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Published in: BMC Infectious Diseases 1/2013

Open Access 01-12-2013 | Research article

Infection by Brazilian and Dutch swine hepatitis E virus strains induces haematological changes in Macaca fascicularis

Authors: Lilian G de Carvalho, Renato S Marchevsky, Debora RL dos Santos, Jaqueline M de Oliveira, Vanessa S de Paula, Leilane M Lopes, Wilhelmus HM Van der Poel, Jorge E González, Maria S Munné, Julio Moran, Ana Carolina R A Cajaraville, Marcelo Pelajo-Machado, Oswaldo G Cruz, Marcelo A Pinto

Published in: BMC Infectious Diseases | Issue 1/2013

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Abstract

Background

Hepatitis E virus (HEV) has been described as an emerging pathogen in Brazil and seems to be widely disseminated among swine herds. An autochthonous human case of acute hepatitis E was recently reported. To obtain a better understanding of the phenotypic profiles of both human and swine HEV strains, a experimental study was conducted using the animal model, Macaca fascicularis.

Methods

Six cynomolgus monkeys (Macaca fascicularis) were inoculated intravenously with swine HEV genotype 3 that was isolated from naturally and experimentally infected pigs in Brazil and the Netherlands. Two other monkeys were inoculated with HEV genotype 3 that was recovered from Brazilian and Argentinean patients with locally acquired acute and fulminant hepatitis E. The haematological, biochemical, and virological parameters of all animals were monitored for 67 days.

Results

Subclinical hepatitis was observed in all monkeys after inoculation with HEV genotype 3 that was recovered from the infected swine and human patients. HEV RNA was detected in the serum and/or faeces of 6 out of the 8 cynomolgus monkeys between 5 and 53 days after inoculation. The mild inflammation of liver tissues and elevations of discrete liver enzymes were observed. Seroconversions to anti-HEV IgM and/or IgG were detected in 7 animals. Reactivities to anti-HEV IgA were also detected in the salivary samples of 3 animals. Interestingly, all of the infected monkeys showed severe lymphopenia and a trend toward monocytosis, which coincided with elevations in alanine aminotransferase and antibody titres.

Conclusions

The ability of HEV to cross the species barrier was confirmed for both the swine (Brazilian and Dutch) and human (Argentinean) strains, thus reinforcing the zoonotic risk of hepatitis E in South America. Cynomolgus monkeys that were infected with HEV genotype 3 developed subclinical hepatitis that was associated with haematological changes. Haematological approaches should be considered in future studies of HEV infection.
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Literature
1.
go back to reference Mushahwar IK: Hepatitis E virus: molecular virology, clinical features, diagnosis, transmission, epidemiology, and prevention. J Med Virol. 2008, 80: 646-658. 10.1002/jmv.21116.CrossRefPubMed Mushahwar IK: Hepatitis E virus: molecular virology, clinical features, diagnosis, transmission, epidemiology, and prevention. J Med Virol. 2008, 80: 646-658. 10.1002/jmv.21116.CrossRefPubMed
2.
go back to reference Kumar S, Subhadra S, Singh B, Panda BK: Hepatitis E virus: the current scenario. Int J Infect Dis. 2013, 17: e228-e233. 10.1016/j.ijid.2012.11.026.CrossRefPubMed Kumar S, Subhadra S, Singh B, Panda BK: Hepatitis E virus: the current scenario. Int J Infect Dis. 2013, 17: e228-e233. 10.1016/j.ijid.2012.11.026.CrossRefPubMed
3.
go back to reference Echevarria JM, Gonzalez JE, Lewis-Ximenez LL, Dos Santos DR, Munne MS, Pinto MA, Pujol FH, Rodriguez-Lay LA: Hepatitis E virus infection in Latin America: a review. J Med Virol. 2013, 85: 1037-1045. 10.1002/jmv.23526.CrossRefPubMed Echevarria JM, Gonzalez JE, Lewis-Ximenez LL, Dos Santos DR, Munne MS, Pinto MA, Pujol FH, Rodriguez-Lay LA: Hepatitis E virus infection in Latin America: a review. J Med Virol. 2013, 85: 1037-1045. 10.1002/jmv.23526.CrossRefPubMed
4.
go back to reference Silva SM, Oliveira JM, Vitral CL, Vieira Kde A, Pinto MA, Souto FJ: Prevalence of hepatitis E virus antibodies in individuals exposed to swine in Mato Grosso, Brazil. Mem Inst Oswaldo Cruz. 2012, 107: 338-341. 10.1590/S0074-02762012000300007.CrossRefPubMed Silva SM, Oliveira JM, Vitral CL, Vieira Kde A, Pinto MA, Souto FJ: Prevalence of hepatitis E virus antibodies in individuals exposed to swine in Mato Grosso, Brazil. Mem Inst Oswaldo Cruz. 2012, 107: 338-341. 10.1590/S0074-02762012000300007.CrossRefPubMed
5.
go back to reference Vitral CL, Pinto MA, Lewis-Ximenez LL, Khudyakov YE, dos Santos DR, Gaspar AM: Serological evidence of hepatitis E virus infection in different animal species from the Southeast of Brazil. Mem Inst Oswaldo Cruz. 2005, 100: 117-122. 10.1590/S0074-02762005000200003.CrossRefPubMed Vitral CL, Pinto MA, Lewis-Ximenez LL, Khudyakov YE, dos Santos DR, Gaspar AM: Serological evidence of hepatitis E virus infection in different animal species from the Southeast of Brazil. Mem Inst Oswaldo Cruz. 2005, 100: 117-122. 10.1590/S0074-02762005000200003.CrossRefPubMed
6.
go back to reference Bortoliero AL, Bonametti AM, Morimoto HK, Matsuo T, Reiche EM: Seroprevalence for hepatitis E virus (HEV) infection among volunteer blood donors of the regional blood bank of Londrina, State of Parana, Brazil. Rev Inst Med Trop Sao Paulo. 2006, 48: 87-92. 10.1590/S0036-46652006000200006.CrossRefPubMed Bortoliero AL, Bonametti AM, Morimoto HK, Matsuo T, Reiche EM: Seroprevalence for hepatitis E virus (HEV) infection among volunteer blood donors of the regional blood bank of Londrina, State of Parana, Brazil. Rev Inst Med Trop Sao Paulo. 2006, 48: 87-92. 10.1590/S0036-46652006000200006.CrossRefPubMed
7.
go back to reference Santos DC, Souto FJ, Santos DR, Vitral CL, Gaspar AM: Seroepidemiological markers of enterically transmitted viral hepatitis A and E in individuals living in a community located in the North Area of Rio de Janeiro, RJ, Brazil. Mem Inst Oswaldo Cruz. 2002, 97: 637-640. 10.1590/S0074-02762002000500007.CrossRefPubMed Santos DC, Souto FJ, Santos DR, Vitral CL, Gaspar AM: Seroepidemiological markers of enterically transmitted viral hepatitis A and E in individuals living in a community located in the North Area of Rio de Janeiro, RJ, Brazil. Mem Inst Oswaldo Cruz. 2002, 97: 637-640. 10.1590/S0074-02762002000500007.CrossRefPubMed
8.
go back to reference dos Santos DR, de Paula VS, de Oliveira JM, Marchevsky RS, Pinto MA: Hepatitis E virus in swine and effluent samples from slaughterhouses in Brazil. Vet Microbiol. 2011, 149: 236-241. 10.1016/j.vetmic.2010.10.024.CrossRefPubMed dos Santos DR, de Paula VS, de Oliveira JM, Marchevsky RS, Pinto MA: Hepatitis E virus in swine and effluent samples from slaughterhouses in Brazil. Vet Microbiol. 2011, 149: 236-241. 10.1016/j.vetmic.2010.10.024.CrossRefPubMed
9.
go back to reference de Souza AJ, Gomes-Gouvea MS, Soares Mdo C, Pinho JR, Malheiros AP, Carneiro LA, Dos-Santos DR, Pereira WL: HEV infection in swine from Eastern Brazilian Amazon: evidence of co-infection by different subtypes. Comp Immunol Microbiol Infect Dis. 2012, 35: 477-485. 10.1016/j.cimid.2012.04.004.CrossRefPubMed de Souza AJ, Gomes-Gouvea MS, Soares Mdo C, Pinho JR, Malheiros AP, Carneiro LA, Dos-Santos DR, Pereira WL: HEV infection in swine from Eastern Brazilian Amazon: evidence of co-infection by different subtypes. Comp Immunol Microbiol Infect Dis. 2012, 35: 477-485. 10.1016/j.cimid.2012.04.004.CrossRefPubMed
10.
go back to reference Gardinali NR, Barry AF, da Silva PF, de Souza C, Alfieri AF, Alfieri AA: Molecular detection and characterization of hepatitis E virus in naturally infected pigs from Brazilian herds. Res Vet Sci. 2012, 93: 1515-1519. 10.1016/j.rvsc.2012.06.003.CrossRefPubMed Gardinali NR, Barry AF, da Silva PF, de Souza C, Alfieri AF, Alfieri AA: Molecular detection and characterization of hepatitis E virus in naturally infected pigs from Brazilian herds. Res Vet Sci. 2012, 93: 1515-1519. 10.1016/j.rvsc.2012.06.003.CrossRefPubMed
11.
go back to reference Bradley DW, Krawczynski K, Cook EH, McCaustland KA, Humphrey CD, Spelbring JE, Myint H, Maynard JE: Enterically transmitted non-A, non-B hepatitis: serial passage of disease in cynomolgus macaques and tamarins and recovery of disease-associated 27- to 34-nm viruslike particles. Proc Natl Acad Sci U S A. 1987, 84: 6277-6281. 10.1073/pnas.84.17.6277.CrossRefPubMedPubMedCentral Bradley DW, Krawczynski K, Cook EH, McCaustland KA, Humphrey CD, Spelbring JE, Myint H, Maynard JE: Enterically transmitted non-A, non-B hepatitis: serial passage of disease in cynomolgus macaques and tamarins and recovery of disease-associated 27- to 34-nm viruslike particles. Proc Natl Acad Sci U S A. 1987, 84: 6277-6281. 10.1073/pnas.84.17.6277.CrossRefPubMedPubMedCentral
12.
go back to reference Gupta H, Joshi YK, Varma A, Shenoy S, Sriramchari S, Iyenger B, Tandon BN: Transmission of enteric non-A, non-B hepatitis virus in Macaca mulatta monkeys by intraportal route: subsequent passages of HEV virus. J Gastroenterol Hepatol. 1990, 5: 608-615. 10.1111/j.1440-1746.1990.tb01114.x.CrossRefPubMed Gupta H, Joshi YK, Varma A, Shenoy S, Sriramchari S, Iyenger B, Tandon BN: Transmission of enteric non-A, non-B hepatitis virus in Macaca mulatta monkeys by intraportal route: subsequent passages of HEV virus. J Gastroenterol Hepatol. 1990, 5: 608-615. 10.1111/j.1440-1746.1990.tb01114.x.CrossRefPubMed
13.
go back to reference Longer CF, Denny SL, Caudill JD, Miele TA, Asher LV, Myint KS, Huang CC, Engler WF, LeDuc JW, Binn LN, Ticehurst JR: Experimental hepatitis E: pathogenesis in cynomolgus macaques (Macaca fascicularis). J Infect Dis. 1993, 168: 602-609. 10.1093/infdis/168.3.602.CrossRefPubMed Longer CF, Denny SL, Caudill JD, Miele TA, Asher LV, Myint KS, Huang CC, Engler WF, LeDuc JW, Binn LN, Ticehurst JR: Experimental hepatitis E: pathogenesis in cynomolgus macaques (Macaca fascicularis). J Infect Dis. 1993, 168: 602-609. 10.1093/infdis/168.3.602.CrossRefPubMed
14.
go back to reference Tsarev SA, Emerson SU, Tsareva TS, Yarbough PO, Lewis M, Govindarajan S, Reyes GR, Shapiro M, Purcell RH: Variation in course of hepatitis E in experimentally infected cynomolgus monkeys. J Infect Dis. 1993, 167: 1302-1306. 10.1093/infdis/167.6.1302.CrossRefPubMed Tsarev SA, Emerson SU, Tsareva TS, Yarbough PO, Lewis M, Govindarajan S, Reyes GR, Shapiro M, Purcell RH: Variation in course of hepatitis E in experimentally infected cynomolgus monkeys. J Infect Dis. 1993, 167: 1302-1306. 10.1093/infdis/167.6.1302.CrossRefPubMed
15.
go back to reference McCaustland KA, Krawczynski K, Ebert JW, Balayan MS, Andjaparidze AG, Spelbring JE, Cook EH, Humphrey C, Yarbough PO, Favorov MO, Carson D, Bradley DW, Robertson BH: Hepatitis E virus infection in chimpanzees: a retrospective analysis. Arch Virol. 2000, 145: 1909-1918. 10.1007/s007050070065.CrossRefPubMed McCaustland KA, Krawczynski K, Ebert JW, Balayan MS, Andjaparidze AG, Spelbring JE, Cook EH, Humphrey C, Yarbough PO, Favorov MO, Carson D, Bradley DW, Robertson BH: Hepatitis E virus infection in chimpanzees: a retrospective analysis. Arch Virol. 2000, 145: 1909-1918. 10.1007/s007050070065.CrossRefPubMed
16.
go back to reference Ji Y, Zhu Y, Liang J, Wei X, Yang X, Wang L, Li L, Chang Y, Tang R, Zhuang H: Swine hepatitis E virus in rural southern China: genetic characterization and experimental infection in rhesus monkeys (Macaca mulatta). J Gastroenterol. 2008, 43: 565-570. 10.1007/s00535-008-2196-3.CrossRefPubMed Ji Y, Zhu Y, Liang J, Wei X, Yang X, Wang L, Li L, Chang Y, Tang R, Zhuang H: Swine hepatitis E virus in rural southern China: genetic characterization and experimental infection in rhesus monkeys (Macaca mulatta). J Gastroenterol. 2008, 43: 565-570. 10.1007/s00535-008-2196-3.CrossRefPubMed
17.
go back to reference Pillot J, Turkoglu S, Dubreuil P, Cosson A, Lemaigre G, Meng J, Lazizi Y: Cross-reactive immunity against different strains of the hepatitis E virus transferable by simian and human sera. C R Acad Sci III. 1995, 318: 1059-1064.PubMed Pillot J, Turkoglu S, Dubreuil P, Cosson A, Lemaigre G, Meng J, Lazizi Y: Cross-reactive immunity against different strains of the hepatitis E virus transferable by simian and human sera. C R Acad Sci III. 1995, 318: 1059-1064.PubMed
18.
go back to reference Meng J, Pillot J, Dai X, Fields HA, Khudyakov YE: Neutralization of different geographic strains of the hepatitis E virus with anti-hepatitis E virus-positive serum samples obtained from different sources. Virology. 1998, 249: 316-324. 10.1006/viro.1998.9346.CrossRefPubMed Meng J, Pillot J, Dai X, Fields HA, Khudyakov YE: Neutralization of different geographic strains of the hepatitis E virus with anti-hepatitis E virus-positive serum samples obtained from different sources. Virology. 1998, 249: 316-324. 10.1006/viro.1998.9346.CrossRefPubMed
19.
go back to reference Sanford BJ, Dryman BA, Huang YW, Feagins AR, Leroith T, Meng XJ: Prior infection of pigs with a genotype 3 swine hepatitis E virus (HEV) protects against subsequent challenges with homologous and heterologous genotypes 3 and 4 human HEV. Virus Res. 2011, 159: 17-22. 10.1016/j.virusres.2011.04.010.CrossRefPubMedPubMedCentral Sanford BJ, Dryman BA, Huang YW, Feagins AR, Leroith T, Meng XJ: Prior infection of pigs with a genotype 3 swine hepatitis E virus (HEV) protects against subsequent challenges with homologous and heterologous genotypes 3 and 4 human HEV. Virus Res. 2011, 159: 17-22. 10.1016/j.virusres.2011.04.010.CrossRefPubMedPubMedCentral
20.
go back to reference Bouwknegt M, Lodder-Verschoor F, van der Poel WH, Rutjes SA, de Roda Husman AM: Hepatitis E virus RNA in commercial porcine livers in The Netherlands. J Food Prot. 2007, 70: 2889-2895.PubMed Bouwknegt M, Lodder-Verschoor F, van der Poel WH, Rutjes SA, de Roda Husman AM: Hepatitis E virus RNA in commercial porcine livers in The Netherlands. J Food Prot. 2007, 70: 2889-2895.PubMed
21.
go back to reference Meng XJ, Halbur PG, Shapiro MS, Govindarajan S, Bruna JD, Mushahwar IK, Purcell RH, Emerson SU: Genetic and experimental evidence for cross-species infection by swine hepatitis E virus. J Virol. 1998, 72: 9714-9721.PubMedPubMedCentral Meng XJ, Halbur PG, Shapiro MS, Govindarajan S, Bruna JD, Mushahwar IK, Purcell RH, Emerson SU: Genetic and experimental evidence for cross-species infection by swine hepatitis E virus. J Virol. 1998, 72: 9714-9721.PubMedPubMedCentral
22.
go back to reference Aggarwal R, Kamili S, Spelbring J, Krawczynski K: Experimental studies on subclinical hepatitis E virus infection in cynomolgus macaques. J Infect Dis. 2001, 184: 1380-1385. 10.1086/324376.CrossRefPubMed Aggarwal R, Kamili S, Spelbring J, Krawczynski K: Experimental studies on subclinical hepatitis E virus infection in cynomolgus macaques. J Infect Dis. 2001, 184: 1380-1385. 10.1086/324376.CrossRefPubMed
23.
go back to reference Bouwknegt M, Frankena K, Rutjes SA, Wellenberg GJ, de Roda Husman AM, van der Poel WH, de Jong MC: Estimation of hepatitis E virus transmission among pigs due to contact-exposure. Vet Res. 2008, 39: 40-10.1051/vetres:2008017.CrossRefPubMed Bouwknegt M, Frankena K, Rutjes SA, Wellenberg GJ, de Roda Husman AM, van der Poel WH, de Jong MC: Estimation of hepatitis E virus transmission among pigs due to contact-exposure. Vet Res. 2008, 39: 40-10.1051/vetres:2008017.CrossRefPubMed
24.
go back to reference Agrawal S, Gupta D, Panda SK: The 3′ end of hepatitis E virus (HEV) genome binds specifically to the viral RNA-dependent RNA polymerase (RdRp). Virology. 2001, 282: 87-101. 10.1006/viro.2000.0819.CrossRefPubMed Agrawal S, Gupta D, Panda SK: The 3′ end of hepatitis E virus (HEV) genome binds specifically to the viral RNA-dependent RNA polymerase (RdRp). Virology. 2001, 282: 87-101. 10.1006/viro.2000.0819.CrossRefPubMed
25.
go back to reference Dalton HR, Hunter JG, Bendall RP: Hepatitis e. Curr Opin Infect Dis. 2013, 26: 471-478.PubMed Dalton HR, Hunter JG, Bendall RP: Hepatitis e. Curr Opin Infect Dis. 2013, 26: 471-478.PubMed
26.
go back to reference Lopes Dos Santos DR, Lewis-Ximenez LL, da Silva MF, de Sousa PS, Gaspar AM, Pinto MA: First report of a human autochthonous hepatitis E virus infection in Brazil. J Clin Virol. 2010, 47: 276-279. 10.1016/j.jcv.2009.12.021.CrossRefPubMed Lopes Dos Santos DR, Lewis-Ximenez LL, da Silva MF, de Sousa PS, Gaspar AM, Pinto MA: First report of a human autochthonous hepatitis E virus infection in Brazil. J Clin Virol. 2010, 47: 276-279. 10.1016/j.jcv.2009.12.021.CrossRefPubMed
27.
go back to reference Jothikumar N, Cromeans TL, Robertson BH, Meng XJ, Hill VR: A broadly reactive one-step real-time RT-PCR assay for rapid and sensitive detection of hepatitis E virus. J Virol Methods. 2006, 131: 65-71. 10.1016/j.jviromet.2005.07.004.CrossRefPubMed Jothikumar N, Cromeans TL, Robertson BH, Meng XJ, Hill VR: A broadly reactive one-step real-time RT-PCR assay for rapid and sensitive detection of hepatitis E virus. J Virol Methods. 2006, 131: 65-71. 10.1016/j.jviromet.2005.07.004.CrossRefPubMed
28.
go back to reference Pinto MA, Marchevsky RS: Serial opened biopsies applied in nonhuman primate model to study the pathogenesis of hepatitis A virus. Virus Reviews and Research. 2001, 6: 26-33.CrossRef Pinto MA, Marchevsky RS: Serial opened biopsies applied in nonhuman primate model to study the pathogenesis of hepatitis A virus. Virus Reviews and Research. 2001, 6: 26-33.CrossRef
29.
go back to reference Halbur PG, Kasorndorkbua C, Gilbert C, Guenette D, Potters MB, Purcell RH, Emerson SU, Toth TE, Meng XJ: Comparative pathogenesis of infection of pigs with hepatitis E viruses recovered from a pig and a human. J Clin Microbiol. 2001, 39: 918-923. 10.1128/JCM.39.3.918-923.2001.CrossRefPubMedPubMedCentral Halbur PG, Kasorndorkbua C, Gilbert C, Guenette D, Potters MB, Purcell RH, Emerson SU, Toth TE, Meng XJ: Comparative pathogenesis of infection of pigs with hepatitis E viruses recovered from a pig and a human. J Clin Microbiol. 2001, 39: 918-923. 10.1128/JCM.39.3.918-923.2001.CrossRefPubMedPubMedCentral
31.
go back to reference Erker JC, Desai SM, Schlauder GG, Dawson GJ, Mushahwar IK: A hepatitis E virus variant from the United States: molecular characterization and transmission in cynomolgus macaques. J Gen Virol. 1999, 80 (Pt 3): 681-690.CrossRefPubMed Erker JC, Desai SM, Schlauder GG, Dawson GJ, Mushahwar IK: A hepatitis E virus variant from the United States: molecular characterization and transmission in cynomolgus macaques. J Gen Virol. 1999, 80 (Pt 3): 681-690.CrossRefPubMed
32.
go back to reference van Cuyck-Gandre H, Cockman-Thomas R, Caudill JD, Asher LS, Armstrong KL, Hauroeder B, Clements NJ, Binn LN, Longer CF: Experimental African HEV infection in cynomolgus macaques (Macaca fascicularis). J Med Virol. 1998, 55: 197-202. 10.1002/(SICI)1096-9071(199807)55:3<197::AID-JMV3>3.0.CO;2-X.CrossRefPubMed van Cuyck-Gandre H, Cockman-Thomas R, Caudill JD, Asher LS, Armstrong KL, Hauroeder B, Clements NJ, Binn LN, Longer CF: Experimental African HEV infection in cynomolgus macaques (Macaca fascicularis). J Med Virol. 1998, 55: 197-202. 10.1002/(SICI)1096-9071(199807)55:3<197::AID-JMV3>3.0.CO;2-X.CrossRefPubMed
33.
go back to reference Liu P, Bu QN, Wang L, Han J, Du RJ, Lei YX, Ouyang YQ, Li J, Zhu YH, Lu FM, Zhuang H: Transmission of hepatitis E virus from rabbits to cynomolgus macaques. Emerg Infect Dis. 2013, 19: 559-565. 10.3201/eid1904.120827.CrossRefPubMedPubMedCentral Liu P, Bu QN, Wang L, Han J, Du RJ, Lei YX, Ouyang YQ, Li J, Zhu YH, Lu FM, Zhuang H: Transmission of hepatitis E virus from rabbits to cynomolgus macaques. Emerg Infect Dis. 2013, 19: 559-565. 10.3201/eid1904.120827.CrossRefPubMedPubMedCentral
34.
go back to reference Hirano M, Ding X, Tran HT, Li TC, Takeda N, Sata T, Nakamura S, Abe K: Prevalence of antibody against hepatitis E virus in various species of non-human primates: evidence of widespread infection in Japanese monkeys (Macaca fuscata). Jpn J Infect Dis. 2003, 56: 8-11.PubMed Hirano M, Ding X, Tran HT, Li TC, Takeda N, Sata T, Nakamura S, Abe K: Prevalence of antibody against hepatitis E virus in various species of non-human primates: evidence of widespread infection in Japanese monkeys (Macaca fuscata). Jpn J Infect Dis. 2003, 56: 8-11.PubMed
35.
go back to reference Huang F, Yu W, Hua X, Jing S, Zeng W, He Z: Seroepidemiology and molecular characterization of hepatitis E virus in Macaca Mulatta from a Village in Yunnan, China, where Infection with this virus is endemic. Hepat Mon. 2011, 11: 745-749.CrossRefPubMedPubMedCentral Huang F, Yu W, Hua X, Jing S, Zeng W, He Z: Seroepidemiology and molecular characterization of hepatitis E virus in Macaca Mulatta from a Village in Yunnan, China, where Infection with this virus is endemic. Hepat Mon. 2011, 11: 745-749.CrossRefPubMedPubMedCentral
36.
go back to reference Okamoto H, Takahashi M, Nishizawa T, Usui R, Kobayashi E: Presence of antibodies to hepatitis E virus in Japanese pet cats. Infection. 2004, 32: 57-58. 10.1007/s15010-004-3078-0.CrossRefPubMed Okamoto H, Takahashi M, Nishizawa T, Usui R, Kobayashi E: Presence of antibodies to hepatitis E virus in Japanese pet cats. Infection. 2004, 32: 57-58. 10.1007/s15010-004-3078-0.CrossRefPubMed
37.
go back to reference Liu J, Zhang W, Shen Q, Yang S, Huang F, Li P, Guo X, Yang Z, Cui L, Zhu J, Hua X: Prevalence of antibody to hepatitis E virus among pet dogs in the Jiang-Zhe area of China. Scand J Infect Dis. 2009, 41: 291-295. 10.1080/00365540902767031.CrossRefPubMed Liu J, Zhang W, Shen Q, Yang S, Huang F, Li P, Guo X, Yang Z, Cui L, Zhu J, Hua X: Prevalence of antibody to hepatitis E virus among pet dogs in the Jiang-Zhe area of China. Scand J Infect Dis. 2009, 41: 291-295. 10.1080/00365540902767031.CrossRefPubMed
38.
go back to reference Arankalle VA, Chadha MS, Banerjee K, Srinivasan MA, Chobe LP: Hepatitis E virus infection in pregnant rhesus monkeys. Indian J Med Res. 1993, 97: 4-8.PubMed Arankalle VA, Chadha MS, Banerjee K, Srinivasan MA, Chobe LP: Hepatitis E virus infection in pregnant rhesus monkeys. Indian J Med Res. 1993, 97: 4-8.PubMed
39.
go back to reference Nakamura S, Tsuchiya H, Okahara N, Nakagawa T, Ohara N, Yamamoto H, Li TC, Takeda N, Ogasawara K, Torii R: Epidemiology of hepatitis E virus in indoor-captive cynomolgus monkey colony. J Vet Med Sci. 2011, 74: 279-283.CrossRefPubMed Nakamura S, Tsuchiya H, Okahara N, Nakagawa T, Ohara N, Yamamoto H, Li TC, Takeda N, Ogasawara K, Torii R: Epidemiology of hepatitis E virus in indoor-captive cynomolgus monkey colony. J Vet Med Sci. 2011, 74: 279-283.CrossRefPubMed
40.
go back to reference Arankalle VA, Chadha MS, Chobe LP, Nair R, Banerjee K: Cross-challenge studies in rhesus monkeys employing different Indian isolates of hepatitis E virus. J Med Virol. 1995, 46: 358-363. 10.1002/jmv.1890460411.CrossRefPubMed Arankalle VA, Chadha MS, Chobe LP, Nair R, Banerjee K: Cross-challenge studies in rhesus monkeys employing different Indian isolates of hepatitis E virus. J Med Virol. 1995, 46: 358-363. 10.1002/jmv.1890460411.CrossRefPubMed
41.
go back to reference Tsarev SA, Tsareva TS, Emerson SU, Rippy MK, Zack P, Shapiro M, Purcell RH: Experimental hepatitis E in pregnant rhesus monkeys: failure to transmit hepatitis E virus (HEV) to offspring and evidence of naturally acquired antibodies to HEV. J Infect Dis. 1995, 172: 31-37. 10.1093/infdis/172.1.31.CrossRefPubMed Tsarev SA, Tsareva TS, Emerson SU, Rippy MK, Zack P, Shapiro M, Purcell RH: Experimental hepatitis E in pregnant rhesus monkeys: failure to transmit hepatitis E virus (HEV) to offspring and evidence of naturally acquired antibodies to HEV. J Infect Dis. 1995, 172: 31-37. 10.1093/infdis/172.1.31.CrossRefPubMed
42.
go back to reference Pischke S, Suneetha PV, Baechlein C, Barg-Hock H, Heim A, Kamar N, Schlue J, Strassburg CP, Lehner F, Raupach R, Bremer B, Magerstedt P, Cornberg M, Seehusen F, Baumgaertner W, Klempnauer J, Izopet J, Manns MP, Grummer B, Wedemeyer H: Hepatitis E virus infection as a cause of graft hepatitis in liver transplant recipients. Liver Transpl. 2009, 16: 74-82.CrossRef Pischke S, Suneetha PV, Baechlein C, Barg-Hock H, Heim A, Kamar N, Schlue J, Strassburg CP, Lehner F, Raupach R, Bremer B, Magerstedt P, Cornberg M, Seehusen F, Baumgaertner W, Klempnauer J, Izopet J, Manns MP, Grummer B, Wedemeyer H: Hepatitis E virus infection as a cause of graft hepatitis in liver transplant recipients. Liver Transpl. 2009, 16: 74-82.CrossRef
43.
go back to reference le Coutre P, Meisel H, Hofmann J, Rocken C, Vuong GL, Neuburger S, Hemmati PG, Dorken B, Arnold R: Reactivation of hepatitis E infection in a patient with acute lymphoblastic leukaemia after allogeneic stem cell transplantation. Gut. 2009, 58: 699-702. 10.1136/gut.2008.165571.CrossRefPubMed le Coutre P, Meisel H, Hofmann J, Rocken C, Vuong GL, Neuburger S, Hemmati PG, Dorken B, Arnold R: Reactivation of hepatitis E infection in a patient with acute lymphoblastic leukaemia after allogeneic stem cell transplantation. Gut. 2009, 58: 699-702. 10.1136/gut.2008.165571.CrossRefPubMed
44.
go back to reference Khuroo MS, Kamili S: Clinical course and duration of viremia in vertically transmitted hepatitis E virus (HEV) infection in babies born to HEV-infected mothers. J Viral Hepat. 2009, 16: 519-523. 10.1111/j.1365-2893.2009.01101.x.CrossRefPubMed Khuroo MS, Kamili S: Clinical course and duration of viremia in vertically transmitted hepatitis E virus (HEV) infection in babies born to HEV-infected mothers. J Viral Hepat. 2009, 16: 519-523. 10.1111/j.1365-2893.2009.01101.x.CrossRefPubMed
45.
go back to reference Zekavat OR, Makarem A, Karami MY, Amanat A, Mohandes M, Habibagahi M: Serological investigation for hepatitis E virus infection in the patients with chronic maintenance hemodialysis from southwest of Iran. Asian J Transfus Sci. 2013, 7: 21-25. 10.4103/0973-6247.106724.CrossRefPubMedPubMedCentral Zekavat OR, Makarem A, Karami MY, Amanat A, Mohandes M, Habibagahi M: Serological investigation for hepatitis E virus infection in the patients with chronic maintenance hemodialysis from southwest of Iran. Asian J Transfus Sci. 2013, 7: 21-25. 10.4103/0973-6247.106724.CrossRefPubMedPubMedCentral
46.
go back to reference Tsarev SA, Tsareva TS, Emerson SU, Govindarajan S, Shapiro M, Gerin JL, Purcell RH: Successful passive and active immunization of cynomolgus monkeys against hepatitis E. Proc Natl Acad Sci U S A. 1994, 91: 10198-10202. 10.1073/pnas.91.21.10198.CrossRefPubMedPubMedCentral Tsarev SA, Tsareva TS, Emerson SU, Govindarajan S, Shapiro M, Gerin JL, Purcell RH: Successful passive and active immunization of cynomolgus monkeys against hepatitis E. Proc Natl Acad Sci U S A. 1994, 91: 10198-10202. 10.1073/pnas.91.21.10198.CrossRefPubMedPubMedCentral
47.
go back to reference Arankalle VA, Chadha MS, Chobe LP: Long-term serological follow up and cross-challenge studies in rhesus monkeys experimentally infected with hepatitis E virus. J Hepatol. 1999, 30: 199-204. 10.1016/S0168-8278(99)80062-2.CrossRefPubMed Arankalle VA, Chadha MS, Chobe LP: Long-term serological follow up and cross-challenge studies in rhesus monkeys experimentally infected with hepatitis E virus. J Hepatol. 1999, 30: 199-204. 10.1016/S0168-8278(99)80062-2.CrossRefPubMed
48.
go back to reference Arankalle VA, Goverdhan MK, Banerjee K: Antibodies against hepatitis E virus in old world monkeys. J Viral Hepat. 1994, 1: 125-129. 10.1111/j.1365-2893.1994.tb00111.x.CrossRefPubMed Arankalle VA, Goverdhan MK, Banerjee K: Antibodies against hepatitis E virus in old world monkeys. J Viral Hepat. 1994, 1: 125-129. 10.1111/j.1365-2893.1994.tb00111.x.CrossRefPubMed
49.
go back to reference Kamili S, Spelbring J, Carson D, Krawczynski K: Protective efficacy of hepatitis E virus DNA vaccine administered by gene gun in the cynomolgus macaque model of infection. J Infect Dis. 2004, 189: 258-264. 10.1086/380801.CrossRefPubMed Kamili S, Spelbring J, Carson D, Krawczynski K: Protective efficacy of hepatitis E virus DNA vaccine administered by gene gun in the cynomolgus macaque model of infection. J Infect Dis. 2004, 189: 258-264. 10.1086/380801.CrossRefPubMed
50.
go back to reference Bryan JP, Tsarev SA, Iqbal M, Ticehurst J, Emerson S, Ahmed A, Duncan J, Rafiqui AR, Malik IA, Purcell RH, Legters LJ: Epidemic hepatitis E in Pakistan: patterns of serologic response and evidence that antibody to hepatitis E virus protects against disease. J Infect Dis. 1994, 170: 517-521. 10.1093/infdis/170.3.517.CrossRefPubMed Bryan JP, Tsarev SA, Iqbal M, Ticehurst J, Emerson S, Ahmed A, Duncan J, Rafiqui AR, Malik IA, Purcell RH, Legters LJ: Epidemic hepatitis E in Pakistan: patterns of serologic response and evidence that antibody to hepatitis E virus protects against disease. J Infect Dis. 1994, 170: 517-521. 10.1093/infdis/170.3.517.CrossRefPubMed
51.
go back to reference TrehanPati N, Sukriti S, Geffers R, Hissar S, Riese P, Toepfer T, Guzman CA, Sarin SK: Gene expression profiles of T cells from hepatitis E virus infected patients in acute and resolving phase. J Clin Immunol. 2011, 31: 498-508. 10.1007/s10875-010-9506-2.CrossRefPubMed TrehanPati N, Sukriti S, Geffers R, Hissar S, Riese P, Toepfer T, Guzman CA, Sarin SK: Gene expression profiles of T cells from hepatitis E virus infected patients in acute and resolving phase. J Clin Immunol. 2011, 31: 498-508. 10.1007/s10875-010-9506-2.CrossRefPubMed
52.
go back to reference Pfefferle S, Frickmann H, Gabriel M, Schmitz N, Gunther S, Schmidt-Chanasit J: Fatal course of an autochthonous hepatitis E virus infection in a patient with leukemia in Germany. Infection. 2012, 40: 451-454. 10.1007/s15010-011-0220-7.CrossRefPubMed Pfefferle S, Frickmann H, Gabriel M, Schmitz N, Gunther S, Schmidt-Chanasit J: Fatal course of an autochthonous hepatitis E virus infection in a patient with leukemia in Germany. Infection. 2012, 40: 451-454. 10.1007/s15010-011-0220-7.CrossRefPubMed
53.
go back to reference Prabhu SB, Gupta P, Durgapal H, Rath S, Gupta SD, Acharya SK, Panda SK: Study of cellular immune response against hepatitis E virus (HEV). J Viral Hepat. 2011, 18: 587-594. 10.1111/j.1365-2893.2010.01338.x.CrossRefPubMed Prabhu SB, Gupta P, Durgapal H, Rath S, Gupta SD, Acharya SK, Panda SK: Study of cellular immune response against hepatitis E virus (HEV). J Viral Hepat. 2011, 18: 587-594. 10.1111/j.1365-2893.2010.01338.x.CrossRefPubMed
54.
go back to reference Amarapurkar DN, Amarapurkar AD: Extrahepatic manifestations of viral hepatitis. Ann Hepatol. 2002, 1: 192-195.PubMed Amarapurkar DN, Amarapurkar AD: Extrahepatic manifestations of viral hepatitis. Ann Hepatol. 2002, 1: 192-195.PubMed
55.
go back to reference Cheung MC, Maguire J, Carey I, Wendon J, Agarwal K: Review of the neurological manifestations of hepatitis E infection. Ann Hepatol. 2012, 11: 618-622.PubMed Cheung MC, Maguire J, Carey I, Wendon J, Agarwal K: Review of the neurological manifestations of hepatitis E infection. Ann Hepatol. 2012, 11: 618-622.PubMed
56.
go back to reference Li L, Zhu Y, Fu H, Wei X, Wang L, Liang J, Ji Y, Tang R, Zhuang H: Full-genome nucleotide sequence and analysis of a Chinese swine hepatitis E virus isolate of genotype 4 identified in the Guangxi Zhuang autonomous region: evidence of zoonotic risk from swine to human in South China. Liver Int. 2009, 29: 1230-1240. 10.1111/j.1478-3231.2009.02012.x.CrossRefPubMed Li L, Zhu Y, Fu H, Wei X, Wang L, Liang J, Ji Y, Tang R, Zhuang H: Full-genome nucleotide sequence and analysis of a Chinese swine hepatitis E virus isolate of genotype 4 identified in the Guangxi Zhuang autonomous region: evidence of zoonotic risk from swine to human in South China. Liver Int. 2009, 29: 1230-1240. 10.1111/j.1478-3231.2009.02012.x.CrossRefPubMed
57.
go back to reference Kamar N, Selves J, Mansuy JM, Ouezzani L, Peron JM, Guitard J, Cointault O, Esposito L, Abravanel F, Danjoux M, Durand D, Vinel JP, Izopet J, Rostaing L: Hepatitis E virus and chronic hepatitis in organ-transplant recipients. N Engl J Med. 2008, 358: 811-817. 10.1056/NEJMoa0706992.CrossRefPubMed Kamar N, Selves J, Mansuy JM, Ouezzani L, Peron JM, Guitard J, Cointault O, Esposito L, Abravanel F, Danjoux M, Durand D, Vinel JP, Izopet J, Rostaing L: Hepatitis E virus and chronic hepatitis in organ-transplant recipients. N Engl J Med. 2008, 358: 811-817. 10.1056/NEJMoa0706992.CrossRefPubMed
58.
go back to reference Ikeda T, Morimoto A, Nakamura S, Yokoyama K, Hayase T, Oh Y, Kashii Y, Yotsumoto S, Okamoto H, YM M: A marked decrease in CD4-positive lymphocytes at the onset of hepatitis in a patient with hepatitis-associated aplastic anemia. J Pediatr Hematol Oncol. 2012, 34: 375-377. 10.1097/MPH.0b013e31822bf699.CrossRefPubMed Ikeda T, Morimoto A, Nakamura S, Yokoyama K, Hayase T, Oh Y, Kashii Y, Yotsumoto S, Okamoto H, YM M: A marked decrease in CD4-positive lymphocytes at the onset of hepatitis in a patient with hepatitis-associated aplastic anemia. J Pediatr Hematol Oncol. 2012, 34: 375-377. 10.1097/MPH.0b013e31822bf699.CrossRefPubMed
59.
go back to reference Mizukawa Y, Shiohara T: Virus-induced immune dysregulation as a triggering factor for the development of drug rashes and autoimmune diseases: with emphasis on EB virus, human herpesvirus 6 and hepatitis C virus. J Dermatol Sci. 2000, 22: 169-180. 10.1016/S0923-1811(99)00083-3.CrossRefPubMed Mizukawa Y, Shiohara T: Virus-induced immune dysregulation as a triggering factor for the development of drug rashes and autoimmune diseases: with emphasis on EB virus, human herpesvirus 6 and hepatitis C virus. J Dermatol Sci. 2000, 22: 169-180. 10.1016/S0923-1811(99)00083-3.CrossRefPubMed
60.
go back to reference Meng XJ: Swine hepatitis E virus: cross-species infection and risk in xenotransplantation. Curr Top Microbiol Immunol. 2003, 278: 185-216. 10.1007/978-3-642-55541-1_7.PubMed Meng XJ: Swine hepatitis E virus: cross-species infection and risk in xenotransplantation. Curr Top Microbiol Immunol. 2003, 278: 185-216. 10.1007/978-3-642-55541-1_7.PubMed
Metadata
Title
Infection by Brazilian and Dutch swine hepatitis E virus strains induces haematological changes in Macaca fascicularis
Authors
Lilian G de Carvalho
Renato S Marchevsky
Debora RL dos Santos
Jaqueline M de Oliveira
Vanessa S de Paula
Leilane M Lopes
Wilhelmus HM Van der Poel
Jorge E González
Maria S Munné
Julio Moran
Ana Carolina R A Cajaraville
Marcelo Pelajo-Machado
Oswaldo G Cruz
Marcelo A Pinto
Publication date
01-12-2013
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2013
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/1471-2334-13-495

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