Pathogenesis of hepatitis C during pregnancy and childhood

Viruses

Volumn 4, Issue 12, 2012, Pages 3531-3550

  Le Campion, Armelle ^a   Larouche, Ariane ^a,b   Fauteux Daniel, Sébastien ^a,b   Soudeyns, Hugo ^a,b  

^a UNIVERSITY OF MONTREAL   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Hepatitis C virus; Mother to child transmission; Pathogenesis; Pediatrics

Indexed keywords

CHILD; CHILDHOOD; DISEASE COURSE; HEPATITIS C; HUMAN; IMMUNOMODULATION; INFECTION PREVENTION; NEWBORN PERIOD; PATHOGENESIS; PERINATAL PERIOD; PREGNANCY; REVIEW; VERTICAL TRANSMISSION; VIRUS TRANSMISSION;

ADOLESCENT; ADULT; CHILD; CHILD, PRESCHOOL; COINFECTION; FEMALE; HEPACIVIRUS; HEPATITIS C; HIV INFECTIONS; HUMANS; INFANT; INFANT, NEWBORN; INFECTIOUS DISEASE TRANSMISSION, VERTICAL; PREGNANCY; PREGNANCY COMPLICATIONS, INFECTIOUS; RISK FACTORS; VIRAL LOAD; YOUNG ADULT;

HEPATITIS C VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84871852930     PISSN: 19994915     EISSN: None     Source Type: Journal    
DOI: 10.3390/v4123531     Document Type: Review

References (140)

1. Lavanchy, D. The global burden of hepatitis C. Liver Int. 2009, 29 (Suppl 1), 74-81.
2. Alter, M.J. Hepatitis C virus infection in the United States. J. Hepatol. 1999, 31 (Suppl 1), 88-91.
3. Arshad, M.; El-Kamary, S.S.; Jhaveri, R. Hepatitis C virus infection during pregnancy and the newborn period--are they opportunities for treatment? J. Viral. Hepat. 2011, 18, 229-236.
4. Zahran, K.M.; Badary, M.S.; Agban, M.N.; Abdel Aziz, N.H. Pattern of hepatitis virus infection among pregnant women and their newborns at the Women's Health Center of Assiut University, Upper Egypt. Int. J. Gynaecol. Obstet. 2010, 111, 171-174.
5. Alter, M. J. Epidemiology of hepatitis C. Hepatology 1997, 26, 62S-65S.
6. Thomas, D.L.; Zenilman, J.M.; Shih, J.W.; Galai, N.; Carella, A.V.; Quinn, T.C. Sexual transmission of hepatitis C virus among patients attending sexually transmitted diseases clinics in Baltimore-an analysis of 309 sex partnerships. J. Infect. Dis. 1995, 171, 768-775.
7. Klevens, R.M.; Hu, D.J.; Jiles, R.; Holmberg, S.D. Evolving epidemiology of hepatitis C virus in the United States. Clin. Infect. Dis. 2012, 55 Suppl 1, S3-S9.
8. Conte, D.; Fraquelli, M.; Prati, D.; Colucci, A.; Minola, E. Prevalence and clinical course of chronic hepatitis C virus (HCV) infection and rate of HCV vertical transmission in a cohort of 15,250 pregnant women. Hepatology 2000, 31, 751-755.
9. Wesjtal, R.; Widell, A.; Mansson, A.S.; Hermodsson, S.; Nokrans, G. Mother-to-infant transmission of hepatitis C virus. Ann. Intern. Med. 1992, 117, 887-890.
10. Ohto, H.; Terazawa, S.; Sasaki, N.; Hino, K.; Ishiwata, C.; Kako, M.; Ujiie, N.; Endo, C.; Matsui, A.; Okamoto, H.; Mishiro, S.; Vertical Transmission of Hepatitis C Virus Collaborative Study Group. Transmission of hepatitis C virus from mothers to infants. N. Engl. J. Med. 1994, 330, 744-750.
11. Novati, R.; Thiers, V.; Monforte, A.D.; Maisonneuve, P.; Principi, N.; Conti, M.; Lazzarin, A.; Brechot, C. Mother-to-child transmission of hepatitis C virus detected by nested polymerase chain reaction. J. Infect. Dis. 1992, 165, 720-723.
12. Zanetti, A.R.; Tanzi, E.; Paccagnini, S.; Principi, N.; Pizzocolo, G.; Caccamo, M.L.; D'Amico, E.; Cambie, G.; Vecchi, L.; Lombardy Study Group on Vertical HCV Transmission. Mother-toinfant transmission of hepatitis C. Lombardy study group on vertical HCV transmission. Lancet 1995, 345, 289-291.
13. Agha, S.; Sherif, L.S.; Allam, M.A.; Fawzy, M. Transplacental transmission of hepatitis C virus in HIV-negative mothers. Res. Virol. 1998, 149, 229-234.
14. Matsubara, T.; Sumazaki, R.; Takita, H. Mother-to-infant transmission of hepatitis C virus: a prospective study. Eur. J. Pediatr. 1995, 154, 973-978.
15. Lin, H.H.; Kao, J.H.; Hsu, H.Y.; Ni, Y.H.; Yeh, S.H.; Hwang, L.H.; Chang, M.H.; Hwang, S.C.; Chen, P.J.; Chen, D.S. Possible role of high-titer maternal viremia in perinatal transmission of hepatitis C virus. J. Infect. Dis. 1993, 169, 638-641.
16. Thomas, S.L.; Newell, M.L.; Peckham, C.S.; Ades, A.E.; Hall, A.J. A review of hepatitis C virus (HCV) vertical transmission: risks of transmission to infants born to mothers with and without HCV viraemia or human immunodeficiency virus infection. Int. J. Epidemiol. 1998, 27, 108-117.
17. Akhtar, S.; Moatter, T. Intra-household clustering of hepatitis C virus infection in Karachi, Pakistan. Trans. R. Soc. Trop. Med. Hyg. 2004, 98, 535-539.
18. Miller, F.D.; Abu-Raddad, L.J. Evidence of intense ongoing endemic transmission of hepatitis C virus in Egypt. Proc. Natl Acad. Sci. USA. 2010, 107, 14757-14762.
19. Schwimmer, J.B.; Balistreri, W.F. Transmission, natural history, and treatment of hepatitis C virus infection in the pediatric population. Semin. Liver Dis. 2000, 20, 37-46.
20. Jafri, W.; Jafri, N.; Yakoob, J.; Islam, M.; Tirmizi, S.F.; Jafar, T.; Akhtar, S.; Hamid, S.; Shah, H.A.; Nizami, S.Q. Hepatitis B and C: prevalence and risk factors associated with seropositivity among children in Karachi, Pakistan. BMC Infect. Dis. 2006, 6, 101.
21. Mor, G.; Cardenas, I. The immune system in pregnancy: a unique complexity. Am. J. Reprod. Immunol. 2010, 63, 425-433.
22. Pergam, S.A.; Wang, C.C.; Gardella, C.M.; Sandison, T.G.; Phipps, W.T.; Hawes, S.E. Pregnancy complications associated with hepatitis C: Data from a 2003-2005 Washington state birth cohort. Am. J. Obstet. Gynecol. 2008, 199, 38. e1-38. e9.
23. Buresi, M.C.; Lee, J.; Gill, S.; Kong, J.M.; Money, D.M.; Yoshida, E.M. Hepatitis C vertical Transmission Study Group. The prevalence of gestational diabetes mellitus and glucose abnormalities in pregnant women with hepatitis C virus infection in British Columbia. J. Obstet. Gynaecol. Can. 2010, 32, 935-941.
24. Reddick, K.L.; Jhaveri, R.; Gandhi, M.; James, A.H.; Swamy, G.K. Pregnancy outcomes associated with viral hepatitis. J. Viral. Hepat. 2011, 18, e394-e398.
25. Locatelli, A.; Roncaglia, N.; Arreghini, A.; Bellini, P.; Vergani, P.; Ghidini, A. Hepatitis C virus infection is associated with a higher incidence of cholestasis of pregnancy. BJOG. 1999, 106, 498-500.
26. Paternoster, D.M.; Fabris, F.; Palu, G.; Santarossa, C.; Bracciante, R.; Snijders, D.; Floreani, A. Intra-hepatic cholestasis of pregnancy in hepatitis C virus infection. Acta Obstet. Gynecol. Scand. 2002, 81, 99-103.
27. Safir, A.; Levy, A.; Sikuler, E.; Sheiner, E. Maternal hepatitis B virus or hepatitis C virus carrier status as an independent risk factor for adverse perinatal outcome. Liver Int. 2010, 30, 765-770.
28. Floreani, A.; Paternoster, D.; Zappala, F.; Cusinato, R.; Bombi, G.; Grella, P.; Chiaramonte, M. Hepatitis C virus infection in pregnancy. BJOG. 1996, 103, 325-329.
29. Jabeen, T.; Cannon, B.; Hogan, J.; Crowley, M.; Devereux, C.; Fanning, L.; Kenny-Walsh, E.; Shanahan, F.; Whelton, M.J. Pregnancy and pregnancy outcome in hepatitis C type 1b. QJM. 2000, 93, 597-601.
30. Gervais, A.; Bacq, Y.; Bernuau, J.; Martinot, M.; Auperin, A.; Boyer, N.; Kilani, A.; Erlinger, S.; Valla, D.; Marcellin, P. Decrease in serum ALT and increase in serum HCV RNA during pregnancy in women with chronic hepatitis C. J. Hepatol. 2000, 32, 293-299.
31. Paternoster, D.M.; Santarossa, C.; Grella, P.; Palu, G.; Baldo, V.; Boccagni, P.; Floreani, A. Viral load in HCV RNA-positive pregnant women. Am. J. Gastroenterol. 2001, 96, 2751-2754.
32. Fontaine, H.; Nalpas, B.; Carnot, F.; Brechot, C.; Pol, S. Effect of pregnancy on chronic hepatitis C: a case-control study. Lancet 2000, 356, 1328-1329.
33. Vento, S.; Longhi, M.S.; Cainelli, F.; Concia, E. Effect of pregnancy on chronic hepatitis C. Lancet 2001, 357, 389-390.
34. Oketani, M.; Shibatou, T.; Yamashita, K.; Arima, T.; Arima, T. Postpartum acute exacerbation of chronic hepatitis C with complete response to interferon-α. J. Gastroenterol. 2002, 37, 658-662.
35. Latt, N.C.; Spencer, J.D.; Beeby, P.J.; McCaughan, G.W.; Saunders, J.B.; Collins, E.; Cossart, Y.E. Hepatitis C in injecting drug-using women during and after pregnancy. J. Gastroenterol. Hepatol. 2000, 15, 175-181.
36. Romero-Gómez, M.; Suárez-García, E.; Casanovas, J.; Nogales, M.C.; Vargas, J.; Otero, M.A.; Castro Fernández, M. Influencia del embarazo en la infección crónica por el virus C de la hepatitis [Influence of pregnancy in chronic hepatitis C virus infection]. Med. Clin. (Barc). 1998, 111, 641-644.
37. Billingham, R.E.; Brent, L.; Medawar, P.B. Actively acquired tolerance of foreign cells. Nature 1953, 172, 603-606.
38. Munoz-Suano, A.; Hamilton, A.B.; Betz, A.G. Gimme shelter: the immune system during pregnancy. Immunol. Rev. 2011, 241, 20-38.
39. Lichtenstein, M.R. Tuberculin reaction in tuberculosis during pregnancy. Am. Rev. Tuberc. Pulm. Dis. 1942, 48, 89-93.
40. Raghupathy, R.; Raghupathy, R.; Makhseed, M.; Azizieh, F.; Omu, A.; Gupta, M.; Farhat, R. Cytokine production by maternal lymphocytes during normal human pregnancy and in unexplained recurrent spontaneous abortion. Hum. Reprod. 2000, 15, 713-718.
41. Narita, M.; Yamada, S.; Kikuta, H.; Togashi, T. Reconstitution of humoral immunity during pregnancy. Am. J. Reprod. Immunol. 2000, 44, 148-152.
42. Watanabe, M.; Iwatani, Y.; Kaneda, T.; Hidaka, Y.; Mitsuda, N.; Morimoto, Y.; Amino, N. Changes in T, B, and NK lymphocyte subsets during and after normal pregnancy. Am. J. Reprod. Immunol. 1997, 37, 368-377.
43. Okuyama, R.; Abo, T.; Seki, S.; Ohteki, T.; Sugiura, K.; Kusumi, A.; Kumagai, K. Estrogen administration activates extrathymic T cell differentiation in the liver. J. Exp. Med. 1992, 175, 661-669.
44. Kimura, M.; Hanawa, H.; Watanabe, H.; Ogawa, M.; Abo, T. Synchronous expansion of intermediate TCR cells in the liver and uterus during pregnancy. Cell. Immunol. 1995, 162, 16-25.
45. Aluvihare, V.R.; Kallikourdis, M.; Betz, A.G. Regulatory T cells mediate maternal tolerance to the fetus. Nat. Immunol. 2004, 5, 266-271.
46. Heikkinen, J.; Mottonen, M.; Alanen, A.; Lassila, O. Phenotypic characterization of regulatory T cells in the human decidua. Clin. Exp. Immunol. 2004, 136, 373-378.
47. +regulatory T-cell subset. Immunology 2004, 112, 38-43.
48. Rogerson, S.J.; Hviid, L.; Duffy, P.E.; Leke, R.F.; Taylor, D.W. Malaria in pregnancy: pathogenesis and immunity. Lancet Infect. Dis. 2007, 7, 105-117.
49. Da Silva, J.A.P.; Spector, T.D. The role of pregnancy in the course and etiology of rheumatoid arthritis. Clin. Rheumatol. 1992, 11, 189-194.
50. Soldan, S.S.; Alvarez Retuerto, A.I.; Sicotte, N.L.; Voskuhi, R.R. Immune modulation in multiple sclerosis patients treated with the pregnancy hormone estradiol. J. Immunol. 2003, 171, 6267-6274.
51. Nahmias, A.J.; Schollin, J.; Abramowsky, C. Evolutionary-developmental perspectives on immune system interactions among the pregnant woman, placenta, and fetus, and responses to sexually transmitted infectious agents. Ann. N. Y. Acad. Sci. 2011, 1230, 25-47.
52. Constantin, C.M.; Masopust, D.; Gourley, T.; Grayson, J.; Strickland, O.L.; Ahmed, R.; Bonney, E.A. Normal establishment of virus-specific memory CD8 T cell pool following primary infection during pregnancy. J. Immunol. 2007, 179, 4383-4389.
53. Norton, M.T.; Fortner, K.A.; Oppenheimer, K.H.; Bonney, E.A. Evidence that CD8 T-cell homeostasis and function remain intact during murine pregnancy. Immunology 2010, 131, 426-437.
54. Troesch, M.; Jalbert, E.; Canobio, S.; Boulassel, M.R.; Routy, J.P.; Bernard, N.F.; Bruneau, J.; Lapointe, N.; Boucher, M.; Soudeyns, H. Characterization of humoral and cell-mediated immune responses directed against hepatitis C virus F protein in subjects co-infected with hepatitis C virus and HIV-1. AIDS 2005, 19, 775-784.
55. o810.
56. Troesch, M.; Meunier, I.; Lapierre, P.; Lapointe, N.; Alvarez, F.; Boucher, M.; Soudeyns, H. Study of a novel hypervariable region in hepatitis C virus (HCV) E2 envelope glycoprotein. Virology 2006, 352, 357-367.
57. Cheynier, R.; Langlade-Demoyen, P.; Marescot, M.R.; Blanche, S.; Blondin, G.; Wain-Hobson, S.; Griscelli, C.; Vilmer, E.; Plata, F. Cytotoxic T lymphocyte responses in the peripheral blood of children born to human immunodeficiency virus-1-infected mothers. Eur. J. Immunol. 1992, 22, 2211-2217.
58. Rowland-Jones, S.; Nixon, D.F.; Aldhous, M.C.; Gotch, F.; Ariyoshi, K.; Hallam, N.; Kroll, J.S.; Froebel, K.; McMichael, A. HIV-specific cytotoxic T-cell activity in an HIV-exposed but uninfected infant. Lancet 1993, 341, 860-861.
59. Dauby, N.; Goetghebuer, T.; Kollmann, T.R.; Levy, J.; Marchant, A. Uninfected but not unaffected: chronic maternal infections during pregnancy, fetal immunity, and susceptibility to postnatal infections. Lancet Infect. Dis. 2012, 12, 330-340.
60. Haynes, B.F.; Heinly, C.S. Early human T cell development: analysis of the human thymus at the time of initial entry of hematopoietic stem cells into the fetal thymic microenvironment. J. Exp. Med. 1995, 181, 1445-1458.
61. Marchant, A.; Appay, V.; Van Der Sande, M.; Dulphy, N.; Liesnard, C.; Kidd, M.; Kaye, S.; Ojuola, O.; Gillespie, G.M.; Vargas Cuero, A.L.; Cerundolo, V.; Callan, M.; McAdam, K.P.; Rowland-Jones, S.L.; Donner, C.; McMichael, A.J.; Whittle, H. Mature CD8(+) T lymphocyte response to viral infection during fetal life. J. Clin. Invest. 2003, 111, 1747-1755.
62. Babik, J.M.; Cohan, D.; Monto, A.; Hartigan-O'Connor, D.J.; McCune, J.M. The human fetal immune response to hepatitis C virus exposure in utero. J. Infect. Dis. 2011, 203, 196-206.
63. Burns, D.N.; Nourjah, P.; Wright, D.J.; Minkoff, H.; Landesman, S.; Rubinstein, A.; Goedert, J.J.; Nugent, R.P. Changes in immune activation markers during pregnancy and postpartum. J. Reprod. Immunol. 1999, 42, 147-165.
64. Hattori, Y.; Orito, E.; Ohno, T.; Sugauchi, F.; Suzuki, S.; Sugiura, M.; Suzumori, K.; Hattori, K.; Ueda, R.; Mizokami, M. Loss of hepatitis C virus RNA after parturition in female patients with chronic HCV infection. J. Med. Virol. 2003, 71, 205-211.
65. Resti, M.; Azzari, C.; Mannelli, F.; Moriondo, M.; Novembre, E.; de Martino, M.; Vierucci, A. Mother to child transmission of hepatitis C virus: prospective study of risk factors and timing of infection in children born to women seronegative for HIV-1. Tuscany Study Group on Hepatitis C Virus Infection. BMJ 1998, 317, 437-441.
66. Indolfi, G.; Resti, M. Perinatal transmission of hepatitis C virus infection. J. Med. Virol. 2009, 81, 836-843.
67. Manns, M.P.; McHutchison, J.G.; Gordon, S.C.; Rustgi, V.K.; Shiffman, M.; Reindollar, R.; Goodman, Z.D.; Koury, K.; Ling, M.; Albrecht, J.K. Peginterferon alfa-2b plus ribavirin compared with interferon alfa-2b plus ribavirin for initial treatment of chronic hepatitis C: A randomised trial. Lancet 2001, 358, 958-965.
68. Fried, M.W.; Shiffman, M.L.; Reddy, K.R.; Smith, C.; Marinos, G.; Goncales, F.L.; Haussinger, D.; Diago, M.; Carosi, G.; Dhumeaux, D.; Craxi, A.; Lin, A.; Hoffman, J.; Yu, J. Peginterferon alfa-2a plus ribavirin for chronic hepatitis C virus infection. N. Engl. J. Med. 2002, 347, 975-982.
69. McHutchison, J.G.; Manns, M.P.; Muir, A.J.; Terrault, N.A.; Jacobson, I.M.; Afdhal, N.H.; Heathcote, E.J.; Zeuzem, S.; Reesink, H.W.; Garg, J.; Bsharat, M.; George, S.; Kauffman, R.S.; Adda, N.; Di Bisceglie, A.M.; PROVE3 Study Team. Telaprevir for previously treated chronic HCV infection. N. Engl. J. Med. 2010, 362, 1292-1303.
70. Poordad, F.; McCone, J.; Bacon, B.R.; Bruno, S.; Manns, M.P.; Sulkowski, M.S.; Jacobson, I.M.; Reddy, K.R.; Goodman, Z.D.; Boparai, N.; DiNubile, M.J.; Sniukiene, V.; Brass, C.A.; Albrecht, J.K.; Bronowicki, J.P.; SPRINT-2 Investigators. Boceprevir for untreated chronic HCV genotype 1 infection. N. Engl. J. Med. 2011, 364, 1195-1206.
71. Connor, E.M.; Sperling, R.S.; Gelber, R.; Kiselev, P.; Scott, G.; O'Sullivan, M.J.; VanDyke, R.; Bey, M.; Shearer, W.; Jacobson, R.L.; Jimenez, E.; O'Neill, E.; Bazin, B.; Delfraissy, J.F.; Culnane, M.; Coombs, R.; Elkins, M.; Moye, J.; Stratton, P.; Balsley, J.; Pediatric AIDS Clinical Trials Group Protocol 076 Study Group. Reduction of maternal-infant transmission of human immunodeficiency virus type 1 with zidovudine treatment. N. Engl. J. Med. 1994, 331, 1173-1180.
72. Townsend, C.L.; Cortina-Borja, M.; Peckham, C.S.; de Ruiter, A.; Lyall, H.; Tookey, P.A. Low rates of mother-to-child transmission of HIV following effective pregnancy interventions in the United Kingdom and Ireland, 2000-2006. AIDS 2008, 22, 973-981.
73. Ferm, V.H.; Willhite, C.; Kilham, L. Teratogenic effects of ribavirin on hamster and rat embryos. Teratology 1978, 17, 93-101.
74. Kilham, L.; Ferm, V.H. Congenital anomalies induced in hamster embryos with ribavirin. Science 1977, 195, 413-414.
75. Roberts, S, S.; Miller, R.K.; Jones, J.K.; Lindsay, K.L.; Greene, M.F.; Maddrey, W.C.; Williams, I.T.; Liu, J.; Spiegel, R.J. The Ribavirin Pregnancy Registry: Findings after 5 years of enrollment, 2003-2009. Birth Defects Res. A. Clin. Mol. Teratol. 2010, 88, 551-559.
76. Trotter, J.F.; Zygmunt, A.J. Conception and pregnancy during interferon-alpha therapy for chronic hepatitis C. J. Clin. Gastroenterol. 2001, 32, 76-78.
77. Labarga, P.; Pinilla, J.; Cachorro, I.; Ruiz, Y. Infant of 22 months of age with no anomalies born from a HCV-and HIV-infected mother under treatment with pegylated interferon, ribavirin and antiretroviral therapy during the first 16 weeks of pregnancy. Reprod. Toxicol. 2007, 24, 414-416.
78. Dubois, J.; Hershon, L.; Carmant, L.; Belanger, S.; Leclerc, J.M.; David, M. Toxicity profile of interferon alfa-2b in children: A prospective evaluation. J. Pediatr. 1999, 135, 782-785.
79. Marine-Barjoan, E.; Berrebi, A.; Giordanengo, V.; Favre, S.F.; Haas, H.; Moreigne, M.; Izopet, J.; Tricoire, J.; Tran, A.; Pradier, C.; Bongain, A. HCV/HIV co-infection, HCV viral load and mode of delivery: risk factors for mother-to-child transmission of hepatitis C virus? AIDS 2007, 21, 1811-1815.
80. Gibb, D.M.; Goodall, R.L.; Dunn, D.T.; Healy, M.; Neave, P.; Cafferkey, M.; Butler, K. Mother-to-child transmission of hepatitis C virus: evidence for preventable peripartum transmission. Lancet 2000, 356, 904-907.
81. European Paediatric Hepatitis C Virus Network. A significant sex--but not elective cesarean section--effect on mother-to-child transmission of hepatitis C virus infection. J. Infect. Dis. 2005, 192, 1872-1879.
82. Ghamar Chehreh, M.E.; Tabatabaei, S.V.; Khazanehdari, S.; Alavian, S.M. Effect of cesarean section on the risk of perinatal transmission of hepatitis C virus from HCV-RNA+/HIVmothers: a meta-analysis. Arch. Gynecol Obstet. 2011, 283, 255-260.
83. Arshad, M.; El-Kamary, S.S.; Jhaveri, R. Hepatitis C virus infection during pregnancy and the newborn period--are they opportunities for treatment? J. Viral. Hepat. 2011, 18, 229-236.
84. Mok, J.; Pembrey, L.; Tovo, P.A.; Newell, M.L.; European Paediatric Hepatitis C Virus Network. When does mother to child transmission of hepatitis C virus occur? Arch. Dis. Child. 2005, 90, F156-F160.
85. Pollack, H.; Hou, Z.; Hughes, A.L.; Borkowsky, W. Perinatal transmission and viral evolution of hepatitis C virus quasispecies in infants coinfected with HIV. J. Acquir. Immune Defic. Syndr. 2004, 36, 890-899.
86. Hayashida, A.; Inaba, N.; Oshima, K.; Nishikawa, M.; Shoda, A.; Hayashida, S.; Negishi, M.; Inaba, F.; Inaba, M.; Fukasawa, I.; Watanabe, H.; Takamizawa, H. Re-evaluation of the true rate of hepatitis C virus mother-to-child transmission and its novel risk factors based on our two prospective studies. J. Obstet. Gynaecol. Res. 2007, 33, 417-422.
87. Indolfi, G.; Azzari, C.; Moriondo, M.; Lippi, F.; de Martino, M.; Resti, M. Alanine transaminase levels in the year before pregnancy predict the risk of hepatitis C virus vertical transmission. J. Med. Virol. 2006, 78, 911-914.
88. Azzari, C.; Resti, M.; Moriondo, M.; Ferrari, R.; Lionetti, P.; Vierucci, A. Vertical transmission of HCV is related to maternal peripheral blood mononuclear cell infection. Blood 2000, 96, 2045-2048.
89. Azzari, C.; Moriondo, M.; Indolfi, G.; Betti, L.; Gambineri, E.; de Martino, M.; Resti, M. Higher risk of hepatitis C virus perinatal transmission from drug user mothers is mediated by peripheral blood mononuclear cell infection. J. Med. Virol. 2008, 80, 65-71.
90. Tovo, P.A.; Palomba, E.; Ferraris, G.; Principi, N.; Ruga, E.; Dallacasa, P.; Maccabruni, A. Increased risk of maternal-infant hepatitis C virus transmission for women coinfected with human immunodeficiency virus type 1. Italian Study Group for HCV Infection in Children. Clin. Infect. Dis. 1997, 25, 1121-1124.
91. Mast, E.E.; Hwang, L.Y.; Seto, D.S.; Nolte, F.S.; Nainan, O.V.; Wurtzel, H.; Alter, M.J. Risk factors for perinatal transmission of hepatitis C virus (HCV) and the natural history of HCV infection acquired in infancy. J. Infect. Dis. 2005, 192, 1880-1889.
92. Polis, C.B.; Shah, S.N.; Johnson, K.E.; Gupta, A. Impact of maternal HIV coinfection on the vertical transmission of hepatitis C virus: a meta-analysis. Clin. Infect. Dis. 2007, 44, 1123-1131.
93. Papaevangelou, V.; Pollack, H.; Rochford, G.; Kokka, R.; Hou, Z.; Chernoff, D.; Hanna, B.; Krasinski, K.; Borkowsky, W. Increased transmission of vertical hepatitis C virus (HCV) infection to human immunodeficiency virus (HIV)-infected infants of HIV-and HCVcoinfected women. J. Infect. Dis. 1998, 178, 1047-1052.
94. Blackard, J.T.; Smeaton, L.; Hiasa, Y.; Horiike, N.; Onji, M.; Jamieson, D.J.; Rodriguez, I.; Mayer, K.H.; Chung, R.T. Detection of hepatitis C virus (HCV) in serum and peripheral-blood mononuclear cells from HCV-monoinfected and HIV/HCV-coinfected persons. J. Infect. Dis. 2005, 192, 258-265.
95. Vidricaire, G.; Gauthier, S.; Tremblay, M.J. HIV-1 infection of trophoblasts is independent of gp120/CD4 Interactions but relies on heparan sulfate proteoglycans. J. Infect. Dis. 2007, 195, 1461-1471.
96. Kwiek, J.J.; Mwapasa, V.; Milner, D.A. Jr; Alker, A.P.; Miller, W.C.; Tadesse, E.; Molyneux, M.E.; Rogerson, S.J.; Meshnick, S.R. Maternal-fetal microtransfusions and HIV-1 mother-tochild transmission in Malawi. PLoS Med. 2006, 3, e10.
97. Gammill, H.S.; Nelson, J.L. Naturally acquired microchimerism. Int. J. Dev. Biol. 2010, 54, 531-543.
98. Mold, J.E.; Michaelsson, J.; Burt, T.D.; Muench, M.O.; Beckerman, K.P.; Busch, M.P.; Lee, T.H.; Nixon, D.F.; McCune, J.M. Maternal alloantigens promote the development of tolerogenic fetal regulatory T cells in utero. Science 2008, 322, 1562-1565.
99. Delamare, C.; Carbonne, B.; Heim, N.; Berkane, N.; Petit, J.C.; Uzan, S.; Grange, J.D. Detection of hepatitis C virus RNA (HCV RNA) in amniotic fluid: A prospective study. J. Hepatol. 1999, 31, 416-420.
100. Pereira, L.; Maidji, E.; McDonagh, S.; Tabata, T. Insights into viral transmission at the uterineplacental interface. Trends Microbiol. 2005, 13, 164-174.
101. Bhat, P.; Anderson, D.A. Hepatitis B virus translocates across a trophoblastic barrier. J. Virol. 2007, 81, 7200-7207.
102. Lagaye, S.; Derrien, M.; Menu, E.; Coïto, C.; Tresoldi, E.; Mauclère, P.; Scarlatti, G.; Chaouat, G.; Barré-Sinoussi, F.; Bomsel, M.; European Network for the Study of In Utero Transmission of HIV-1. Cell-to-cell contact results in a selective translocation of maternal human immunodeficiency virus type 1 quasispecies across a trophoblastic barrier by both transcytosis and infection. J. Virol. 2001, 75, 4780-4791.
103. Hygino, J.; Lima, P.G.; Filho, R.G.; Silva, A.A.; Saramago, C.S.; Andrade, R.M.; Andrade, D.M.; Andrade, A.F.; Brindeiro, R.; Tanuri, A.; Bento, C.A. Altered immunological reactivity in HIV-1-exposed uninfected neonates. Clin. Immunol. 2008, 127, 340-347.
104. Kuhn, L.; Coutsoudis, A.; Moodley, D.; Mngqundaniso, N.; Trabattoni, D.; Shearer, G.M.; Clerici, M.; Coovadia, H.M. Interferon-gamma and interleukin-10 production among HIV-1-infected and uninfected infants of HIV-1-infected mothers. Ped. Res. 2001, 50, 412-416.
105. McDonagh, S.; Maidji, E.; Ma, W.; Chang, H.T.; Fisher, S.; Pereira, L. Viral and bacterial pathogens at the maternal-fetal interface. J. Infect. Dis. 2004, 190, 826-834.
106. Dye, J.F.; Jablenska, R.; Donnelly, J.L.; Lawrence, L.; Leach, L.; Clark, P.; Firth, J.A. Phenotype of the endothelium in the human term placenta. Placenta 2001, 22, 32-43.
107. Ethier-Chiasson, M.; Duchesne, A.; Forest, J.C.; Giguere, Y.; Masse, A.; Mounier, C.; Lafond, J. Influence of maternal lipid profile on placental protein expression of LDLr and SR-BI. Biochem. Biophys. Res. Comm. 2007, 359, 8-14.
108. Soilleux, E.J.; Barten, R.; Trowsdale, J. DC-SIGN; a related gene, DC-SIGNR; and CD23 form a cluster on 19p13. J. Immunol. 2000, 165, 2937-2942.
109. Nie, Q.H.; Gao, L.H.; Cheng, Y.Q.; Huang, X.F.; Zhang, Y.F.; Luo, X.D.; Wang, J.Q.; Wang, Y.Y. Hepatitis C virus infection of human cytotrophoblasts cultured in vitro. J. Med. Virol. 2012, 84, 1586-1592.
110. Hurtado, C.W.; Golden-Mason, L.; Brocato, M.; Krull, M.; Narkewicz, M.R.; Rosen, H.R. Innate immune function in placenta and cord blood of hepatitis C-seropositive mother-infant dyads. PloS One 2010, 5, e12232.
111. Pelletier, S.; Drouin, C.; Bédard, N.; Khakoo, S.I.; Bruneau, J.; Shoukry, N.H. Increased degranulation of natural killer cells during acute HCV correlates with the magnitude of virusspecific T cell responses. J. Hepatol. 2010, 53, 805-816.
112. +NK cells in acute HCV infection may predict viral clearance. J Hepatol. 2011, 55, 278-288.
113. Durante-Mangoni, E.; Wang, R.; Shaulov, A.; He, Q.; Nasser, I.; Afdhal, N.; Koziel, M.J.; Exley, M.A. Hepatic CD1d expression in hepatitis C virus infection and recognition by resident proinflammatory CD1d-reactive T cells. J. Immunol. 2004, 173, 2159-2166.
114. Farci, P.; Quinti, I.; Farci, S.; Alter, H.J.; Strazzera, R.; Palomba, E.; Coiana, A.; Cao, D.; Casadei, A.M.; Ledda, R.; Iorio, R.; Vegnente, A.; Diaz, G.; Tovo, P.A. Evolution of hepatitis C viral quasispecies and hepatic injury in perinatally infected children followed prospectively. Proc. Natl Acad. Sci. USA. 2006, 103, 8475-8480.
115. Gerotto, M.; Resti, M.; Dal Pero, F.; Migliorato, I.; Alberti, A.; Bortolotti, F. Evolution of hepatitis C virus quasispecies in children with chronic hepatitis C. Infection 2006, 34, 62-65.
116. Manzin, A.; Solforosi, L.; Debiaggi, M.; Zara, F.; Tanzi, E.; Romano, L.; Zanetti, A.R.; Clementi, M. Dominant role of host selective pressure in driving hepatitis C virus evolution in perinatal infection. J. Virol. 2000, 74, 4327-4334.
117. Dowd, K.A.; Hershow, R.C.; Yawetz, S.; Larussa, P.; Diaz, C.; Landesman, S.H.; Paul, M.E.; Read, J.S.; Lu, M.; Thomas, D.L.; Netski, D.M.; Ray, S.C. Maternal neutralizing antibody and transmission of hepatitis C virus to infants. J. Infect. Dis. 2008, 198, 1651-1655.
118. Meunier, J.C.; Bukh, J.; Diaz, G.; Tovo, P.A.; Casadei, A.M.; Quinti, I.; Iorio, R.; Emerson, S.; Purcell, R.H.; Farci, P. Neutralizing antibodies to hepatitis C virus in perinatally infected children followed up prospectively. J. Infect. Dis. 2011, 204, 1741-1745.
119. Yeung, L.T.; King, S.M.; Roberts, E.A. Mother-to-infant transmission of hepatitis C virus. Hepatology 2001, 34, 223-229.
120. Centers for Disease Control and Prevention. Recommendations for prevention and control of hepatitis C virus (HCV) infection and HCV-related chronic disease. MMWR 1998, 47, No. RR-19.
121. Centers for Disease Control and Prevention. Recommendations for the identification of chronic hepatitis C virus infection among persons born during 1945-1965. MMWR 2012, 61, No. RR-4.
122. Resti, M.; Jara, P.; Hierro, L.; Azzari, C.; Giacchino, R.; Zuin, G.; Zancan, L.; Pedditzi, S.; Bortolotti, F. Clinical features and progression of perinatally acquired hepatitis C virus infection. J. Med. Virol. 2003, 70, 373-377.
123. Tovo, P.A.; Pembrey, L.J.; Newell, M.L. Persistence rate and progression of vertically acquired hepatitis C infection. European Paediatric Hepatitis C Virus Infection. J. Infect. Dis. 2000, 181, 419-424.
124. Yeung, L.T.; To, T.; King, S.M.; Roberts, E.A. Spontaneous clearance of childhood hepatitis C virus infection. J. Viral Hepat. 2007, 14, 797-805.
125. Alter, H.J.; Seeff, L.B. Recovery, persistence, and sequelae in hepatitis C virus infection: A perspective on long-term outcome. Semin. Liv. Dis. 2000, 20, 17-35.
126. Vogt, M.; Lang, T.; Frosner, G.; Klingler, C.; Sendl, A.F.; Zeller, A.; Wiebecke, B.; Langer, B.; Meisner, H.; Hess, J. Prevalence and clinical outcome of hepatitis C infection in children who underwent cardiac surgery before the implementation of blood-donor screening. New Engl. J. Med. 1999, 341, 866-870.
127. El-Kamary, S.S.; Hashem, M.; Saleh, D.A.; Abdelwahab, S.F.; Sobhy, M.; Shebl, F.M.; Shardell, M.D.; Strickland, G.T.; Shata, M.T. Hepatitis C virus-specific cell-mediated immune responses in children born to mothers infected with hepatitis C virus. J. Pediatr. 2012, in press.
128. European Paediatric Hepatitis C Virus Network. Three broad modalities in the natural history of vertically acquired hepatitis C virus infection. Clin. Infect. Dis. 2005, 41, 45-51.
129. Jonas, M.M. Children with hepatitis C. Hepatology 2002, 36, S173-178.
130. Palomba, E.; Manzini, P.; Fiammengo, P.; Maderni, P.; Saracco, G.; Tovo, P.A. Natural history of perinatal hepatitis C virus infection. Clin. Infect. Dis. 1996, 23, 47-50.
131. Gismondi, M.I.; Becker, P.D.; Diaz Carrasco, J.M.; Guzman, C.A.; Campos, R.H.; Preciado, M.V. Evolution of hepatitis C virus hypervariable region 1 in immunocompetent children born to HCV-infected mothers. J. Viral Hepat. 2009, 16, 332-339.
132. Canobio, S,; Guilbert, C.; Troesch, M.; Samson, J.; Lemay, M.; Pelletier, V.A.; Bernard-Bonnin, A.C.; Kozielski, R.; Lapointe, N.; Martin, S.R.; Soudeyns, H. Differing patterns of liver disease progression and hepatitis C virus (HCV) quasispecies evolution in children vertically coinfected with HCV and human immunodeficiency virus type 1. J. Clin. Microbiol. 2004, 42, 4365-4369.
133. Quesnel-Vallières, M.; Lemay, M.; Lapointe, N.; Martin, S.R.; Soudeyns, H. HCV quasispecies evolution during treatment with interferon alfa-2b and ribavirin in two children coinfected with HCV and HIV-1. J. Clin. Virol. 2008, 43, 236-240.
134. Gaud, U.; Langer, B.; Petropoulou, T.; Thomas, H.C.; Karayiannis, P. Changes in hypervariable region 1 of the envelope 2 glycoprotein of hepatitis C virus in children and adults with humoral immune defects. J. Med. Virol. 2003, 69, 350-356.
135. Larouche, A.; Gaëtan, G.; El-Bilali, N.; Quesnel-Vallières, M.; Martin, S.R.; Alvarez, F.; Shoukry, N.H.; Soudeyns, H. A case of seronegative HCV infection in a child infected via mother-to-child transmission. J. Clin. Microbiol. 2012, 50, 2515-2519.
136. Castello, G.; Scala, S.; Palmieri, G.; Curley, S.A.; Izzo, F. HCV-related hepatocellular carcinoma: From chronic inflammation to cancer. Clin. Immunol. 2010, 134, 237-250.
137. Wirth, S.; Ribes-Koninckx, C.; Calzado, M.A.; Bortolotti, F.; Zancan, L.; Jara, P.; Shelton, M.; Kerkar, N.; Galoppo, M.; Pedreira, A.; Rodriguez-Baez, N.; Ciocca, M.; Lachaux, A.; Lacaille, F.; Lang, T.; Kullmer, U.; Huber, W.D.; Gonzalez, T.; Pollack, H.; Alonso, E.; Broue, P.; Ramakrishna, J.; Neigut, D.; Valle-Segarra, A.D.; Hunter, B.; Goodman, Z.; Xu, C.R.; Zheng, H.; Noviello, S.; Sniukiene, V.; Brass, C.; Albrecht, J.K. High sustained virologic response rates in children with chronic hepatitis C receiving peginterferon alfa-2b plus ribavirin. J. Hepatol. 2010, 52, 501-507.
138. Schwarz, K.B.; Gonzalez-Peralta, R.P.; Murray, K.F.; Molleston, J.P.; Haber, B.A.; Jonas, M.M.; Rosenthal, P.; Mohan, P.; Balistreri, W.F.; Narkewicz, M.R.; Smith, L.; Lobritto, S.J.; Rossi, S.; Valsamakis, A.; Goodman, Z.; Robuck, P.R.; Barton, B.A.; Peds-C Clinical Research Network. The combination of ribavirin and peginterferon is superior to peginterferon and placebo for children and adolescents with chronic hepatitis C. Gastroenterology 2011, 140, 450-458.
139. Mack, C.L.; Gonzalez-Peralta, R.P.; Gupta, N.; Leung, D.; Narkewicz, M.R.; Roberts, E.A.; Rosenthal, P.; Schwarz, K.B.; North American Society for Pediatric Gastroenterology, Hepatology, and Nutrition. NASPGHAN practice guidelines: Diagnosis and management of hepatitis C infection in infants, children, and adolescents. J. Pediatr. Gastroenterol. Nutr. 2012, 54, 838-855.
140. Pharmacokinetics of Boceprevir in Pediatric Subjects With Chronic Hepatitis C Genotype 1 (SCH503034-P07614 AM4). Available online: http://clinicaltrials.gov/ct2/show/NCT01425190 (accessed on 29 September 2012).