationship between cytokines gene polymorphism and susceptibility to hepatitis B virus intrauterine infection. Chin Med J 2005; 118:1604–1609 [PubMed]
    [Google Scholar]
  63. de Lima A, Kanis SL, Escher JC, van der Woude CJ. Hepatitis B vaccination effective in children exposed to anti-tumour necrosis factor alpha in utero. J Crohns Colitis 2018; 12:948–953 [View Article] [PubMed]
    [Google Scholar]
  64. Bertoletti A, Hong M. Age-dependent immune events during HBV infection from birth to adulthood: an alternative interpretation. Front Immunol 2014; 5:441 [View Article] [PubMed]
    [Google Scholar]
  65. Shen L, Zhang X, Hu D, Feng T, Li H et al. Hepatitis B virus X (HBx) play an anti-apoptosis role in hepatic progenitor cells by activating Wnt/β-catenin pathway. Mol Cell Biochem 2013; 383:213–222 [View Article] [PubMed]
    [Google Scholar]
  66. Hösel M, Quasdorff M, Ringelhan M, Kashkar H, Debey-Pascher S et al. Hepatitis B virus activates signal transducer and activator of transcription 3 supporting hepatocyte survival and virus replication. Cell Mol Gastroenterol Hepatol 2017; 4:339–363 [View Article] [PubMed]
    [Google Scholar]
  67. Wang F, Sha L, Ye L, Zhang X. Promotion of cell proliferation by HBXIP via upregulation of human telomerase reverse transcriptase in human mesenchymal stem cells. Acta Pharmacol Sin 2008; 29:83–89 [View Article] [PubMed]
    [Google Scholar]
  68. Cui H, Li Q-L, Chen J, Na Q, Liu C-X. Hepatitis B virus X protein modifies invasion, proliferation and the inflammatory response in an HTR-8/SVneo cell model. Oncol Rep 2015; 34:2090–2098 [View Article] [PubMed]
    [Google Scholar]
  69. Bai G, Wang Y, Zhang L, Tang Y, Fu F. The study on the role of hepatitis B virus X protein and apoptosis in HBV intrauterine infection. Arch Gynecol Obstet 2012; 285:943–949 [View Article] [PubMed]
    [Google Scholar]
  70. EASL EASL clinical practice guidelines: Management of chronic hepatitis B virus infection. J Hepatol 2012; 57:167–185 [View Article] [PubMed]
    [Google Scholar]
  71. Raffetti E, Fattovich G, Donato F. Incidence of hepatocellular carcinoma in untreated subjects with chronic hepatitis B: a systematic review and meta-analysis. Liver Int 2016; 36:1239–1251 [View Article] [PubMed]
    [Google Scholar]
  72. Hong M, Sandalova E, Low D, Gehring AJ, Fieni S et al. Trained immunity in newborn infants of HBV-infected mothers. Nat Commun 2015; 6:6588 [View Article] [PubMed]
    [Google Scholar]
  73. Cruz LAB, Moraes MOA, Queiroga-Barros MR, Fukutani KF, Barral-Netto M et al. Chronic hepatitis B virus infection drives changes in systemic immune activation profile in patients coinfected with Plasmodium vivax malaria. PLoS Negl Trop Dis 2019; 13:e0007535 [View Article] [PubMed]
    [Google Scholar]
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