Este é o primeiro relato do isolamento de NoV de rato em cultura celular;
Este isolado de cultura celular resultou no depósito da cepa brasileira no GenBank sob o n° de acesso KU169124;
Nós desenvolvemos uma semi-nested RT-PCR sensível, capaz de detectar de maneira eficiente NoV em amostras de fezes de rato, bem como determinamos a prevalência molecular de NoV de rato em biotérios brasileiros mantidos sob sistema de barreiras sanitárias ou convencionais;
Implantamos a reação sorológica de IFI como uma alternativa eficiente na detecção de NoV de rato, bem como determinamos a prevalência sorológica do vírus;
Baseado na análise filogenética dos isolados nós sugerimos que Norovírus do rato seja classificado no GV como um novo genótipo, chamado GV.II;
Devido à prevalência do vírus, sugerimos a inserção deste agente na lista de exclusão da FELASA (Federação Européia de Animais de Laboratório).
5 REFERÊNCIAS
1 Harris JP, Lopman BA, O-Brien SJ. Infection control measures for norovirus: a systematic review of outbreaks in semi-enclosed settings. Journal of Hospital
Infection. 2010;74(1):1–9.
2 Ahmed SM, Hall AJ, Robinson AE, et al. Global prevalence of norovirus in cases of gastroenteritis: a systematic review and meta-analysis. Lancet Infect Dis 2014; 14: 725–730.
3 Troeger H, Loddenkemper C, Schneider T, et al. Structural and functional changes of the duodenum in human norovirus infection. Gut 2009; 58: 1070–1077.
4 Scipioni A, Mauroy A, Vinjé J, Thiry E. 2008. Animal noroviruses. Vet J 178:32– 45.
5 Zahorsky J. Hyperemesis hiemis or the winter vomiting disease. Arch Pediatr 1929; 46: 391–395.
6 Adler, J. L.; Zickl, R. Winter vomiting disease.The Journal of Infectious Diseases, Chicago, v. 119, p. 668-673, 1969.
7 Madeley, C. R.; Cosgrove, B. P. Caliciviruses in man.The Lancet, London, v.307, n. 7952, p. 199-200, 1976.
8 Kapikian AZ, Wyatt RG, Dolin R, Thornhill TS, Kalica AR, Chanock RM. Visualization by immune electron microscopy of a 27-nm particle associated with acute infectious nonbacterial gastroenteritis. J Virol 1972; 10:1075–81.
9 Kapikian AZ. The discovery of the 27-nm Norwalk virus: an historic perspective.
J Infect Dis 2000; 181 (Suppl 2): S295–S302.
10 Jiang, X.; Huang, P. W.; Zhong, W. M.; Farkas, T.; Cubitti, D. W.; Matson, D. O. Design and evaluation of a primer pair that detects both norwalk- and Sapporo-like caliciviruses by RT-PCR. Journal of Virological Methods, Amsterdam, v. 83, n. 1-2, p. 145- 154, 1999.
11 Green KY, Ando T, Balayan MS, Berke T, Clarke IN, Estes MK, et al. Taxonomy of the caliciviruses. J Infect Dis. 2000;181: S322-S330. doi: 10.1086/315591
12 Elizabeth Robilotti,a Stan Deresinski,a Benjamin A. Pinskya,b Norovirus Clinical Microbiology Reviews January 2015 p.134-164, vol 28, n 1.
13 Smiley, J. R.; Chang, K. O.; Hayes, J.; Vinjé, J.; Saif, L.J. Characterization of an Enteropathogenic Bovine Calicivirus Representing a Potential New Calicivirus Genus. Journal of Virology, Washington, v.76, n.20, p.10089-10098, 2002.
14 Wang, Q. W. Costantiti, V., Saif, L. J. Porcine enteric caliciviruses: genetic and antigenic relatedness to human caliciviruses, diagnosis and epidemiology. Vaccine. Kidlinton, v.25, n.30, p. 5453-5466. 2007.
15 Wang, Q. W.; Chang, K. O.; Han, M. G.; Sreevatsan, S.; Saif, L. J. Development of a new microwell hybridization assay and an internal control RNA for the detection of porcine noroviruses and sapoviruses by reverse transcription-PCR. Journal of Virological Methods, Amsterdam, v.132, n. 1-2, p. 135-145, 2006a.
16 Wang, Q. W.; Souza, M.; Funk, J. A.; Zhang, W.; Saif, L. J. Prevalence of noroviruses and sapoviruses in swine of various ages determined by reverse transcription- PCR and microwell hybridization assays. Journal of Clinical Microbiology, Washington, v. 44, n.6, p. 2057-2062, 2006b.
17 Green KY. Caliciviridae: the noroviruses. In Fields Virology, Volume 1 (6th edn), Knipe DM, Howley PM (eds). LippincottWilliams and Wilkins: Philadelphia, 2013; 582– 608.
18 Vinje J. Advances in laboratory methods for detection and typing of norovirus. J Clin Microbiol. 2015;53: 373-381. doi: 10.1128/JCM.01535-14
19 Karst SM, Zhu S, Goodfellow IG. The molecular pathology of noroviruses. J Pathol. 2015;235: 206-216. doi: 10.1002/path.4463
20 Sugieda M, Nakajima S. Viruses detected in the caecum contents of healthy pigs representing a new genetic cluster in genogroup II of the genus "Norwalk-like viruses". Virus Res. 2002;87: 165-17210.1016/S0168-1702(02)00107-7.
21 Oliver SL, Asobayire E, Charpilienne A, Cohen J, Bridger JC. Complete genomic characterization and antigenic relatedness of genogroup III, genotype 2 bovine noroviruses. Arch Virol. 2007;152: 257-272. doi: 10.1007/s00705-006-0856-2
22 van der Poel WH, van der Heide R, Verschoor F, Gelderblom H, Vinje J, Koopmans MP. Epidemiology of Norwalk-like virus infections in cattle in The Netherlands. Vet Microbiol. 2003;92: 297-309. Doi: 10.1016/S0378-1135(02)00421-2.
23 Karst SM, Wobus CE, Lay M, Davidson J, Virgin HWt. STAT1-dependent innate immunity to a Norwalk-like virus. Science. 2003;299: 1575-1578. doi:
10.1126/science.1077905
24 Martella V, Lorusso E, Decaro N, Elia G, Radogna A, D'Abramo M, et al. Detection and molecular characterization of a canine norovirus. Emerg Infect Dis. 2008;14: 1306-1308. doi: 10.3201/eid1408.080062
25 Green, K. Y. Caliciviridae: The Norovíruses, p. 949-979. In B. N. Fields, D. M. Knipe, and P. M. Howley (ed.), Fields ‘ virology, 5th ed. Wolters Kluwer Health/Lippincott Willliams e Wilkins, Philadelphia, 2007.
26 Chang, K. O.; Sosnovtsev, S. V.; Belliot, G.; Kim, Y.; Saif, L. J.; Green, K. Y. Bile acids are essential for porcine enteric calicivirus replication in association with down- regulation of signal transducer and activator of transcription 1. Proceedings of the National Academy of Sciences of the United States of America, Washington, v. 101, n.23 p. 303-308, 2004.
27 Blakeney, S. J.; Cahil, A.; Reylli, P.A. Processing of Norwalk virus non- structural proteins by a 3C-like cysteine proteinase.Virology, v.308, p. 216-224, 2003.
28 Sosnovtsev, S. V.; Garfield, M.; Green, K. Y. Processing map and essential cleavage sites of the nonstructural polyprotein encoded by ORF1 of the feline calicivirus genome. Journal of Virology, Washington, v.76, n. 14, p. 7060-7072, 2002.
29 Thackray LB, Wobus CE, Chachu KA, Liu B, Alegre ER, Henderson KS, et al. Murine noroviruses comprising a single genogroup exhibit biological diversity despite limited sequence divergence. J Virol. 2007;81: 10460-10473. doi: 10.1128/JVI.00783-07
30 Zheng DP, Ando T, Fankhauser RL, Beard RS, Glass RI, Monroe SS.
Norovirus classification and proposed strain nomenclature. Virology. 2006;346: 312-323. doi: 10.1016/j.virol.2005.11.015
31 McFadden N, Bailey D, Carrara G, Benson A, Chaudhry Y, Shortland A, et al. Norovirus regulation of the innate immune response and apoptosis occurs via the product of the alternative open reading frame 4. PLoS Pathog. 2011;7: e1002413. doi:
10.1371/journal.ppat.1002413
32 Mead, P.S.; Slutsker, L.; Dietz, V.; McCaig, L.F.; Bresee, J.S.; Shapiro, C.; Griffin, P.M.; Tauxe,R.V. Food-related illness and death in the United States. Emerg. Infect.
Dis. 1999, 5, 607–625.
33 Donaldson, E.F.; Lindesmith, L.C.; Lobue, A.D.; Baric, R.S. Norovirus pathogenesis: mechanisms of persistence and immune evasion in human populations.
Immunol. Rev. 2008, 225,190–211.
34 Goto K, Hayashimoto N, Yasuda M, Ishida T, Kameda S, Takakura A, et al. Molecular detection of murine norovirus from experimentally and spontaneously infected mice. Exp Anim. 2009;58: 135-140. doi.10.1538/expanim.58.135.
35 Henderson KS. Murine norovirus, a recently discovered and highly prevalent viral agent of mice. Lab Anim (NY). 2008;37: 314-320. doi: 10.1038/laban0708-314
36 Wobus CE, Thackray LB, Virgin HWt. Murine norovirus: a model system to study norovirus biology and pathogenesis. J Virol. 2006;80: 5104-5112. doi:
10.1128/JVI.02346-05
37 Hsu CC, Wobus CE, Steffen EK, Riley LK, Livingston RS. Development of a microsphere-based serologic multiplexed fluorescent immunoassay and a reverse
transcriptase PCR assay to detect murine norovirus 1 infection in mice. Clin Diagn Lab Immunol. 2005;12: 1145-1151. doi: 10.1128/CDLI.12.10.1145-1151.2005
38 HSU, C.C.; RILEY, L.K.; WILLS, H.M.; LIVINGTON, R.S. Persistent infection with and serologic cross-reactivity of three novel murine Norovíruses.Comparative Medicine v.56, p. 247–251, 2006.
39 Perdue KA, Green KY, Copeland M, Barron E, Mandel M, Faucette LJ, et al. Naturally occurring murine norovirus infection in a large research institution. J Am Assoc Lab Anim Sci. 2007;46: 39-45. doi:10.3389/fmicb.2013.00012.
40 Kim JR, Seok SH, Kim DJ, Baek MW, Na YR, Han JH, et al. Prevalence of murine norovirus infection in Korean laboratory animal facilities. J Vet Med Sci. 2011;73: 687-691. doi.org/10.1292/jvms. 10-0226.
41 Kitagawa Y, Tohya Y, Ike F, Kajita A, Park SJ, Ishii Y, et al. Indirect ELISA and indirect immunofluorescent antibody assay for detecting the antibody against murine norovirus S7 in mice. Exp Anim. 2010;59: 47-55. doi: 10.1538/expanim.59.47.
42 Manjunath S, Kulkarni PG, Nagavelu K, Samuel RJ, Srinivasan S, Ramasamy N, et al. Sero-prevalence of rodent pathogens in India. PLoS One. 2015;10: e0131706. doi: 10.1371/journal.pone.0131706
43 Kitajima M, Oka T, Takagi H, Tohya Y, Katayama H, Takeda N, et al.
Development and application of a broadly reactive real-time reverse transcription-PCR assay for detection of murine noroviruses. J Virol Methods. 2010;169: 269-273. doi:
10.1016/j.jviromet.2010.07.018.
44 Mumphrey, S.M., Changotra, H., Moore, T.N., Heimann-Nichols, E.R., Wobus, C.E., Reilly, M.J., Moghadamfalahi, M., Shukla, D., Karst, S.M., 2007. Murine norovirus1 infection is associated with histopathological changes in immunocompetent hosts, but clinical disease is prevented by STAT1-dependent interferon responses. J. Virol. 81, 3251–3263.
45 Wobus, C.E., Karst, S.M., Thackray, L.B., Chang, K.O., Sosnovtsev, S.V., Belliot, G., Krug,A., Mackenzie, J.M., Green, K.Y., Virgin, H.W., 2004. Replication of
Norovirus in cell culture reveals a tropism for dendritic cells and macrophages. PLoS Biol. 2, 2076–2084.
46 Lay MK, Atmar RL, Guix S, Bharadwaj U, He H, Neill FH, Sastry KJ, Yao Q, Estes MK. Norwalk virus does not replicate in human macrophages or dendritic cells derived from the peripheral blood of susceptible humans. Virology. 2010;406:1–11
47 Takanashi S, Saif LJ, Hughes JH, Meulia T, Jung K, Scheuer KA, et al. Failure of propagation of human norovirus in intestinal epithelial cells with microvilli grown in three- dimensional cultures. Arch Virol. 2014;159: 257-266. doi: 10.1007/s00705-013-1806-4
48 Jones MK, Watanabe M, Zhu S, Graves CL, Keyes LR, Grau KR, et al. Enteric bacteria promote human and mouse norovirus infection of B cells. Science. 2014;346: 755- 759. doi: 10.1126/science.1257147
49 Jones MK, Grau KR, Costantini V, Kolawole AO, de Graaf M, Freiden P, et al. Human norovirus culture in B cells. Nat Protoc. 2015;10: 1939-1947. doi:
10.1038/nprot.2015.121
50 Megan T. Baldridge, Timothy J. Nice, Broc T. McCune1 Christine C.
Yokoyama, Amal Kambal, Michael Wheadon, Michael S. Diamond, Yulia Ivanova1, Maxim Artyomov, and Herbert W. Virgin. Commensal microbes and interferon-λ determine
persistence of enteric murine norovirus infection Science. 2015 January 16; 347(6219): 266– 269. doi:10.1126/science.1258025
51 Brown JR, Gilmour K, Breuer J. Norovirus infections occur in B cell deficient patients. Clin Infect Dis 2016; doi:10.1093/cid/ciw060.
52 Green. K. Y. Noroviruses and B Cells.Clinical Infectious Diseases Advance Access published March 2, 2016
53 Karst SM. Pathogenesis of noroviruses, emerging RNA viruses. Viruses. 2010;2: 748-781. doi: 10.3390/v2030748
54 Mohler J. Norovirus Gastroenteritis. 2007. N Engl J Med. 2009 October 29; 361(18): . doi:10.1056/NEJMra0804575.
55 Mumphrey SM, Changotra H, Moore TN, et al. Murine norovirus 1 infection is associated with histopathological changes in immunocompetent hosts, but clinical disease is prevented by STAT1-dependent interferon responses. J Virol 2007; 81:3251–3263.
56 Nordgren J, Sharma S, Kambhampati A, Lopman B, Svensson L (2016) Innate Resistance and Susceptibility to Norovirus Infection. PLoS Pathog 12(4): e1005385. doi:10.1371/journal.ppat.1005385NORDGREN et, al., 2016).
57 Payne DC, Vinje J, Szilagyi PG, et al. Norovirus and medically attended gastroenteritis in U.S. children. N Engl J Med 2013; 368:1121–30.
58 Atmar RL, Estes MK.Norovirus vaccine development: next steps. Expert Rev Vaccines 2012; 11:1023–5.
59 Lopman B. Air sickness: vomiting and environmental transmissionof norovirus on aircraft. Clin Infect Dis 2011; 53: 521–522.
60 Bernstein. DI, Atmar. R L., Lyon G. M, Treanor J.J, Chen W.H, Jiang. X., Vinjé J, Gregoricus. N., Frenck Jr. R W, Moe C L., Al-Ibrahim M S., Barrett J., Ferreira J,. Estes M K, Graham D Y, Goodwin R, Borkowski A, Clemens. R, and Mendelman PM. Norovirus Vaccine Against Experimental Human GII.4 Virus Illness: A Challenge Study in Healthy Adults. J. Infect. Dis. 2015;211: 870-878.
61 Timo Vesikari, Vesna Blazevic. Norovirus vaccine: one step closer. Journal of Infectious Diseases Advance Access published September 9, 2014
62 Kitajima M, Oka T, Tohya Y, Katayama H, Takeda N, Katayama K.
Development of a broadly reactive nested reverse transcription-PCR assay to detect murine noroviruses, and investigation of the prevalence of murine noroviruses in laboratory mice in Japan. Microbiol Immunol. 2009;53: 531-534. doi: 10.1111/j.1348-0421.2009.00152.x
63 Livingston RS, Riley LK. Diagnostic testing of mouse and rat colonies for infectious agents. Lab Anim (NY). 2003;32: 44-51. doi: 10.1038/laban0503-44
64 Farkas T, Fey B, Keller G, Martella V, Egyed L. Molecular detection of murine noroviruses in laboratory and wild mice. Vet Microbiol. 2012;160: 463-467. doi:
10.1016/j.vetmic.2012.06.002
65 Tsunesumi N, Sato G, Iwasa M, Kabeya H, Maruyama S, Tohya Y. Novel murine norovirus-like genes in wild rodents in Japan. J Vet Med Sci. 2012;74: 1221-1224. doi.org/10.1292/jvms. 12-0106.
66 Smith DB, McFadden N, Blundell RJ, Meredith A, Simmonds P. Diversity of murine norovirus in wild-rodent populations: species-specific associations suggest an ancient divergence. J Gen Virol. 2012;93: 259-266. doi: 10.1099/vir.0.036392-0
67 Tse H, Chan WM, Lam CS, Lau SK, Woo PC, Yuen KY. Complete genome sequences of novel rat noroviruses in Hong Kong. J Virol. 2012;86: 12435-12436. doi: 10.1128/JVI.01976-12
68 Rodrigues, D. M. Infecção por Cardiovirus (Vírus da Encefalomielite murina de Theiler – TMEV) em colônias convencionais de ratos. Mestrado em Genética e Biologia
Molecular, Área de Microbiologia. Instituto de Biologia, Universidade Estadual de Campinas, 138p., 2003.
69 Gonzalez-Hernandez MB, Bragazzi CJ, Wobus CE. Plaque assay for murine norovirus. J Vis Exp. 2012 Aug 22;(66):e4297. doi: 10.3791/4297.
70 Hall T.: Bioedit: a user friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acid Symp. 1999;41: 95-98.
doi:10.1234/12345678
71 Gillioli, R. Avaliação do perfil sanitário de colônias de camundongos e de ratos em biotérios brasileiros: ocorrência de bactérias, parasitas e vírus murino. Tese de Doutorado em Genética e Biologia Molecular, Área de Microbiologia. Instituto de Biologia, Universidade Estadual de Campinas, 138p., 2003.
72 Kraft, V.; Meyer, B. Diagnosis of murine infections in relation to test methods employed. Lab. Animal Science, v.36 (3), p. 271-276, 1986.
73 Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol. 2013;30: 2725-2729.
74 Green, K. Y., R. M. Chanock, and A. Z. Kapikian. 2001. Human
caliciviruses,p. 841–874. In D. M. Knipe and P. M. Howley (ed.), Fields virology, 4th ed. Lippincott Williams & Wilkins, Philadelphia, Pa.
75 Patel MM, Hall AJ, Vinje J, Parashar UD. Noroviruses: a comprehensive review. J Clin Virol. 2009;44: 1-8. doi: 10.1016/j.jcv.2008.10.009
76 Duizer E, van Duynhoven Y, Vennema H, Koopmans M. Failure to detect norovirus in a large group of asymptomatic individuals by Marshall et al. (Public Health Vol 118 (3) 230-233). Public Health. 2004;118: 455-456. doi: 10.1016/j.puhe.2004.07.001
77 Lay MK, Atmar RL, Guix S, Bharadwaj U, He H, Neill FH, Sastry KJ, Yao Q, Estes MK. Norwalk virus does not replicate in human macrophages or dendritic cells derived from the peripheral blood of susceptible humans. Virology. 2010;406:1–11.
78 Moser MJ, DiFrancesco RA, Gowda K, Klingele AJ, Sugar DR, Stocki S, et al. Thermostable DNA polymerase from a viral metagenome is a potent RT-PCR enzyme. PLoS One. 2012;7: e38371. doi: 10.1371/journal.pone.0038371
79 Gonzalez-Hernandez MB, Liu T, Blanco LP, Auble H, Payne HC, Wobus CE. Murine Norovirus Transcytosis across an In Vitro Polarized Murine Intestinal Epithelial Monolayer Is Mediated by M-Like Cells. J Virol. 2013;87:12685–12693.
80 Gonzalez-Hernandez MB, Liu T, Payne HC, Stencel-Baerenwald J, Ikizler M, Yagita H, Dermody TS, Williams IR, Wobus CE. Efficient norovirus and reovirus replication in the mouse intestine requires microfold (M) cells. J Virol JVI. 2014:00204–14.
81 Farkas T, Fey B, Keller G, Martella V, Egyed L. Molecular detection of murine noroviruses in laboratory and wild mice. Vet Microbiol. 2012;160: 463-467. doi:
10.1016/j.vetmic.2012.06.002
82 Pang X, Lee BE. Laboratory diagnosis of noroviruses: present and future. Clin Lab Med. 2015;35: 345-362. doi: 10.1016/j.cll.2015.02.008
83 Hanaki K, Ike F, Kajita A, Yasuno W, Yanagiba M, Goto M, et al. A broadly reactive one-step SYBR Green I real-time RT-PCR assay for rapid detection of murine norovirus. PLoS One. 2014;9: e98108. doi: 10.1371/journal.pone.0098108
84 Obara M, Hasegawa S, Iwai M, Horimoto E, Nakamura K, Kurata T, et al. Single base substitutions in the capsid region of the norovirus genome during viral shedding in cases of infection in areas where norovirus infection is endemic. J Clin Microbiol. 2008;46: 3397-3403. doi: 10.1128/JCM.01932-07
85 Muller B, Klemm U, Mas Marques A, Schreier E. Genetic diversity and recombination of murine noroviruses in immunocompromised mice. Arch Virol. 2007;152: 1709-1719. doi: 10.1007/s00705-007-0989-y
86 Ferragut F, Vega CG, Mauroy A, Conceicao-Neto N, Zeller M, Heylen E, et al. Molecular detection of bovine Noroviruses in Argentinean dairy calves: Circulation of a tentative new genotype. Infect Genet Evol. 2016;40: 144-150. doi:
10.1016/j.meegid.2016.02.034
87 Compton SR, Riley LK. Detection of infectious Agents in Laboratory Rodents: Traditiona and Molecular Techniques. AALAS 2001. Vol 51, n2, pag 113-119.l
88 Paik J, Fierce Y, Drivdahl R, Treuting PM, Seamons A, Brabb T, Maggio-Price L. 2010. Effects of murine norovirus infection on a mouse model of diet-induced obesity and insulin resistance. Comp Med 60:189–195.
89 Paik J, Fierce Y, Mai PO, Phelps SR, McDonald T, Treuting P, Drivdahl R, Brabb T, LeBoeuf R, O’Brien KD, Maggio-Price L. 2011. Murine norovirus increases atherosclerotic lesion size and macrophages in Ldlr−/− mice. Comp Med 61:330–338.
90 Paik J, Kwork F, Seamons A, Brabb T, Kim J, Sullivan B, Hsu C, O' Brien KD, , Maggio-Price L. 2015. Effects of Murine Norovirus on Atherosclerosis in Ldlr–/– Mice Depends on the Timing of Infection. Comp Med 65: 114-122.
91 Mahabir E, Bauer B, and Schmidt J. Rodent and Germplasm Trafficking: Risks of Microbial Contamination in a High-Tech Biomedical World. ILAR Journal. vol49, n3, 2008.
92 Raspa M , Mahabir E, Fray M , Volland R, Scavizz F. Lack of transmission of murine norovirus to mice via in vitro fertilization, intracytoplasmic sperm injection, and ovary transplantation. Theriogenology 86 (2016) 579–588.
93 FELASA working group on revision of guidelines for health monitoring of rodents and rabbits, Mahler Convenor M, Berard M, Feinstein R, Gallagher A, Illgen-Wilcke B, et al. FELASA recommendations for the health monitoring of mouse, rat, hamster, guinea pig and rabbit colonies in breeding and experimental units. Lab Anim. 2014;48: 178-192. doi: 10.1177/0023677213516312