A guide to the management of hepatitis E infection during pregnancy

References

• Rein DB, Stevens GA, Theaker J, et al. The global burden of hepatitis E genotypes 1 and 2 in 2005. Hepatology. 2012;55(4):988–997.
   PubMed Web of Science ®Google Scholar
• Tam AW, Smith MM, Guerra ME, et al. Hepatitis E virus (HEV): molecular cloning and sequencing of the full-length viral genome. Virology. 1991;185:120–131.
   PubMed Web of Science ®Google Scholar
• Pérez‐Gracia MT, Mateos Lindemann ML, Montalvo Villalba MC, et al. Current status. Rev Med Virol. 2013;23:384‐398.
   PubMed Web of Science ®Google Scholar
• Lee GH, Tan BH, Chi‐Yuan E, et al. Chronic infection with camelid hepatitis E virus in a liver transplant recipient who regularly consumes camel meat and milk. Gastroenterology. 2016;150:355‐357.
   Web of Science ®Google Scholar
• Purcell RH, Emerson SU, Hepatitis E. an emerging awareness of an old disease. J Hepatol. 2008 Mar;48(3):494–503.
   PubMed Web of Science ®Google Scholar
• Acharya SK, Dasarathy S, Kumer TL, et al. Fulminant hepatitis in a tropical population: clinical course, cause, and early predictors of outcome. Hepatology. 1996;23:1448‐1455.
   PubMed Web of Science ®Google Scholar
• Patra S, Kumar A, Trivedi SS, et al. Maternal and fetal outcomes in pregnant women with acute hepatitis E virus infection. Ann Intern Med. 2007a;147:28‐33.
   PubMed Web of Science ®Google Scholar
• Rein DB, Stevens GA, Theaker J, et al. The global burden of hepatitis E virus genotypes 1 and 2 in 2005. Hepatology. 2012;55:988‐997.
   PubMed Web of Science ®Google Scholar
• Hussaini SH, Skidmore SJ, Richardson P, et al. Severe hepatitis E infection during pregnancy. J Viral Hepat. 1997;4:51‐54.
   PubMed Web of Science ®Google Scholar
• Pérez-Gracia MT, Suay-García B, Mateos-Lindemann ML. Hepatitis E and pregnancy: current state. Reviews in Medical Virology. 2017;27(3):e1929.
   PubMed Web of Science ®Google Scholar
• Khuroo MS, Teli MR, Skidmore S, et al. Incidence and severity of viral hepatitis in pregnancy. Am J Med. 1981 Feb;70(2):252–255.
   PubMed Web of Science ®Google Scholar
• Shrestha S. An epidemic of hepatitis E in Nepal: clinical and epidemiological study. J Inst Med. 1990;12:195‐204.
   Google Scholar
• Anty R, Ollier L, Péron JM, et al. First case report of an acute genotype 3 hepatitis E infected pregnant woman living in south‐eastern France. J Clin Virol. 2012;54:76‐78.
   PubMed Web of Science ®Google Scholar
• Tabatabai J, Wenzel JJ, Soboletzki M, et al. First case report of an acute hepatitis E subgenotype 3c infection during pregnancy in Germany. J Clin Virol. 2014;61:170‐172.
   PubMed Web of Science ®Google Scholar
• Renou C, Gobert V, Locher C, et al. Prospective study of hepatitis E virus infection among pregnant women in France. Virol J. 2014;11:68.
   PubMed Web of Science ®Google Scholar
• Khuroo MS, Kamili S, Jameel S. Vertical transmission of hepatitis E virus. Lancet. 1995;345:1025‐1026.
   PubMedGoogle Scholar
• Kumar RM, Uduman S, Rana S, et al. Seroprevalence and mother‐to‐infant transmission of hepatitis E virus among pregnant women in the United Arab Emirates. Eur J Obstet Gynecol Reprod Biol. 2001;100:9‐15.
   PubMed Web of Science ®Google Scholar
• Gouilly J, Chen Q, Siewiera J, et al. Genotype specific pathogenicity of hepatitis E virus at the human maternal-fetal interface. Nat Commun. 2018;9(1).
   PubMedGoogle Scholar
• Meeusen EN, Bischof RJ, Lee CS. Comparative T‐cell responses during pregnancy in large animals and humans. Am J Reprod Immunol. 2001;46:169‐179.
   PubMed Web of Science ®Google Scholar
• Pal R, Aggarwal R, Naik SR, et al. Immunological alterations in pregnant women with acute hepatitis E. J Gastroenterol Hepatol. 2005;20:1094‐1101.
   Web of Science ®Google Scholar
• Dudley DJ, Chen C, Mitchell MD, et al. Adaptive immune responses during murine pregnancy: pregnancy-induced regulation of lymphokine production by activated T lymphocytes. Am J Obstet Gynecol. 1993;168:1155–1163.
   PubMed Web of Science ®Google Scholar
• Jilani N, Das BC, Husain SA, et al. Hepatitis E virus infection and fulminant hepatic failure during pregnancy. J Gastroenterol Hepatol. 2007;22:676‐682.
   PubMed Web of Science ®Google Scholar
• Prusty BK, Hedau S, Singh A, et al. Selective suppression of NF‐kBp65 in hepatitis virus‐infected pregnant women manifesting severe liver damage and high mortality. Mol Med. 2007;13:518‐526.
   PubMed Web of Science ®Google Scholar
• Bhatnagar G, Sharma S, Kumar A, et al. Reduced glutathione in hepatitis E infection and pregnancy outcome. J Obstet Gynaecol Res. 2016;42:789‐795.
   PubMed Web of Science ®Google Scholar
• Kmush BL, Labrique A, Li W, et al. The association of cytokines and micronutrients with hepatitis e virus infection during pregnancy and the postpartum period in rural Bangladesh. Am J Trop Med Hyg. 2016;94:203‐211.
   PubMed Web of Science ®Google Scholar
• Labrique AB, Klein S, Kmush B, et al. Immunologic dysregulation and micronutrient deficiencies associated with risk of intrapartum hepatitis E infections in pregnant Bangladeshi women. FASEB J. 2012;26:127.4.
   Web of Science ®Google Scholar
• Puri M, Patra S, Singh P, et al. Factors influencing occurrence of postpartum haemorrhage in pregnant women with hepatitis E infection and deranged coagulation profile. Obstet Med. 2011;4:108‐112.
   PubMedGoogle Scholar
• Gurley ES, Halder AK, Streatfield PK, et al. Estimating the burden of maternal and neonatal deaths associated with jaundice in Bangladesh: possible role of hepatitis E infection. Am J Public Health. 2012;102:2248‐2254.
   PubMed Web of Science ®Google Scholar
• Teo CG. Fatal outbreaks of jaundice in pregnancy and the epidemic history of hepatitis E. Epidemiol Infect. 2012;140(5):767–787.
   PubMed Web of Science ®Google Scholar
• Ranger-Rogez S, Alain S, Denis F. Hepatitis viruses: mother to child transmission. Pathol Biol. 2002;50(9):568–575.
   PubMedGoogle Scholar
• Khuroo MS, Kamil S. Aetiology, clinical course and outcome of sporadic acute viral hepatitis in pregnancy. J Viral Hepat. 2003;10:61‐69.
   Web of Science ®Google Scholar
• Kaskheli MN, Baloch S, Sheeba A, et al. Acute hepatitis E viral infection in pregnancy and maternal morbidity. J Coll Physicians Surg Pak. 2015;24:734‐737.
   Google Scholar
• Krain LJ, Atwell JE, Nelson KE, et al. Fetal and neonatal health consequences of vertically transmitted hepatitis E virus infection. Am J Trop Med Hyg. 2014;90(2):365–370.
   PubMed Web of Science ®Google Scholar
• Naidu SS, Viswanathan R. Infectious hepatitis in pregnancy during Delhi epidemic. Indian J Med Res. 1957;45(Suppl):71–76.
   PubMedGoogle Scholar
• Rasheeda CA, Navaneethan U, Jayanthi V. Liver disease in pregnancy and its influence on maternal and fetal mortality: a prospective study from Chennai, Southern India. Eur J Gastroenterol Hepatol. 2008;20(4):362–364.
   PubMed Web of Science ®Google Scholar
• Rayis DA, Jumaa AM, Gasim GI, et al. An outbreak of hepatitis E and high maternal mortality at Port Sudan, Eastern Sudan. Pathog Glob Health. 2013;107(2):66–68.
   PubMed Web of Science ®Google Scholar
• Stoszek SK, Abdel-Hamid M, Saleh DA, et al. High prevalence of hepatitis E antibodies in pregnant Egyptian women. Trans R Soc Trop Med Hyg. 2006;100:95–101.
   PubMed Web of Science ®Google Scholar
• Stoszek SK, Engle RE, Abdel-Hamid M, et al. Hepatitis E antibody seroconversion without disease in highly endemic rural Egyptian communities. Trans R Soc Trop Med Hyg. 2006;100:89–94.
   PubMed Web of Science ®Google Scholar
• Lachish T, Erez O, Daudi N, et al. Acute hepatitis E virus in pregnant women in Israel and in other industrialized countries. J Clin Virol. 2015;73:20‐24.
   PubMed Web of Science ®Google Scholar
• Aggarwal R, Goel A. Advances in hepatitis E‐I: virology, pathogenesis and diagnosis. Expert Rev Gastroenterol Hepatol. 2016;10:1053‐1063.
   Web of Science ®Google Scholar
• Dawson GJ, Mushahwar IK, Chau KH, et al. Detection of long‐ lasting antibody to hepatitis E virus in a US traveller to Pakistan. Lancet. 1992;340:426‐427.
   Web of Science ®Google Scholar
• Bendall R, Ellis V, Ijaz S, et al. A comparison of two commercially available anti‐HEV IgG kits and a re‐evaluation of anti‐HEV seroprevalence data in developed countries. J Med Virol. 2010;82:799‐805.
   PubMed Web of Science ®Google Scholar
• Pas S, Streefkerk R, Pronk M, et al. Diagnostic performance of selected commercial HEV IgM and IgG ELISAs for immunocompromised and immunocompetent patients. J Clin Virol. 2013;58(4):629–634.
   PubMed Web of Science ®Google Scholar
• Abravanel F, Chapuy-Regaud S, Lhomme S, et al. Performance of anti-HEV assays for diagnosing acute hepatitis E in immunocompromised patients. J Clin Virol. 2013;58(4):624–628.
   PubMed Web of Science ®Google Scholar
• Hyams C, Da M, Copping R, et al. Serological cross reactivity to CMV and EBV causes problems in the diagnosis of acute hepatitis E virus infection. J Med Virol. 2014;86(3):478-83.
   PubMed Web of Science ®Google Scholar
• Baylis SA, Hanschmann KM, Blumel J, et al. Standardization of hepatitis E virus (HEV) nucleic acid amplification technique-based assays: an initial study to evaluate a panel of HEV strains and investigate laboratory performance. J Clin Microbiol. 2011 Apr;49(4):1234–1239.
   PubMed Web of Science ®Google Scholar
• Sauleda S, Ong E, Bes M, et al. Seroprevalence of hepatitis E virus (HEV) and detection of HEV RNA with a transcription-mediated amplification assay in blood donors from Catalonia (Spain). Transfusion. 2015 May;55(5):972–979.
   PubMed Web of Science ®Google Scholar
• Lan X, Yang B, Li BY, et al. Reverse transcription-loop-mediated isothermal amplification assay for rapid detection of hepatitis E virus. J Clin Microbiol. 2009 Jul;47(7):2304–2306.
   PubMed Web of Science ®Google Scholar
• Sarin SK, Kumar M, Hepatitis E. Zakim & Boyer’s hepatology: a textbook of liver disease. 5th ed; Philadelphia, PA: Saunders Elsevier. 2006:693–724.
   Google Scholar
• Kamar N, Bendall R, Legrand-Abravanel F, et al. Hepatitis E. Lancet. 2012;379(9835):2477–2488.
   PubMed Web of Science ®Google Scholar
• Kamar N, Selves J, Mansuy JM, et al. Hepatitis E virus and chronic hepatitis in organ-transplant recipients. N Engl J Med. 2008;358:811–817.
   PubMed Web of Science ®Google Scholar
• Wen GP, Tang ZM, Yang F, et al. A valuable antigen detection method for the diagnosis of acute hepatitis E. J Clin Microbiol. 2015 Mar;53(3):782–788.
   PubMed Web of Science ®Google Scholar
• Myint KS, Guan M, Chen HY, et al. Evaluation of a new rapid immunochromatographic assay for serodiagnosis of acute hepatitis E infection. Am J Trop Med Hyg. 2005 Nov;73(5):942–946.
   PubMed Web of Science ®Google Scholar
• Legrand-Abravanel F, Thevenet I, Mansuy JM, et al. Good performance of immunoglobulin M assays in diagnosing genotype 3 hepatitis E virus infections. Clin Vaccine Immunol. 2009 May;16(5):772–774.
   PubMed Web of Science ®Google Scholar
• Abravanel F, Lhomme S, Chapuy-Regaud S, et al. Performance of a new rapid test for detecting anti-hepatitis E virus immunoglobulin M in immunocompetent and immunocompromised patients. J Clin Virol. 2015;70:101–104.
   PubMed Web of Science ®Google Scholar
• Bhatia V, Singhal A, Panda SK, et al. A 20-year single-center experience with acute liver failure during pregnancy: is the prognosis really worse? Hepatology. 2008 Nov;48(5):1577–1585.
   PubMed Web of Science ®Google Scholar
• Dao Thi VL, Debing Y, Wu X, et al. Sofosbuvir inhibits hepatitis E virus replication in vitro and results in an additive effect when combined with ribavirin. Gastroenterology. 2016 Jan;150(1):82–85.e4.
   PubMed Web of Science ®Google Scholar
• Van der Valk M, Zaaijer HL, Kater AP, et al. Sofosbuvir shows antiviral activity in a patient with chronic hepatitis E virus infection. J Hepatol. 2017 Jan;66(1):242–243.
   PubMedGoogle Scholar
• Mjahed K, Charra B, Hamoudi D, et al. Acute fatty liver of pregnancy. Arch Gynecol Obstet. 2006;274:349–353.
   PubMedGoogle Scholar
• Banait VS, Sandur V, Parikh F, et al. Outcome of acute liver failure due to acute hepatitis E in pregnant women. Indian J Gastroenterol. 2007;26:6–10.
   PubMedGoogle Scholar
• Pandey CK, Karna ST, Pandey VK, et al. Acute liver failure in pregnancy: challenges and management. Indian J Anaesth. 2015 Mar;59(3):144–149.
   PubMed Web of Science ®Google Scholar
• O’Grady JG, Alexander GJ, Hayllar KM, et al. Early indicators of prognosis in fulminant hepatic failure. Gastroenterology. 1989;97:439–445.
   PubMed Web of Science ®Google Scholar
• Laifer SA, Darby MJ, Scantlebury VP, et al. Pregnancy and liver transplantation. Obstet Gynecol. 1990;76:1083–1088.
   PubMed Web of Science ®Google Scholar
• Jarufe N, Soza A, Pérez-Ayuso RM, et al. Successful liver transplantation and delivery in a woman with fulminant hepatic failure occurring during the second trimester of pregnancy. Liver Int. 2006;26:494–497.
   PubMed Web of Science ®Google Scholar
• Moreno EG, García GI, Gómez SR, et al. Fulminant hepatic failure during pregnancy successfully treated by orthotopic liver transplantation. Transplantation. 1991;52:923–926.
   PubMed Web of Science ®Google Scholar
• Valentine JM, Parkin G, Pollard SG, et al. Combined orthotopic liver transplantation and caesarean section for the Budd-Chiari syndrome. Br J Anaesth. 1995;75:105–108.
   PubMed Web of Science ®Google Scholar
• Rivero-Juarez A, Frias M, Rodriguez-Cano D, et al. Isolation of eepatitis E virus from breast milk during acute infection. Clin Infect Dis. 2016 Jun 1;62(11):1464.
   PubMed Web of Science ®Google Scholar
• Kumar RM, Uduman S, Rana S, et al. Sero-prevalence and mother-to-infant transmission of hepatitis E virus among pregnant women in the United Arab Emirates. Eur J Obstet Gynecol Reprod Biol. 2001;100(1):9–15.
   PubMed Web of Science ®Google Scholar
• Chibber RM, Usmani MA, Al-Sibai MH. Should HEV infected mothers breast feed? Arch Gynecol Obstet. 2004;270(1): 15–20. Epub 2003 Apr 16.
   PubMedGoogle Scholar
• Committee to Advise on Tropical Medicine and Travel (CATMAT). An advisory committee statement (ACS). Statement to travellers’ diarrhea. Can Commun Dis Rep. 2001;27:1‐12.
   Google Scholar
• Li SW, Zhao Q, Wu T, et al. The development of a recombinant hepatitis E vaccine HEV 239. Hum Vaccin Immunother. 2015;11:908‐914.
   Web of Science ®Google Scholar
• Josh SS, Arankalle VA. Enhanced humoral response in pregnant mice immunized with liposome encapsulated recombinant neutralizing epitope protein of hepatitis E virus. Virol J. 2015;12:70.
   PubMed Web of Science ®Google Scholar
• Arankalle VA, Chadha MS, Dama BM, et al. Role of immune serum globulins in pregnant women during an epidemic of hepatitis E. J Viral Hepat. 1998;5:199–204.
   PubMed Web of Science ®Google Scholar