Cynomolgus monkeys are successfully and persistently infected with hepatitis E virus genotype 3 (HEV-3) after long-term immunosuppressive therapy

PLoS ONE

Volumn 12, Issue 3, 2017, Pages

  Gardinali, Noemi Rovaris ^a   Guimarães, Juliana Rodrigues ^a   Melgaço, Juliana Gil ^a   Kevorkian, Yohan Britto ^a   De Bottino, Fernanda Oliveira ^a   Vieira, Yasmine Rangel ^a   De Silva, Aline Campos Azevedo Da ^a   Pinto, Douglas Pereira ^a   Fonseca, Laís Bastos Da ^a   Vilhena, Leandro Schiavo ^a   Uiechi, Edilson ^b   Silva, Maria Cristina Carlan Da ^c   Moran, Julio ^d   Marchevsky, Renato Sérgio ^a   Cruz, Oswaldo Gonçalves ^a   Otonel, Rodrigo Alejandro Arellano ^e   Alfieri, Amauri Alcindo ^e   Oliveira, Jaqueline Mendes De ^a   Gaspar, Ana Maria Coimbra ^a   Pinto, Marcelo Alves ^a  

^a INSTITUTO OSWALDO CRUZ   (Brazil)

^b Libbs Pharmaceuticals Ltd   (Brazil)

^c UNIVERSIDADE FEDERAL DO ABC   (Brazil)

^d Dr Julio Moran Laboratories   (Switzerland)

^e STATE UNIVERSITY OF LONDRINA   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

LIVER ENZYME; TACROLIMUS; VIRUS RNA; HEPATITIS ANTIBODY; IMMUNOSUPPRESSIVE AGENT;

ALOPECIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD LEVEL; CLINICAL FEATURE; CONTROLLED STUDY; FEMALE; GENOTYPE; HEMATOLOGICAL PARAMETERS; HEPATITIS E; HEPATITIS E VIRUS 3 INFECTION; HISTOPATHOLOGY; IMMUNOSUPPRESSIVE TREATMENT; LIVER BIOPSY; LONG TERM CARE; MACACA FASCICULARIS; MALE; NONHUMAN; OPPORTUNISTIC INFECTION; VIRUS GENOME; VIRUS IDENTIFICATION; VIRUS SHEDDING; VIRUS STRAIN; WEIGHT REDUCTION; ANIMAL; BRAZIL; GENETICS; HEPATITIS E VIRUS; IMMUNOLOGY; LIVER; LIVER CIRRHOSIS; LIVER FUNCTION TEST; PATHOGENICITY; PROCEDURES; VIROLOGY;

ANIMALS; BRAZIL; FEMALE; GENOTYPE; HEPATITIS ANTIBODIES; HEPATITIS E; HEPATITIS E VIRUS; IMMUNOSUPPRESSION; IMMUNOSUPPRESSIVE AGENTS; LIVER; LIVER CIRRHOSIS; LIVER FUNCTION TESTS; MACACA FASCICULARIS; MALE; RNA, VIRAL; VIRUS SHEDDING;

EID: 85015891169     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0174070     Document Type: Article

References (62)

1. Smith DB, Simmonds P, International Committee on Taxonomy of Viruses Hepeviridae Study G, Jameel S, Emerson SU, Harrison TJ, et al. Consensus proposals for classification of the family Hepeviridae. J Gen Virol. 2014; 95(Pt 10):2223-32. PubMed Central PMCID: PMC4165930. https://doi.org/10. 1099/vir.0.068429-0 PMID: 24989172
2. Khuroo MS, Khuroo NS. Transmission of Hepatitis E Virus in Developing Countries. Viruses. 2016; 8 (9). Epub 2016/09/23. PubMed Central PMCID: PMCPMC5035967.
3. 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(3):276-9.Epub 2010/02/02. https://doi.org/10.1016/j.jcv.2009.12.021 PMID: 20116328
4. Hering T, Passos AM, Perez RM, Bilar J, Fragano D, Granato C, et al. Past and current hepatitis E virus infection in renal transplant patients. J Med Virol. 2014; 86(6):948-53. Epub 2014/03/13. https://doi.org/ 10.1002/jmv.23915 PMID: 24619955
5. Passos-Castilho AM, Porta G, Miura IK, Pugliese RP, Danesi VL, Porta A, et al. Chronic hepatitis E virus infection in a pediatric female liver transplant recipient. J Clin Microbiol. 2014; 52(12):4425-7.PubMed Central PMCID: PMCPMC4313334. https://doi.org/10.1128/JCM.02286-14 PMID: 25275004
6. 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(1-2):236-41. Epub 2010/12/07. https://doi.org/10.1016/j.vetmic.2010.10.024 PMID: 21129863
7. 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 (3):1515-9. Epub 2012/07/10. https://doi.org/10.1016/j.rvsc.2012.06.003 PMID: 22769738
8. Heldt FH, Staggmeier R, Gularte JS, Demoliner M, Henzel A, Spilki FR. Hepatitis E Virus in Surface Water, Sediments, and Pork Products Marketed in Southern Brazil. Food Environ Virol. 2016. Epub 2016/05/14.
9. Yugo DM, Meng XJ. Hepatitis E virus: foodborne, waterborne and zoonotic transmission. Int J Environ Res Public Health. 2013; 10(10):4507-33. Epub 2013/09/28. PubMed Central PMCID: PMCPMC3823334. https://doi.org/10.3390/ijerph10104507 PMID: 24071919
10. Said B, Ijaz S, Kafatos G, Booth L, Thomas HL, Walsh A, et al. Hepatitis E outbreak on cruise ship. Emerg Infect Dis. 2009; 15(11):1738-44. Epub 2009/11/07. PubMed Central PMCID: PMCPMC2857258. https://doi.org/10.3201/eid1511.091094 PMID: 19891860
11. Kokkinos P, Kozyra I, Lazic S, Bouwknegt M, Rutjes S, Willems K, et al. Harmonised investigation of the occurrence of human enteric viruses in the leafy green vegetable supply chain in three European countries. Food Environ Virol. 2012; 4(4):179-91. Epub 2013/02/16. https://doi.org/10.1007/s12560-012-9087-8 PMID: 23412890
12. Maunula L, Kaupke A, Vasickova P, Soderberg K, Kozyra I, Lazic S, et al. Tracing enteric viruses in the European berry fruit supply chain. Int J Food Microbiol. 2013; 167(2):177-85. Epub 2013/10/19. https:// doi.org/10.1016/j.ijfoodmicro.2013.09.003 PMID: 24135674
13. Kamar N, Selves J, Mansuy JM, Ouezzani L, Peron JM, Guitard J, et al. Hepatitis E virus and chronic hepatitis in organ-transplant recipients. N Engl J Med. 2008; 358(8):811-7. Epub 2008/02/22. https:// doi.org/10.1056/NEJMoa0706992 PMID: 18287603
14. Haagsma EB, van den Berg AP, Porte RJ, Benne CA, Vennema H, Reimerink JH, et al. Chronic hepatitis E virus infection in liver transplant recipients. Liver Transpl. 2008; 14(4):547-53. Epub 2008/04/03. https://doi.org/10.1002/lt.21480 PMID: 18383084
15. Geng Y, Zhao C, Huang W, Harrison TJ, Zhang H, Geng K, et al. Detection and assessment of infectivity of hepatitis E virus in urine. J Hepatol. 2016; 64(1):37-43. https://doi.org/10.1016/j.jhep.2015.08.034PMID: 26362822
16. Tamura A, Shimizu YK, Tanaka T, Kuroda K, Arakawa Y, Takahashi K, et al. Persistent infection of hepatitis E virus transmitted by blood transfusion in a patient with T-cell lymphoma. Hepatol Res. 2007; 37 (2):113-20. Epub 2007/02/16. https://doi.org/10.1111/j.1872-034X.2007.00024.x PMID: 17300706
17. Dalton HR, Bendall RP, Keane FE, Tedder RS, Ijaz S. Persistent carriage of hepatitis E virus in patients with HIV infection. N Engl J Med. 361. United States2009. p. 1025-7. https://doi.org/10.1056/ NEJMc0903778 PMID: 19726781
18. Kamar N, Rostaing L, Legrand-Abravanel F, Izopet J. How should hepatitis E virus infection be defined in organ-transplant recipients? Am J Transplant. 2013; 13(7):1935-6. Epub 2013/05/11. https://doi.org/ 10.1111/ajt.12253 PMID: 23659713
19. Kamar N, Garrouste C, Haagsma EB, Garrigue V, Pischke S, Chauvet C, et al. Factors associated with chronic hepatitis in patients with hepatitis E virus infection who have received solid organ transplants.Gastroenterology. 2011; 140(5):1481-9. Epub 2011/03/01. https://doi.org/10.1053/j.gastro.2011.02.050 PMID: 21354150
20. Legrand-Abravanel F, Kamar N, Sandres-Saune K, Garrouste C, Dubois M, Mansuy JM, et al. Characteristics of autochthonous hepatitis E virus infection in solid-organ transplant recipients in France. J Infect Dis. 2010; 202(6):835-44. Epub 2010/08/11. https://doi.org/10.1086/655899 PMID: 20695798
21. Griffin SP, Nelson JE. Impact of a Clinical Solid Organ Transplant Pharmacist on Tacrolimus Nephrotoxicity, Therapeutic Drug Monitoring, and Institutional Revenue Generation in Adult Kidney Transplant Recipients. Prog Transplant. 2016. Epub 2016/09/16.
22. Wang Y, Zhou X, Debing Y, Chen K, Van Der Laan LJ, Neyts J, et al. Calcineurin inhibitors stimulate and mycophenolic acid inhibits replication of hepatitis E virus. Gastroenterology. 2014; 146(7):1775-83. Epub 2014/03/04. https://doi.org/10.1053/j.gastro.2014.02.036 PMID: 24582714
23. Huang F, Yang C, Zhou X, Yu W, Pan Q. Rhesus macaques persistently infected with hepatitis E shed virus into urine. J Hepatol. 2016.
24. Longer CF, Denny SL, Caudill JD, Miele TA, Asher LV, Myint KS, et al. Experimental hepatitis E: pathogenesis in cynomolgus macaques (Macaca fascicularis). J Infect Dis. 1993; 168(3):602-9. Epub 1993/ 09/01. PMID: 8354901
25. Tsarev SA, Emerson SU, Tsareva TS, Yarbough PO, Lewis M, Govindarajan S, et al. Variation in course of hepatitis E in experimentally infected cynomolgus monkeys. J Infect Dis. 1993; 167(6):1302-6. Epub 1993/06/01. PMID: 8501318
26. de Carvalho LG, Marchevsky RS, dos Santos DR, de Oliveira JM, de Paula VS, Lopes LM, et al. Infection by Brazilian and Dutch swine hepatitis E virus strains induces haematological changes in Macaca fascicularis. BMC Infect Dis. 2013; 13:495. Epub 2013/10/24. PubMed Central PMCID: PMCPMC3870956. https://doi.org/10.1186/1471-2334-13-495 PMID: 24148233
27. Matthews KA, Tonsho M, Madsen JC. New-Onset Diabetes Mellitus After Transplantation in a Cynomolgus Macaque (Macaca fasicularis). Comp Med. 2015; 65(4):352-6. Epub 2015/08/28. PubMed Central PMCID: PMCPMC4549682. PMID: 26310466
28. Kinugasa F, Nagatomi I, Ishikawa H, Nakanishi T, Maeda M, Hirose J, et al. Efficacy of oral treatment with tacrolimus in the renal transplant model in cynomolgus monkeys. J Pharmacol Sci. 2008; 108 (4):529-34. Epub 2008/12/23. PMID: 19098392
29. Haustein SV, Kolterman AJ, Sundblad JJ, Fechner JH, Knechtle SJ. Nonhuman primate infections after organ transplantation. Ilar j. 2008; 49(2):209-19. Epub 2008/03/08. PubMed Central PMCID: PMCPMC4876599. PMID: 18323582
30. 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(1):65-71. Epub 2005/08/30. https://doi.org/10.1016/j.jviromet.2005.07.004 PMID: 16125257
31. Wang Y, Ling R, Erker JC, Zhang H, Li H, Desai S, et al. A divergent genotype of hepatitis E virus in Chinese patients with acute hepatitis. J Gen Virol. 1999; 80 Pt 1):169-77. Epub 1999/02/06.
32. Huang FF, Haqshenas G, Guenette DK, Halbur PG, Schommer SK, Pierson FW, et al. Detection by reverse transcription-PCR and genetic characterization of field isolates of swine hepatitis E virus from pigs in different geographic regions of the United States. J Clin Microbiol. 2002; 40(4):1326-32. Epub 2002/03/30. PubMed Central PMCID: PMCPMC140370. https://doi.org/10.1128/JCM.40.4.1326-1332.2002 PMID: 11923352
33. Kleiner DE, Brunt EM, Van Natta M, Behling C, Contos MJ, Cummings OW, et al. Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology. 2005; 41(6):1313-21.Epub 2005/05/26. https://doi.org/10.1002/hep.20701 PMID: 15915461
34. Pischke S, Stiefel P, Franz B, Bremer B, Suneetha PV, Heim A, et al. Chronic hepatitis e in heart transplant recipients. Am J Transplant. 2012; 12(11):3128-33. Epub 2012/07/25. https://doi.org/10.1111/j. 1600-6143.2012.04200.x PMID: 22823202
35. Haagsma EB, Niesters HG, van den Berg AP, Riezebos-Brilman A, Porte RJ, Vennema H, et al. Prevalence of hepatitis E virus infection in liver transplant recipients. Liver Transpl. 2009; 15(10):1225-8.Epub 2009/10/01. https://doi.org/10.1002/lt.21819 PMID: 19790147
36. Passos AM, Heringer TP, Medina-Pestana JO, Ferraz ML, Granato CF. First report and molecular characterization of hepatitis E virus infection in renal transplant recipients in Brazil. J Med Virol. 2013; 85 (4):615-9. Epub 2013/02/06. https://doi.org/10.1002/jmv.23494 PMID: 23382036
37. Aggarwal R, Kamili S, Spelbring J, Krawczynski K. Experimental studies on subclinical hepatitis E virus infection in cynomolgus macaques. J Infect Dis. 2001; 184(11):1380-5. Epub 2001/12/26. https://doi. org/10.1086/324376 PMID: 11709779
38. Zhu FC, Zhang J, Zhang XF, Zhou C, Wang ZZ, Huang SJ, et al. Efficacy and safety of a recombinant hepatitis E vaccine in healthy adults: a large-scale, randomised, double-blind placebo-controlled, phase3 trial. Lancet. 2010; 376(9744):895-902. Epub 2010/08/24. https://doi.org/10.1016/S0140-6736(10) 61030-6 PMID: 20728932
39. Pischke S, Suneetha PV, Baechlein C, Barg-Hock H, Heim A, Kamar N, et al. Hepatitis E virus infection as a cause of graft hepatitis in liver transplant recipients. Liver Transpl. 2010; 16(1):74-82. Epub 2009/ 10/30. https://doi.org/10.1002/lt.21958 PMID: 19866448
40. Suneetha PV, Pischke S, Schlaphoff V, Grabowski J, Fytili P, Gronert A, et al. Hepatitis E virus (HEV)-specific T-cell responses are associated with control of HEV infection. Hepatology. 2012; 55(3):695-708. Epub 2011/10/19. https://doi.org/10.1002/hep.24738 PMID: 22006345
41. Lhomme S, Abravanel F, Dubois M, Sandres-Saune K, Rostaing L, Kamar N, et al. Hepatitis E virus quasispecies and the outcome of acute hepatitis E in solid-organ transplant patients. J Virol. 2012; 86 (18):10006-14. Epub 2012/07/05. PubMed Central PMCID: PMCPMC3446597. https://doi.org/10. 1128/JVI.01003-12 PMID: 22761386
42. Krogsgaard K, Wantzin P, Mathiesen L, Ring-Larsen H. Chronic evolution of acute hepatitis B: the significance of simultaneous infections with hepatitis C and D. Copenhagen Hepatitis Acuta Programme. Scand J Gastroenterol. 1991; 26(3):275-80. Epub 1991/03/01. PMID: 1906632
43. Ciftci HS, Ayna TK, Caliskan YK, Turkmen A, Gurtekin M. Lipid parameters, doses and blood levels of calcineurin inhibitors in renal transplant patients. Indian J Clin Biochem. 2013; 28(2):164-8. Epub 2014/ 01/16. PubMed Central PMCID: PMCPMC3613508. https://doi.org/10.1007/s12291-012-0251-6 PMID: 24426203
44. Du L, Tang H. An insight into the molecular characteristics of hepatitis C virus for clinicians. Saudi Med J. 2016; 37(5):483-91. https://doi.org/10.15537/smj.2016.5.14178 PMID: 27146609
45. Mahalingam R, Traina-Dorge V, Wellish M, Deharo E, Singletary ML, Ribka EP, et al. Latent simian varicella virus reactivates in monkeys treated with tacrolimus with or without exposure to irradiation. J Neurovirol. 2010; 16(5):342-54. Epub 2010/09/09. PubMed Central PMCID: PMCPMC3076590. https://doi. org/10.3109/13550284.2010.513031 PMID: 20822371
46. Chin JL, Hisamuddin SH, O'Sullivan A, Chan G, McCormick PA. Thrombocytopenia, Platelet Transfusion, and Outcome Following Liver Transplantation. Clin Appl Thromb Hemost. 2016; 22(4):351-60.Epub 2014/11/29. https://doi.org/10.1177/1076029614559771 PMID: 25430936
47. Diaz GC, Prowda J, Lo IJ, Arepally GM, Evans N, Wheeless Y, et al. Transplantation-mediated alloimmune thrombocytopenia: Guidelines for utilization of thrombocytopenic donors. Liver Transpl. 2008; 14 (12):1803-9. Epub 2008/11/26. https://doi.org/10.1002/lt.21539 PMID: 19025920
48. Arai K, Kuramitsu K, Fukumoto T, Kido M, Takebe A, Tanaka M, et al. A Case Report of Drug-Induced Thrombocytopenia after Living Donor Liver Transplantation. Kobe J Med Sci. 2016; 62(1):E9-e12.Epub 2016/08/06. PMID: 27492209
49. Colson P, Payraudeau E, Leonnet C, De Montigny S, Villeneuve L, Motte A, et al. Severe thrombocytopenia associated with acute hepatitis E virus infection. J Clin Microbiol. 2008; 46(7):2450-2. Epub 2008/05/16. PubMed Central PMCID: PMCPMC2446901. https://doi.org/10.1128/JCM.02295-07PMID: 18480231
50. Fourquet E, Mansuy JM, Bureau C, Recher C, Vinel JP, Izopet J, et al. Severe thrombocytopenia associated with acute autochthonous hepatitis E. J Clin Virol. 48. Netherlands2010. p. 73-4. https://doi.org/ 10.1016/j.jcv.2010.02.016 PMID: 20308017
51. Jusko WJ, Thomson AW, Fung J, McMaster P, Wong SH, Zylber-Katz E, et al. Consensus document: therapeutic monitoring of tacrolimus (FK-506). Ther Drug Monit. 1995; 17(6):606-14. Epub 1995/12/01.PMID: 8588229
52. Kisu I, Mihara M, Banno K, Hara H, Masugi Y, Araki J, et al. Uterus allotransplantation in cynomolgus macaque: a preliminary experience with non-human primate models. J Obstet Gynaecol Res. 2014; 40 (4):907-18. Epub 2014/03/13. https://doi.org/10.1111/jog.12302 PMID: 24612366
53. Kamar N, Abravanel F, Selves J, Garrouste C, Esposito L, Lavayssiere L, et al. Influence of immunosuppressive therapy on the natural history of genotype 3 hepatitis-E virus infection after organ transplantation. Transplantation. 2010; 89(3):353-60. Epub 2010/02/11. https://doi.org/10.1097/TP.0b013e3181c4096c PMID: 20145528
54. Dalton HR, Webb GW, Norton BC, Woolson KL. Hepatitis E Virus: Time to Change the Textbooks. Dig Dis. 2016; 34(4):308-16. Epub 2016/05/14. https://doi.org/10.1159/000444468 PMID: 27170383
55. Williams TP, Kasorndorkbua C, Halbur PG, Haqshenas G, Guenette DK, Toth TE, et al. Evidence of extrahepatic sites of replication of the hepatitis E virus in a swine model. J Clin Microbiol. 2001; 39 (9):3040-6. Epub 2001/08/30. PubMed Central PMCID: PMCPMC88293. https://doi.org/10.1128/JCM. 39.9.3040-3046.2001 PMID: 11526125
56. Liu P, Bu QN, Wang L, Han J, Du RJ, Lei YX, et al. Transmission of hepatitis E virus from rabbits to cynomolgus macaques. Emerg Infect Dis. 2013; 19(4):559-65. Epub 2013/05/01. PubMed Central PMCID: PMCPMC3647409. https://doi.org/10.3201/eid1904.120827 PMID: 23628346
57. Kamar N, Marion O, Abravanel F, Izopet J, Dalton HR. Extrahepatic manifestations of hepatitis E virus. Liver Int. 2016; 36(4):467-72. https://doi.org/10.1111/liv.13037 PMID: 27005692
58. Kamar N, Izopet J, Cintas P, Garrouste C, Uro-Coste E, Cointault O, et al. Hepatitis E virus-induced neurological symptoms in a kidney-transplant patient with chronic hepatitis. Am J Transplant. 2010; 10 (5):1321-4. Epub 2010/03/30. https://doi.org/10.1111/j.1600-6143.2010.03068.x PMID: 20346067
59. Han J, Lei Y, Liu L, Liu P, Xia J, Zhang Y, et al. SPF rabbits infected with rabbit hepatitis E virus isolate experimentally showing the chronicity of hepatitis. PLoS One. 2014; 9(6):e99861. Epub 2014/06/18.PubMed Central PMCID: PMCPMC4061063. https://doi.org/10.1371/journal.pone.0099861 PMID: 24937350
60. Marchetti P, Navalesi R. The metabolic effects of cyclosporin and tacrolimus. J Endocrinol Invest. 2000; 23(7):482-90. Epub 2000/09/27. https://doi.org/10.1007/BF03343761 PMID: 11005276
61. Muduma G, Saunders R, Odeyemi I, Pollock RF. Systematic Review and Meta-Analysis of Tacrolimus versus Ciclosporin as Primary Immunosuppression After Liver Transplant. PLOS ONE. 2016; 11(11): e0160421. https://doi.org/10.1371/journal.pone.0160421 PMID: 27812112
62. Bloom RD, Rao V, Weng F, Grossman RA, Cohen D, Mange KC. Association of hepatitis C with posttransplant diabetes in renal transplant patients on tacrolimus. J Am Soc Nephrol. 2002; 13(5):1374-80.Epub 2002/04/19. PMID: 11961026