Hepatitis E in India

Review

Abstract

Hepatitis E is an enterically transmitted disease prevalent in developing countries in epidemic and sporadic forms. The waterborne epidemic of hepatitis in Delhi in 1955 was shown to be due to non-A–non-B aetiology, later confirmed as hepatitis E. Thereafter, a large number of epidemics of the disease have been reported from different parts of the country. Hepatitis E is the major cause of sporadic viral hepatitis among adults. High mortality among pregnant women, especially in the third trimester, and predilection for young adults remain the characteristic feature. However, the exact reasons remain unidentified. Hepatitis E virus (HEV) is an RNA virus belonging to a newly identified Hepeviridae family. The human HEV from India belongs to genotype-1 while pigs circulate genotype-4. So far, no zoonotic transmission is reported. The virus has been shown in water, sewage and soil samples. Faecal contamination of drinking water is the major source of HEV infection. Intrafamilial and parenteral transmissions are rare. The virus was transmitted to chimpanzees and rhesus monkeys. Highly sensitive and specific immunoassays have been developed for the detection of both IgM and IgG-anti-HEV antibodies. A clinical trial is awaited following the development of an effective recombinant protein-based vaccine. A significant reduction in hepatitis E was shown in pregnant women receiving human immunoglobulins. Several basic studies have thrown light on the role of different genes/proteins of the virus in the pathogenesis/replication of the virus.

Keywords

Enterically transmitted non-A Non-B virus Epidemiology Hepeviridae Swine HEV Genotypes Recombinant vaccine 

References

  1. 1.
    Viswanathan R (1957) Infectious hepatitis in Delhi (1955–56): a critical study; epidemiology. Ind J Med Res 45(suppl 1):1–30Google Scholar
  2. 2.
    Sreenivasan MA, Banerjee K, Pandya PG, Kotak RR, Pandya PM, Desai NJ et al (1977) Epidemiological investigations of an outbreak of infectious hepatitis in Ahmedabad city during 1975–76. Indian J Med Res 67:197–206Google Scholar
  3. 3.
    Pavri KM, Niphadkar KB, Sheikh BH (1972) Retrospective studies on Australia antigen in sera collected during the epidemic of viral hepatitis in Delhi in 1956. Indian J Med Res 60:1575PubMedGoogle Scholar
  4. 4.
    Wong DC, Purcell RH, Sreenivasan MA, Prasad SR, Pavri KM (1980) Epidemic and endemic hepatitis in India: evidence for a non A non B hepatitis aetiology. Lancet 2:876–879PubMedGoogle Scholar
  5. 5.
    Khuroo MS (1980) Study of an epidemic of non-A non-B hepatitis: possibility of another human hepatitis virus distinct from post-transfusion non-A, non-B type. Am J Med 68:818–824PubMedGoogle Scholar
  6. 6.
    Prince AM, Brotman B, Grady GF, Khuns WJ, Hazzi C, Levine RW, Millian SJ (1947) Long-incubation post-transfusion hepatitis without serological evidence for exposure to hepatitis B virus. Lancet 2:241–246Google Scholar
  7. 7.
    Khuroo MS, Teli RT, Skidmore S, Sofi MA, Khuroo HI (1981) Incidence and severity of viral hepatitis in pregnancy. Am J Med 70:252–255PubMedGoogle Scholar
  8. 8.
    Khuroo MS, Duermeyer W, Zargar SA, Ahanger MA, Shah MA (1983) Acute sporadic non-A, non B hepatitis in India. Am J Epidemiol 118:360–364PubMedGoogle Scholar
  9. 9.
    Arankalle VA, Chobe LP, Jha J, Chadha MS, Banerjee K, Favorov MO, Kalinina T, Fields H (1993) Aetiology of acute sporadic non-A, non-B viral hepatitis in India. J Med Virol 40:121–125PubMedGoogle Scholar
  10. 10.
    Chadha MS, Walimbe AM, Chobe LP, Arankalle VA (2003) Comparison of etiology of sporadic acute and fulminant viral hepatitis in hospitalized patients in Pune, India during 1978–81 and 1994–97. Indian J Gastroenterol 22:11–15PubMedGoogle Scholar
  11. 11.
    Kar P, Budhiraja S, Narang A, Chakravarthy A (1997) Etiology of sporadic acute and fulminant non-A, non-B viral hepatitis in north India. Indian J Gastroenterol 16:43–45PubMedGoogle Scholar
  12. 12.
    Balayan MS, Andjaparidze AG, Savinskaya SS, Ketiladze ES, Braginsky DN, Savinov AP et al (1993) Evidence for a virus in non-A non-B hepatitis transmitted via fecal-oral route. Intervirology 20:23–31Google Scholar
  13. 13.
    Sreenivasan MA, Arankalle VA, Sehgal A, Pavri KM (1984) Non-A, non-B hepatitis: visualisation of virus-like particles in the stool by immune electron microscopy. J Gen Virol 65:1005–1008PubMedGoogle Scholar
  14. 14.
    Chauhan A, Jameel S, Dilawari JB, Chawla YK, Kaur U, Ganguly NK (1993) Hepatitis E virus transmission to a volunteer. Lancet 341:149–150PubMedGoogle Scholar
  15. 15.
    Arankalle VA, Ticehurst JT, Sreenivasan MA, Kapikian AZ, Popper H, Pavri KM, Purcell RH (1988) Etiologic association of a virus-like particle with enterically transmitted non-A non-B hepatitis. Lancet 1:550–554PubMedGoogle Scholar
  16. 16.
    Gupta H, Joshi YK, Varma A, Shenoy S, Sriramchari S, Iyenger B, Tandon BN (1990) Transmission of enteric non-A, non-B hepatitis virus in Macaca mulatta monkeys by intraportal route: subsequent passages of HEV virus. J Gastroenterol Hepatol 5:608–615PubMedGoogle Scholar
  17. 17.
    Jameel S, Durgapal H, Habibullah CM, Khuroo MS, Panda SK (1992) Enteric non-A, non-B hepatitis: epidemics, animal transmission, and hepatitis E virus detection by the polymerase chain reaction. J Med Virol 37:263–270PubMedGoogle Scholar
  18. 18.
    Vrati S, Giri DK, Parida SK, Talwar GP (1992) An epidemic of non-A, non-B hepatitis in south Delhi: epidemiological studies and transmission of the disease to rhesus monkeys. Arch Virol 125:319–326PubMedGoogle Scholar
  19. 19.
    Arankalle VA, Chadha MS, Banerjee K, Srinivasan MA, Chobe LP (1993) Hepatitis E virus infection in pregnant rhesus monkeys. Indian J Med Res 97:4–8PubMedGoogle Scholar
  20. 20.
    Arankalle VA, Favorov MO, Chadha MS, Phule DM, Banerjee K (1993) Rhesus monkeys infected with hepatitis E virus (HEV) from the former USSR are immune to subsequent challenge with an Indian strain of HEV. Acta Virol 37:515–518PubMedGoogle Scholar
  21. 21.
    Arankalle VA, Chadha MS, Chobe LP, Nair R, Banerjee K (1995) Cross-challenge studies in rhesus monkeys employing different Indian isolates of hepatitis E virus. J Med Virol 46:358–363PubMedGoogle Scholar
  22. 22.
    Arankalle VA, Chadha MS, Chobe LP (1999) Long-term serological follow up and cross-challenge studies in rhesus monkeys experimentally infected with hepatitis E virus. J Hepatol 30:199–204PubMedGoogle Scholar
  23. 23.
    Arankalle VA, Paranjape S, Emerson SU, Purcell RH, Walimbe AM (1999) Phylogenetic analysis of hepatitis E virus isolates from India (1976–1993). J Gen Virol 80:1691–1700PubMedGoogle Scholar
  24. 24.
    Arankalle VA, Chadha MS, Tsarev SA, Emerson SU, Risbud AR, Banerjee K, Purcell RH (1994) Seroepidemiology of water-borne hepatitis in India and evidence for a third enterically-transmitted hepatitis agent. Proc Natl Acad Sci USA 91:3428–3432PubMedGoogle Scholar
  25. 25.
    Sreenivasan MA, Sehgal A, Prasad SR, Dhorje SA (1984) Seroepidemiologic study of a waterborne epidemic of viral hepatitis in Kolhapur city. Indian J Hyg 93:113–122Google Scholar
  26. 26.
    Dilawari JB, Singh K, Chawla YK, Ramesh GN, Chauhan A, Bhusnurmath SR, Sharma TR, Sokhey CS (1994) Hepatitis E virus: epidemiological, clinical and serological studies of north Indian epidemic. Indian J Gastroenterol 13:44–48PubMedGoogle Scholar
  27. 27.
    Naik SR, Aggarwal R, Salunke PN, Mehrotra NN (1992) A large waterborne viral hepatitis E epidemic in Kanpur, India. Bull World Health Organ 70:597–604PubMedGoogle Scholar
  28. 28.
    Gupta RS, Jain DC, Bandyopadhyay S, Meena VR, Prakash C, Datta KK (1995) An outbreak of viral hepatitis in Jodhpur city of Rajasthan. J Commun Dis 27:175–180PubMedGoogle Scholar
  29. 29.
    Sailaja B, Murhekar MV, Hutin YJ, Kuruva S, Murthy SP, Reddy KS, Rao GM, Gupte MD (2009) Outbreak of waterborne hepatitis E in Hyderabad, India 2005. Epidemiol Infect 137:234–240PubMedGoogle Scholar
  30. 30.
    Swain SK, Baral P, Hutin YJ, Rao TV, Murhekar M, Gupte MD (2010) A hepatitis E outbreak caused by a temporary interruption in a municipal water treatment system, Baripada, Orissa, India, 2004. Trans R Soc Trop Med Hyg 104:66–69PubMedGoogle Scholar
  31. 31.
    Risbud AR, Chadha MS, Kushwah SS, Arankalle VA, Rodrigues FM, Banerjee K (1992) Non-A, non-B hepatitis epidemic in Rewa district of Madhya Pradesh. JAPI 40:262–266PubMedGoogle Scholar
  32. 32.
    Chadha MS, Mehendale SM, Arankalle VA, Athley NK, Banerjee K (1991) Water supply schemes and enterically transmitted non-A, non-B hepatitis epidemics: an experience in Khadakwasla village of Pune district. Indian J Comm Med 16:153–158Google Scholar
  33. 33.
    Neogi DK, Bhattacharya N, De PN, Chakravarti T, Hati AK, Prakash C, Datta KK, Mukherjee KK (1995) An institutional outbreak of hepatitis E: reported first time from Calcutta city. J Commun Dis 27:229–233PubMedGoogle Scholar
  34. 34.
    Bora D, Jain DC, Gupta RS, Prakash C, Godhara NS, Datta KK (1996) An outbreak of non-A non-B viral hepatitis in rural areas of northern Rajasthan. J Commun Dis 28:70–72PubMedGoogle Scholar
  35. 35.
    Vivek R, Nihal L, Illiayaraja J, Reddy PK, Sarkar R, Eapen CE, Kang G (2010) Investigation of an epidemic of Hepatitis E in Nellore in south India. Trop Med Int Health 15:1333–1339PubMedGoogle Scholar
  36. 36.
    Chauhan NT, Prajapati P, Trivedi AV, Bhagyalaxmi A (2010) Epidemic investigation of the jaundice outbreak in girdharnagar, Ahmedabad, Gujarat, India, 2008. Indian J Community Med 35:294–297PubMedGoogle Scholar
  37. 37.
    Martolia HC, Hutin Y, Ramachandran V, Manickam P, Murhekar M, Gupte M (2009) An outbreak of hepatitis E tracked to a spring in the foothills of the Himalayas, India, 2005. Indian J Gastroenterol 28:99–101PubMedGoogle Scholar
  38. 38.
    Prinja S, Kumar S, Reddy GM, Ratho RK, Kumar R (2008) Investigation of viral hepatitis E outbreak in a town in Haryana. J Commun Dis 40:249–254PubMedGoogle Scholar
  39. 39.
    Bali S, Kar SS, Kumar S, Ratho RK, Dhiman RK, Kumar R (2008) Hepatitis E epidemic with bimodal peak in a town of north India. Indian J Public Health 52:189–193PubMedGoogle Scholar
  40. 40.
    Singh V, Singh V, Raje M, Nain CK, Singh K (1998) Routes of transmission in the hepatitis E epidemic of Saharanpur. Trop Gastroenterol 19:107–109PubMedGoogle Scholar
  41. 41.
    Arankalle VA, Chadha MS, Mehendale SM, Banerjee K (1988) Outbreak of enterically transmitted non-A non-B hepatitis among school children. Lancet 2:1199–1200PubMedGoogle Scholar
  42. 42.
    Arora NK, Panda SK, Nanda SK, Ansari IH, Joshi S, Dixit R, Bathla R (1999) Hepatitis E infection in children: study of an outbreak. J Gastroenterol Hepatol 14:572–577PubMedGoogle Scholar
  43. 43.
    John R, Abraham P, Kurien G, Chandy G, Sridharan G (1997) Sporadic hepatitis E in southern India. Trans R Soc Trop Med Hyg 91:392PubMedGoogle Scholar
  44. 44.
    Das K, Agarwal A, Andrew R, Frösner GG, Kar P (2000) Role of hepatitis E and other hepatotropic virus in aetiology of sporadic acute viral hepatitis: a hospital based study from urban Delhi. Eur J Epidemiol 16:937–940PubMedGoogle Scholar
  45. 45.
    Kaur H, John M, Pawar G, Ninan J, Verma V (2003) Spectrum of acute viral hepatitis and its clinical outcome: a study from Ludhiana, Punjab. Indian J Med Sci 57:71–75PubMedGoogle Scholar
  46. 46.
    Radhakrishnan S, Raghuraman S, Abraham P, Kurian G, Chandy G, Sridharan G (2000) Prevalence of enterically transmitted hepatitis viruses in patients attending a tertiary: care hospital in south India. Indian J Pathol Microbiol 43:433–436PubMedGoogle Scholar
  47. 47.
    Jaiswal SP, Jain AK, Naik G, Soni N, Chitnis DS (2001) Viral hepatitis during pregnancy. Int J Gynaecol Obstet 72:103–108PubMedGoogle Scholar
  48. 48.
    Beniwal M, Kumar A, Kar P, Jilani N, Sharma JB (2003) Prevalence and severity of acute viral hepatitis and fulminant hepatitis during pregnancy: a prospective study from north India. Indian J Med Microbiol 21:184–185PubMedGoogle Scholar
  49. 49.
    Dahiya M, Kumar A, Kar P, Gupta RK, Kumar A (2005) Acute viral hepatitis in third trimester of pregnancy. Indian J Gastroenterol 24:128–129PubMedGoogle Scholar
  50. 50.
    Arankalle VA, Jha J, Favorov MO, Chaudhari A, Fields HA, Banerjee K (1995) Contribution of HEV and HCV in causing fulminant non-A, non-B hepatitis in western India. J Viral Hepat 2:189–193PubMedGoogle Scholar
  51. 51.
    Bhatia V, Singhal A, Panda SK, Acharya SK (2008) A 20-year single-center experience with acute liver failure during pregnancy: is the prognosis really worse? Hepatology 48:1577–1585PubMedGoogle Scholar
  52. 52.
    Khuroo MS, Kamili S (2003) Aetiology and prognostic factors in acute liver failure in India. J Viral Hepat 10:224–231PubMedGoogle Scholar
  53. 53.
    Kumar A, Beniwal M, Kar P, Sharma JB, Murthy NS (2004) Hepatitis E in pregnancy. Int J Gynaecol Obstet 85:240–244PubMedGoogle Scholar
  54. 54.
    Kumar A, Aggarwal R, Naik SR, Saraswat V, Ghoshal UC, Naik S (2004) Hepatitis E virus is responsible for decompensation of chronic liver disease in an endemic region. Indian J Gastroenterol 23:59–62PubMedGoogle Scholar
  55. 55.
    Monga R, Garg S, Tyagi P, Kumar N (2004) Superimposed acute hepatitis E infection in patients with chronic liver disease. Indian J Gastroenterol 23:50–52PubMedGoogle Scholar
  56. 56.
    Ramachandran J, Eapen CE, Kang G, Abraham P, Hubert DD, Kurian G, Hephzibah J, Mukhopadhya A, Chandy GM (2004) Hepatitis E superinfection produces severe decompensation in patients with chronic liver disease. J Gastroenterol Hepatol 19:134–138PubMedGoogle Scholar
  57. 57.
    Kumar Acharya S, Kumar Sharma P, Singh R, Kumar Mohanty S, Madan K, Kumar Jha J, Kumar Panda S (2007) Hepatitis E virus (HEV) infection in patients with cirrhosis is associated with rapid decompensation and death. J Hepatol 46:387–394PubMedGoogle Scholar
  58. 58.
    Aggarwal R (2008) Hepatitis E: does it cause chronic hepatitis? Hepatology 48:1328–1330PubMedGoogle Scholar
  59. 59.
    Radha Krishna Y, Saraswat VA, Das K, Himanshu G, Yachha SK, Aggarwal R, Choudhuri G (2009) Clinical features and predictors of outcome in acute hepatitis A and hepatitis E virus hepatitis on cirrhosis. Liver Int 29:392–398PubMedGoogle Scholar
  60. 60.
    Kumar M, Sharma BC, Sarin SK (2008) Hepatitis E virus as an etiology of acute exacerbation of previously unrecognized asymptomatic patients with hepatitis B virus-related chronic liver disease. J Gastroenterol Hepatol 23:883–887PubMedGoogle Scholar
  61. 61.
    Arankalle VA, Tsarev SA, Chadha MS, Alling DW, Emerson SU, Banerjee K, Purcell RH (1995) Age-specific prevalence of antibodies to hepatitis A and E viruses in Pune, India, 1982 and 1992. J Infect Dis 171:447–450PubMedGoogle Scholar
  62. 62.
    Arankalle VA, Chadha MS, Chitambar SD, Walimbe AM, Chobe LP, Gandhe SS (2001) Changing epidemiology of hepatitis A and hepatitis E in urban and rural India (1982–98). J Viral Hepat 8:293–303PubMedGoogle Scholar
  63. 63.
    Daniel HD, Warier A, Abraham P, Sridharan G (2004) Age-wise exposure rates to hepatitis e virus in a southern Indian patient population without liver disease. Am J Trop Med Hyg 71:675–678PubMedGoogle Scholar
  64. 64.
    Vivek R, Chandy GM, Brown DW, Kang G (2010) Seroprevalence of IgG antibodies to hepatitis E in urban and rural southern India. Trans R Soc Trop Med Hyg 104:307–308PubMedGoogle Scholar
  65. 65.
    Murhekar MV, Sehgal SC, Murhekar KM, Padbhidri SP, Chitambar SD, Arankalle VA (2002) Changing scenario of hepatitis A virus and hepatitis E virus exposure among the primitive tribes of Andaman and Nicobar Islands, India over the 10-year period 1989–99. J Viral Hepat 9:315–321PubMedGoogle Scholar
  66. 66.
    Arankalle VA, Chadha MS, Dama BM, Tsarev SA, Purcell RH, Banerjee K (1998) Role of immune serum globulins in pregnant women during an epidemic of hepatitis E. J Viral Hepat 5:199–204PubMedGoogle Scholar
  67. 67.
    Arankalle VA, Chadha MS, Mehendale SM, Tungatkar SP (2000) Epidemic hepatitis E: serological evidence for lack of intrafamilial spread. Indian J Gastroenterol 19:24–28PubMedGoogle Scholar
  68. 68.
    Verma V, Arankalle VA (2010) Hepatitis E virus-based evaluation of a virion concentration method and detection of enteric viruses in environmental samples by multiplex nested RT-PCR. J Appl Microbiol 108:1630–1641PubMedGoogle Scholar
  69. 69.
    Jothikumar N, Aparna K, Kamatchiammal S, Paulmurugan R, Saravanadevi S, Khanna P (1993) Detection of hepatitis E virus in raw and treated wastewater with the polymerase chain reaction. Appl Environ Microbiol 59:2558–2562PubMedGoogle Scholar
  70. 70.
    Jothikumar N, Khanna P, Paulmurugan R, Kamatchiammal S, Padmanabhan P (1995) A simple device for the concentration and detection of enterovirus, hepatitis E virus and rotavirus from water samples by reverse transcription-polymerase chain reaction. J Virol Methods 55:401–415PubMedGoogle Scholar
  71. 71.
    Vaidya SR, Chitambar SD, Arankalle VA (2002) Polymerase chain reaction-based prevalence of hepatitis A, hepatitis E and TT viruses in sewage from an endemic area. J Hepatol 37:131–136PubMedGoogle Scholar
  72. 72.
    Hazam RK, Singla R, Kishore J, Singh S, Gupta RK, Kar P (2010) Surveillance of hepatitis E virus in sewage and drinking water in a resettlement colony of Delhi: what has been the experience? Arch Virol 155:1227–1233PubMedGoogle Scholar
  73. 73.
    Vaidya SR, Tilekar BN, Walimbe AM, Arankalle VA (2003) Increased risk of hepatitis E in sewage workers from India. J Occup Environ Med 45:1167–1170PubMedGoogle Scholar
  74. 74.
    Verma V, Arankalle VA (2009) Virological evaluation of domestic water purification devices commonly used in India emphasizes inadequate quality and need for virological standards. Trop Med Int Health 14:885–891PubMedGoogle Scholar
  75. 75.
    Ippagunta SK, Naik S, Sharma B, Aggarwal R (2007) Presence of hepatitis E virus in sewage in northern India: frequency and seasonal pattern. J Med Virol 79:1827–1831PubMedGoogle Scholar
  76. 76.
    Aggarwal R, Naik SR (1994) Hepatitis E: intrafamilial transmission versus waterborne spread. J Hepatol 21:718–723PubMedGoogle Scholar
  77. 77.
    Somani SK, Aggarwal R, Naik SR, Srivastava S, Naik S (2003) A serological study of intrafamilial spread from patients with sporadic hepatitis E virus infection. J Viral Hepat 10:446–449PubMedGoogle Scholar
  78. 78.
    Khuroo MS, Kamili S, Khuroo MS (2009) Clinical course and duration of viremia in vertically transmitted hepatitis E virus (HEV) infection in babies born to HEV-infected mothers. J Viral Hepat 16:519–523PubMedGoogle Scholar
  79. 79.
    Arankalle VA, Chobe LP (1999) Hepatitis E virus: can it be transmitted parenterally? J Viral Hepat 6:161–164PubMedGoogle Scholar
  80. 80.
    Arankalle VA, Chobe LP (2000) Retrospective analysis of blood transfusion recipients: evidence for post-transfusion hepatitis E. Vox Sang 79:72–74PubMedGoogle Scholar
  81. 81.
    Karetnyi YV, Dzhumalieva DI, Usmanov RK, Titova IP, Litvak YI, Balayan MS (1993) Possible involvement of rodents in the spread of viral hepatitis E. J Microbiol Epidemiol Immunol (in Russian) 4:52–56Google Scholar
  82. 82.
    Johne R, Plenge-Bönig A, Hess M, Ulrich RG, Reetz J, Schielke A (2010) Detection of a novel hepatitis E-like virus in faeces of wild rats using a nested broad-spectrum RT-PCR. J Gen Virol 91:750–758PubMedGoogle Scholar
  83. 83.
    Arankalle VA, Goverdhan MK, Banerjee K (1994) Antibodies against hepatitis E virus in old world monkeys. J Viral Hepat 1:125–129PubMedGoogle Scholar
  84. 84.
    Arankalle VA, Joshi MV, Kulkarni AM, Gandhe SS, Chobe LP, Rautmare SS, Mishra AC, Padbidri VS (2001) Prevalence of anti-hepatitis E virus antibodies in different Indian animal species. J Viral Hepat 8:223–227PubMedGoogle Scholar
  85. 85.
    Meng XJ, Purcell RH, Halbur PG, Lehman JR, Webb DM, Tsareva TS, Haynes JS, Thacker BJ, Emerson SU (1997) A novel virus in swine is closely related to the human hepatitis E virus. PNAS USA 94:9860–9865Google Scholar
  86. 86.
    Kwo PY, Schlauder GG, Carpenter HA, Carpenter HA, Murphy PJ, Rosenblatt JE et al (1997) Acute hepatitis E by a new isolate acquired in the United States. Mayo Clinic Proc 72:1133–1136Google Scholar
  87. 87.
    Schlauder GG, Dawson GJ, Erker JC, Kow PY, Knigge MP, Smalley DL et al (1998) The sequence and phylogenetic analysis of a novel hepatitis E virus isolated from a patient with acute hepatitis reported in the United States. J Gen Virol 79:447–456PubMedGoogle Scholar
  88. 88.
    Meng XJ, Halbur PG, Shapiro MS, Govindrajan S, Bruna JD, Mushawar IK et al (1998) Genetic and experimental evidence for cross-species infection by swine hepatitis E virus. J Virol 72:9714–9721PubMedGoogle Scholar
  89. 89.
    Arankalle VA, Chobe LP, Joshi MV, Chadha MS, Kundu B, Walimbe AM (2002) Human and swine hepatitis E viruses from western India belong to different genotypes. J Hepatol 36:417–425PubMedGoogle Scholar
  90. 90.
    Arankalle VA, Chobe LP, Walimbe AM, Yergolkar PN, Jacob GP (2003) Swine HEV infection in south India and phylogenetic analysis (1985–1999). J Med Virol 69:391–396PubMedGoogle Scholar
  91. 91.
    Shukla P, Chauhan UK, Naik S, Anderson D, Aggarwal R (2007) Hepatitis E virus infection among animals in northern India: an unlikely source of human disease. J Viral Hepat 14:310–317PubMedGoogle Scholar
  92. 92.
    Begum N, Polipalli SK, Husain SA, Kar P (2010) Molecular analysis of swine hepatitis E virus from north India. Indian J Med Res 132:504–508PubMedGoogle Scholar
  93. 93.
    Chobe LP, Lole KS, Arankalle VA (2006) Full genome sequence and analysis of Indian swine hepatitis E virus isolate of genotype 4. Vet Microbiol 114:240–251PubMedGoogle Scholar
  94. 94.
    Arankalle VA, Chobe LP, Chadha MS (2006) Type-IV Indian swine HEV infects rhesus monkeys. J Viral Hepat 13:742–745PubMedGoogle Scholar
  95. 95.
    Arankalle VA, Lole KS, Deshmukh TM, Chobe LP, Gandhe SS (2007) Evaluation of human (genotype 1) and swine (genotype 4)-ORF2-based ELISAs for anti-HEV IgM and IgG detection in an endemic country and search for type 4 human HEV infections. J Viral Hepat 14:435–445PubMedGoogle Scholar
  96. 96.
    Kulkarni MA, Arankalle VA (2008) The detection and characterization of hepatitis E virus in pig livers from retail markets of India. J Med Virol 80:1387–1390PubMedGoogle Scholar
  97. 97.
    Rolfe KJ, Curran MD, Mangrolia N, Gelson W, Alexander GJ, L’estrange M, Vivek R, Tedder R, Ijaz S (2010) First case of genotype 4 human hepatitis E virus infection acquired in India. J Clin Virol 48(1):58–61 Epub 2010 MarPubMedGoogle Scholar
  98. 98.
    Vivek R, Kang G (2011) Hepatitis E virus infections in Swine and Swine handlers in vellore, southern India. Am J Trop Med Hyg 84:647–649PubMedGoogle Scholar
  99. 99.
    Pujhari SK, Kumar S, Ratho RK, Chawla YK, Chakraborti A (2010) Phylogenetic analysis and subtyping of acute and fulminant strains of hepatitis E virus isolates of north India with reference to disease severity. Arch Virol 155:1483–1486PubMedGoogle Scholar
  100. 100.
    Panda SK Nanda SK, Zafrullah M, Ansari IH, Ozdener MH, Jameel S (1995) An Indian strain of Hepatitis E Virus: Cloning, sequence and expression of structural region and antibody responses in sera from individuals from an area of high level HEV endemicity. J Clin Microbiol 33:2653–2659Google Scholar
  101. 101.
    Husain MM, Srivastava R, Akondy R, Aggarwal R, Jameel S, Naik S (2010) Evidence of hepatitis E virus exposure among seronegative healthy residents of an endemic area. Intervirology 54:139–143PubMedGoogle Scholar
  102. 102.
    Jilani N, Das BC, Husain SA, Baweja UK, Chattopadhya D, Gupta RK, Sardana S, Kar P (2007) Hepatitis E virus infection and fulminant hepatic failure during pregnancy. J Gastroenterol Hepatol 22:676–682PubMedGoogle Scholar
  103. 103.
    Kar P, Jilani N, Husain SA, Pasha ST, Anand R, Rai A, Das BC (2008) Does hepatitis E viral load and genotypes influence the final outcome of acute liver failure during pregnancy? Am J Gastroenterol 103:2495–2501PubMedGoogle Scholar
  104. 104.
    Bose PD, Das BC, Kumar A, Gondal R, Kumar D, Kar P (2010) High viral load and deregulation of the progesterone receptor signaling pathway: association with Hepatitis E-related poor pregnancy outcome. J Hepatol 1:4444–4447Google Scholar
  105. 105.
    Begum N, Polipalli SK, Husain SA, Kumar A, Kar P (2010) Duration of hepatitis E viremia in pregnancy. Int J Gynaecol Obstet 108:207–210PubMedGoogle Scholar
  106. 106.
    Banait VS, Sandur V, Parikh F, Murugesh M, Ranka P, Ramesh VS, Sasidharan M, Sattar A, Kamat S, Dalal A, Bhatia SJ (2007) Outcome of acute liver failure due to acute hepatitis E in pregnant women. Indian J Gastroenterol 26:6–10PubMedGoogle Scholar
  107. 107.
    Saravanabalaji S, Tripathy AS, Dhoot RR, Chadha MS, Kakrani AL, Arankalle VA (2009) Viral load, antibody titers and recombinant open reading frame 2 protein-induced TH1/TH2 cytokines and cellular immune responses in self-limiting and fulminant hepatitis E. Intervirology 52:78–85PubMedGoogle Scholar
  108. 108.
    Prabhu SB, Gupta P, Durgapal H, Rath S, Gupta SD, Acharya SK, Panda SK (2010) Study of cellular immune response against Hepatitis E Virus (HEV). J Viral Hepat 18(8):587–594PubMedGoogle Scholar
  109. 109.
    Srivastava R, Aggarwal R, Sachdeva S, Alam MI, Jameel S, Naik S (2011) Adaptive immune responses during acute uncomplicated and fulminant hepatitis E. J Gastroenterol Hepatol 26:306–311PubMedGoogle Scholar
  110. 110.
    Taneja S, Ahmad I, Sen S, Kumar S, Arora R, Gupta VK, Aggarwal R, Narayanasamy K, Reddy VS, Jameel S (2011) Plasma peptidome profiling of acute hepatitis E patients by MALDI-TOF/TOF. Proteome Sci 9:5Google Scholar
  111. 111.
    Taneja S, Sen S, Gupta VK, Aggarwal R, Jameel S (2009) Plasma and urine biomarkers in acute viral hepatitis E. Proteome Sci 27:7–39Google Scholar
  112. 112.
    Tuteja R, Li TC, Takeda N, Jameel S (2000) Augmentation of immune responses to hepatitis E virus ORF2 DNA vaccination by codelivery of cytokine genes. Viral Immunol 13:169–178PubMedGoogle Scholar
  113. 113.
    Deshmukh TM, Lole KS, Tripathy AS, Arankalle VA (2007) Immunogenicity of candidate hepatitis E virus DNA vaccine expressing complete and truncated ORF2 in mice. Vaccine 25:4350–4360PubMedGoogle Scholar
  114. 114.
    Arankalle VA, Lole KS, Deshmukh TM, Srivastava S, Shaligram US (2009) Challenge studies in Rhesus monkeys immunized with candidate hepatitis E vaccines: DNA, DNA-prime-protein-boost and DNA-protein encapsulated in liposomes. Vaccine 27:1032–1039PubMedGoogle Scholar
  115. 115.
    Shrestha MP, Scott RM, Joshi DM, Mammen MP Jr, Thapa GB, Thapa N, Myint KS, Fourneau M, Kuschner RA, Shrestha SK, David MP, Seriwatana J, Vaughn DW, Safary A, Endy TP, Innis BL (2007) Safety and efficacy of a recombinant hepatitis E vaccine. N Engl J Med 356:895–903PubMedGoogle Scholar
  116. 116.
    Zhu FC, Zhang J, Zhang XF, Zhou C, Wang ZZ, Huang SJ, Wang H, Yang CL, Jiang HM, Cai JP, Wang YJ, Ai X, Hu YM, Tang Q, Yao X, Yan Q, Xian YL, Wu T, Li YM, Miao J, Ng MH, Shih JW, Xia NS (2010) Efficacy and safety of a recombinant hepatitis E vaccine in healthy adults: a large-scale, randomised, double-blind placebo-controlled, phase 3 trial. Lancet 376:895–902PubMedGoogle Scholar
  117. 117.
    Shrivastava S, Lole KS, Tripathy AS, Shaligram US, Arankalle VA (2009) Development of candidate combination vaccine for hepatitis E and hepatitis B: a liposome encapsulation approach. Vaccine 27:6582–6588PubMedGoogle Scholar
  118. 118.
    Chadha MS, Walimbe AM, Arankalle VA (1999) Retrospective serological analysis of hepatitis E patients: a long-term follow-up study. J Viral Hepat 6:457–461PubMedGoogle Scholar
  119. 119.
    Rai RR, Nijhawan S, Mathur A, Sharma MP, Udawat HP, Singh N (2008) Seroepidemiology and role of polymerase chain reaction to detect viremia in an epidemic of hepatitis E in Western India. Trop Gastroenterol 29(4):202–206 Google Scholar
  120. 120.
    Panda SK, Ansari IH, Durgapal H, Agrawal S, Jameel S (2000) The in vitro-synthesized RNA from a cDNA clone of hepatitis E virus is infectious. J Virol 74:2430–2437PubMedGoogle Scholar
  121. 121.
    Varma SP, Kumar A, Kapur N, Durgapal H, Acharya SK, Panda SK (2011) Hepatitis E virus replication involves alternating negative- and positive-sense RNA synthesis. J Gen Virol 92:572–581PubMedGoogle Scholar
  122. 122.
    Kumar A, Panda SK, Durgapal H, Acharya SK, Rehman S, Kar UK (2010) Inhibition of Hepatitis E virus replication using short hairpin RNA (shRNA). Antiviral Res 85(3):541–550Google Scholar
  123. 123.
    Sehgal D, Thomas S, Chakraborty M, Jameel S (2006) Expression and processing of the Hepatitis E virus ORF1 nonstructural polyprotein. Virol J 3:38PubMedGoogle Scholar
  124. 124.
    Rehman S, Kapur N, Durgapal H, Panda SK (2008) Subcellular localization of hepatitis E virus (HEV) replicase. Virology 370:77–92PubMedGoogle Scholar
  125. 125.
    Karpe YA, Lole KS (2010) NTPase and 5′ to 3′ RNA duplex-unwinding activities of the hepatitis E virus helicase domain. J Virol 84:3595–3602PubMedGoogle Scholar
  126. 126.
    Karpe YA, Lole KS (2010) RNA 5′-triphosphatase activity of the hepatitis E virus helicase domain. J Virol 84:9637–9641PubMedGoogle Scholar
  127. 127.
    Surjit M, Jameel S, Lal SK (2007) Cytoplasmic localization of the ORF2 protein of hepatitis E virus is dependent on its ability to undergo retrotranslocation from the endoplasmic reticulum. J Virol 81:3339–3345PubMedGoogle Scholar
  128. 128.
    Kalia M, Chandra V, Rahman SA, Sehgal D, Jameel S (2009) Heparan sulfate proteoglycans are required for cellular binding of the hepatitis E virus ORF2 capsid protein and for viral infection. J Virol 83:12714–12724PubMedGoogle Scholar
  129. 129.
    Zafrullah M, Ozdener MH, Panda SK, Jameel S (1997) The ORF3 protein of hepatitis E virus is a phosphoprotein that associates with the cytoskeleton. J Virol 71:9045–9053PubMedGoogle Scholar
  130. 130.
    Korkaya H, Jameel S, Gupta D, Tyagi S, Kumar R, Zafrullah M, Mazumdar M, Lal SK, Xiaofang L, Sehgal D, Das SR, Sahal D (2001) The ORF3 protein of hepatitis E virus binds to Src homology 3 domains and activates MAPK. J Biol Chem 276:42389–42400PubMedGoogle Scholar
  131. 131.
    Tyagi S, Korkaya H, Zafrullah M, Jameel S, Lal SK (2002) The phosphorylated form of the ORF3 protein of hepatitis E virus interacts with its non-glycosylated form of the major capsid protein, ORF2. J Biol Chem 277:22759–22767PubMedGoogle Scholar
  132. 132.
    Kar-Roy A, Korkaya H, Oberoi R, Lal SK, Jameel S (2004) The hepatitis E virus open reading frame 3 protein activates ERK through binding and inhibition of the MAPK phosphatase. J Biol Chem 279:28345–28357PubMedGoogle Scholar
  133. 133.
    Moin SM, Panteva M, Jameel S (2007) The hepatitis E virus Orf3 protein protects cells from mitochondrial depolarization and death. J Biol Chem 282:21124–21133PubMedGoogle Scholar
  134. 134.
    Chandra V, Kalia M, Hajela K, Jameel S (2010) The ORF3 protein of hepatitis E virus delays degradation of activated growth factor receptors by interacting with CIN85 and blocking formation of the Cbl-CIN85 complex. J Virol 84:3857–3867PubMedGoogle Scholar

Copyright information

© The National Academy of Sciences, India 2012

Authors and Affiliations

  1. 1.National Institute of VirologyPuneIndia

Personalised recommendations