Retrospective Investigation in Horses with Encephalitis Reveals Unnoticed Circulation of West Nile Virus in Brazil
Abstract
:1. Introduction
2. Materials and Methods
2.1. Ethical Statement
2.2. Sample Collection and RNA Isolation
2.3. cDNA and Multiplex Sequencing PCR Procedures
2.4. Library Preparation and Viral Whole-Genome Nanopore Sequencing
2.5. WNV Lineage Classification
2.6. Phylogenetic and Bayesian Analysis
3. Results
4. Discussion
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Fall, G.; Di Paola, N.; Faye, M.; Dia, M.; de Melo Freire, C.C.; Loucoubar, C.; de Andrade Zanotto, P.M.; Faye, O.; Sall, A.A. Biological and phylogenetic characteristics of West African lineages of West Nile virus. PLoS Negl. Trop. Dis. 2017, 11, e0006078. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hughes, T.P.; Paul, J.H.; Smithburn, K.C.; Burke, A.W. A Neurotropic Virus Isolated from the Blood of a Native of Uganda. Am. J. Trop. Med. Hyg. 1940, 20, 471–492. [Google Scholar] [CrossRef]
- Morales, M.A.; Barrandeguy, M.; Fabbri, C.; Garcia, J.B.; Vissani, A.; Trono, K.; Gutierrez, G.; Pigretti, S.; Menchaca, H.; Garrido, N.; et al. West Nile virus isolation from equines in Argentina. Emerg. Infect. Dis. 2006, 12, 1559–1561. [Google Scholar] [CrossRef] [PubMed]
- Osorio, J.E.; Carrillo, L.; Ciuoderis, K.A.; Murphy, D.; Hofmeister, E.; Piedrahita, L.D.; LeVasseur, J.; Ocampo, M.C.; Lopera, J.G. Characterization of West Nile viruses isolated from captive American Flamingoes (Phoenicopterus ruber) in Medellin, Colombia. Am. J. Trop. Med. Hyg. 2012, 87, 565–572. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Campbell, G.L.; Staples, J.E.; Sejvar, J.J.; Fischer, M. West nile virus disease. In Netter’s Infectious Diseases; Elsevier: Amsterdam, The Netherlands, 2012; pp. 554–559. [Google Scholar]
- Bunning, M.L.; Bowen, R.A.; Cropp, C.B.; Sullivan, K.G.; Davis, B.S.; Komar, N.; Godsey, M.S.; Baker, D.; Hettler, D.L.; Holmes, D.A.; et al. Experimental infection of horses with West Nile virus. Emerg. Infect. Dis. 2002, 8, 380–386. [Google Scholar] [CrossRef] [PubMed]
- Hayes, E.B.; Sejvar, J.J.; Zaki, S.R.; Lanciotti, R.S.; Bode, A.V.; Campbell, G.L. Virology, pathology, and clinical manifestations of West Nile virus disease. Emerg. Infect. Dis. 2005, 11, 1174–1179. [Google Scholar] [CrossRef]
- Kramer, L.D.; Li, J.; Shi, P.-Y. West Nile virus. Lancet Neurol. 2007, 6, 171–181. [Google Scholar] [CrossRef]
- Morel, A.P.; Webster, A.; Zitelli, L.C.; Umeno, K.; Souza, U.A.; Prusch, F.; Anicet, M.; Marsicano, G.; Bandarra, P.; Trainini, G.; et al. Serosurvey of West Nile virus (WNV) in free-ranging raptors from Brazil. Braz. J. Microbiol. 2021, 52, 411–418. [Google Scholar] [CrossRef]
- Silva, A.S.G.; Matos, A.C.D.; da Cunha, M.A.C.R.; Rehfeld, I.S.; Galinari, G.C.F.; Marcelino, S.A.C.; Saraiva, L.H.G.; Martins, N.R.D.S.; Maranhão, R.D.P.A.; Lobato, Z.I.P.; et al. West Nile virus associated with equid encephalitis in Brazil, 2018. Transbound Emerg. Dis. 2019, 66, 445–453. [Google Scholar] [CrossRef] [Green Version]
- Silva, J.R.; de Medeiros, L.C.; dos Reis, V.P.; Chávez, J.H.; Munhoz, T.D.; Borges, G.P.; Soares, O.A.B.; de Campos, C.H.C.; Machado, R.Z.; Baldani, C.D.; et al. Serologic survey of West Nile virus in horses from Central-West, Northeast and Southeast Brazil. Mem. Inst. Oswaldo Cruz 2013, 108, 921–923. [Google Scholar] [CrossRef]
- Vieira, M.A.C.E.S.; Aguiar, A.d.A.X.; Borba, A.d.S.; Guimarães, H.C.L.; Eulálio, K.D.; de Albuquerque-Neto, L.L.; Salmito, M.d.A.; Lima, O.B. West Nile fever in Brazil: Sporadic case, silent endemic disease or epidemic in its initial stages? Rev. Inst. Med. Trop. Sao Paulo 2015, 57, 276. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vieira, M.A.C.S.; Romano, A.P.M.; Almeida-Neto, W.S.; Rodrigues, S.G.; Azevedo, R.S.S.; Eulálio, K.D.; Chiang, J.O.; Vasconcelos, P.F.C.; Silva, E.V.P.; Borba, A.S. West Nile virus encephalitis: The first human case recorded in Brazil. Am. J. Trop. Med. Hyg. 2015, 93, 377–379. [Google Scholar] [CrossRef] [PubMed]
- Weber, M.N.; Mosena, A.C.S.; Baumbach, L.F.; da Silva, M.S.; Canova, R.; Dos Santos, D.R.L.; da Budaszewski, R.F.; de Oliveira, L.V.; Soane, M.M.; Saraiva, N.B.; et al. Serologic evidence of West Nile virus and Saint Louis encephalitis virus in horses from Southern Brazil. Braz. J. Microbiol. 2021, 52, 1021–1027. [Google Scholar] [CrossRef] [PubMed]
- Pauvolid-Corrêa, A.; Campos, Z.; Juliano, R.; Velez, J.; Nogueira, R.M.R.; Komar, N. Serological evidence of widespread circulation of West Nile virus and other flaviviruses in equines of the Pantanal, Brazil. PLoS Negl. Trop. Dis. 2014, 8, e2706. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Melandri, V.; Guimarães, A.É.; Komar, N.; Nogueira, M.L.; Mondini, A.; Fernandez-Sesma, A.; Alencar, J.; Bosch, I. Serological detection of West Nile virus in horses and chicken from Pantanal, Brazil. Mem. Inst. Oswaldo Cruz 2012, 107, 1073–1075. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ometto, T.; Durigon, E.L.; de Araujo, J.; Aprelon, R.; de Aguiar, D.M.; Cavalcante, G.T.; Melo, R.M.; Levi, J.E.; de Azevedo Júnior, S.M.; Petry, M.V.; et al. West Nile virus surveillance, Brazil, 2008. Trans. R. Soc. Trop. Med. Hyg. 2013, 107, 723–730. [Google Scholar] [CrossRef]
- Martins, L.C.; da Silva, E.V.P.; Casseb, L.M.N.; da Silva, S.P.; Cruz, A.C.R.; Pantoja, J.A.d.S.; Medeiros, D.B.d.A.; Martins Filho, A.J.; da Cruz, E.d.R.M.; de Araújo, M.T.F.; et al. First isolation of West Nile virus in Brazil. Mem. Inst. Oswaldo Cruz 2019, 114, e180332. [Google Scholar] [CrossRef]
- Costa, É.A.; Giovanetti, M.; Silva Catenacci, L.; Fonseca, V.; Aburjaile, F.F.; Chalhoub, F.L.L.; Xavier, J.; Campos de Melo Iani, F.; da Cunha E Silva Vieira, M.A.; Freitas Henriques, D.; et al. West Nile virus in Brazil. Pathogens 2021, 10, 896. [Google Scholar] [CrossRef]
- Löwen Levy Chalhoub, F.; Maia de Queiroz, E., Jr.; Holanda Duarte, B.; Eielson Pinheiro de Sá, M.; Cerqueira Lima, P.; Carneiro de Oliveira, A.; Medeiros Neves Casseb, L.; Leal das Chagas, L.; Antônio de Oliveira Monteiro, H.; Sebastião Alberto Santos Neves, M.; et al. West Nile virus in the state of ceará, northeast Brazil. Microorganisms 2021, 9, 1699. [Google Scholar] [CrossRef]
- Quick, J.; Grubaugh, N.D.; Pullan, S.T.; Claro, I.M.; Smith, A.D.; Gangavarapu, K.; Oliveira, G.; Robles-Sikisaka, R.; Rogers, T.F.; Beutler, N.A.; et al. Multiplex PCR method for MinION and Illumina sequencing of Zika and other virus genomes directly from clinical samples. Nat. Protoc. 2017, 12, 1261–1276. [Google Scholar] [CrossRef] [Green Version]
- Vilsker, M.; Moosa, Y.; Nooij, S.; Fonseca, V.; Ghysens, Y.; Dumon, K.; Pauwels, R.; Alcantara, L.C.; Vanden Eynden, E.; Vandamme, A.-M.; et al. Genome Detective: An automated system for virus identification from high-throughput sequencing data. Bioinformatics 2019, 35, 871–873. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Katoh, K.; Rozewicki, J.; Yamada, K.D. MAFFT online service: Multiple sequence alignment, interactive sequence choice and visualization. Brief. Bioinform. 2019, 20, 1160–1166. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Larsson, A. AliView: A fast and lightweight alignment viewer and editor for large datasets. Bioinformatics 2014, 30, 3276–3278. [Google Scholar] [CrossRef] [PubMed]
- Nguyen, L.-T.; Schmidt, H.A.; von Haeseler, A.; Minh, B.Q. IQ-TREE: A fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 2015, 32, 268–274. [Google Scholar] [CrossRef]
- Darriba, D.; Taboada, G.L.; Doallo, R.; Posada, D. jModelTest 2: More models, new heuristics and parallel computing. Nat. Methods 2012, 9, 772. [Google Scholar] [CrossRef] [Green Version]
- Rambaut, A.; Lam, T.T.; Max Carvalho, L.; Pybus, O.G. Exploring the temporal structure of heterochronous sequences using TempEst (formerly Path-O-Gen). Virus Evol. 2016, 2, vew007. [Google Scholar] [CrossRef] [Green Version]
- Suchard, M.A.; Lemey, P.; Baele, G.; Ayres, D.L.; Drummond, A.J.; Rambaut, A. Bayesian phylogenetic and phylodynamic data integration using BEAST 1. Virus Evol. 2018, 4, vey016. [Google Scholar] [CrossRef] [Green Version]
- Rambaut, A.; Drummond, A.J.; Xie, D.; Baele, G.; Suchard, M.A. Posterior summarization in Bayesian phylogenetics using Tracer 1. Syst. Biol. 2018, 67, 901–904. [Google Scholar] [CrossRef] [Green Version]
- Vasconcelos, H.B.; Nunes, M.R.T.; Casseb, L.M.N.; Carvalho, V.L.; Pinto da Silva, E.V.; Silva, M.; Casseb, S.M.M.; Vasconcelos, P.F.C. Molecular epidemiology of Oropouche virus, Brazil. Emerg. Infect. Dis. 2011, 17, 800–806. [Google Scholar] [CrossRef]
- Mourão, M.P.G.; Bastos, M.d.S.; de Figueiredo, R.P.; Gimaque, J.B.L.; Galusso, E.d.S.; Kramer, V.M.; de Oliveira, C.M.C.; Naveca, F.G.; Figueiredo, L.T.M. Mayaro fever in the city of Manaus, Brazil, 2007. Vector Borne Zoonotic Dis. 2012, 12, 42–46. [Google Scholar] [CrossRef]
- Julia da Silva Pessoa Vieira, C.; José Ferreira da Silva, D.; Rigotti Kubiszeski, J.; Ceschini Machado, L.; Pena, L.J.; Vieira de Morais Bronzoni, R.; da Luz Wallau, G. The emergence of chikungunya ECSA lineage in a mayaro endemic region on the southern border of the amazon forest. Trop. Med. Infect. Dis. 2020, 5, 105. [Google Scholar] [CrossRef] [PubMed]
- Mota, M.T.d.O.; Terzian, A.C.; Silva, M.L.C.R.; Estofolete, C.; Nogueira, M.L. Mosquito-transmitted viruses—The great Brazilian challenge. Braz. J. Microbiol. 2016, 47, 38–50. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Moraes, M.M.; Kubiszeski, J.R.; Vieira, C.J.d.S.P.; Gusmao, A.F.; Pratis, T.S.; Colombo, T.E.; Thies, S.F.; do Carmo Araujo, F.; Zanelli, C.F.; Milhim, B.H.G.d.A.; et al. Detection of Saint Louis encephalitis virus in two Brazilian states. J. Med. Virol. 2022, 94, 776–781. [Google Scholar] [CrossRef] [PubMed]
- Giovanetti, M.; de Mendonça, M.C.L.; Fonseca, V.; Mares-Guia, M.A.; Fabri, A.; Xavier, J.; de Jesus, J.G.; Gräf, T.; Dos Santos Rodrigues, C.D.; Dos Santos, C.C.; et al. Yellow Fever Virus Reemergence and Spread in Southeast Brazil, 2016. J. Virol. 2019, 94, e01623-19. [Google Scholar] [CrossRef]
- Xavier, J.; Fonseca, V.; Bezerra, J.F.; do Monte Alves, M.; Mares-Guia, M.A.; Claro, I.M.; de Jesus, R.; Adelino, T.; Araújo, E.; Cavalcante, K.R.L.J.; et al. Chikungunya virus ECSA lineage reintroduction in the northeasternmost region of Brazil. Int. J. Infect. Dis. 2021, 105, 120–123. [Google Scholar] [CrossRef]
- Xavier, J.; Giovanetti, M.; Fonseca, V.; Thézé, J.; Gräf, T.; Fabri, A.; Goes de Jesus, J.; Lima de Mendonça, M.C.; Damasceno Dos Santos Rodrigues, C.; Mares-Guia, M.A.; et al. Circulation of chikungunya virus East/Central/South African lineage in Rio de Janeiro, Brazil. PLoS ONE 2019, 14, e0217871. [Google Scholar] [CrossRef]
- Goes de Jesus, J.; Gräf, T.; Giovanetti, M.; Mares-Guia, M.A.; Xavier, J.; Lima Maia, M.; Fonseca, V.; Fabri, A.; Dos Santos, R.F.; Mota Pereira, F.; et al. Yellow fever transmission in non-human primates, Bahia, Northeastern Brazil. PLoS Negl. Trop. Dis. 2020, 14, e0008405. [Google Scholar] [CrossRef]
- Adelino, T.É.R.; Giovanetti, M.; Fonseca, V.; Xavier, J.; de Abreu, Á.S.; do Nascimento, V.A.; Demarchi, L.H.F.; Oliveira, M.A.A.; da Silva, V.L.; de Mello, A.L.E.S.; et al. Field and classroom initiatives for portable sequence-based monitoring of dengue virus in Brazil. Nat. Commun. 2021, 12, 2296. [Google Scholar] [CrossRef]
- Costa, E.A.; Bayeux, J.J.M.; Silva, A.S.G.; De Queiroz, G.A.; Santos, B.S.Á.d.S.; Rocha, M.N.; Rehfeld, I.S.; Franklin, L.F.d.S.; Valle, L.B.; Guedes, M.I.M.C.; et al. Epidemiological surveillance of West Nile virus in the world and Brazil. Braz. J. Vet. Res. Anim. Sci. 2020, 56, e164335. [Google Scholar] [CrossRef] [Green Version]
- Pauvolid-Corrêa, A.; Morales, M.A.; Levis, S.; Figueiredo, L.T.M.; Couto-Lima, D.; Campos, Z.; Nogueira, M.F.; da Silva, E.E.; Nogueira, R.M.R.; Schatzmayr, H.G. Neutralising antibodies for West Nile virus in horses from Brazilian Pantanal. Mem. Inst. Oswaldo Cruz 2011, 106, 467–474. [Google Scholar] [CrossRef] [Green Version]
- Siconelli, M.J.L.; Jorge, D.M.d.M.; de Castro-Jorge, L.A.; Fonseca, A.A., Jr.; Nascimento, M.L.; Floriano, V.G.; de Souza, F.R.; de Queiroz, E.M., Jr.; Camargos, M.F.; Costa, E.D.L.; et al. Evidence for current circulation of an ancient West Nile virus strain (NY99) in Brazil. Rev. Soc. Bras. Med. Trop. 2021, 54, e0687-2020. [Google Scholar] [CrossRef] [PubMed]
- Ministério da Saúde, Secretaria de Vigilância em Saúde. Boletim Epidemiológico—Vigilância Sentinela das Doenças Neuroinvasivas por Arbovírus, Brasil, 2017 a 2019; Ministério da Saúde—Secretaria de Vigilância em Saúde: Brasília, Brazil, 2020. [Google Scholar]
- Ministério da Saúde. Boletim Epidemiológico—Monitoramento dos Casos de Arboviroses Urbanas Causados por Vírus Transmitidos Pelo mosquito Aedes (Dengue, Chikungunya e Zika), Semanas Epidemiológicas 1 a 7, 2022, vol.; Secretaria de Vigilância em Saúde: Brasília, Brazil, 2022. [Google Scholar]
- Ministério da Saúde. Boletim Epidemiológico—Monitoramento dos Casos de Arboviroses Urbanas Causados por Vírus Transmitidos Pelo Mosquito Aedes (Dengue, Chikungunya e Zika), Semanas Epidemiológicas 1 a 51, 2021, vol.; Secretaria de Vigilância em Saúde: Brasília, Brazil, 2021. [Google Scholar]
Acession Number | Lineage | Sample Type | Collection Date | State | Municipality | Sex | Age | Reads | Coverage (%) | Clinical Sign |
---|---|---|---|---|---|---|---|---|---|---|
ON782108 | 1a | Brain/Spinal cord | 21 April 2018 | Bahia | Itagibá | Female | 8 | 179,788 | 91.6 | NA |
ON782109 | 1a | Brain/Spinal cord | 22 July 2019 | Bahia | Ipirá | Male | 4 | 260,093 | 94.3 | NA |
ON782107 | 1a | Brain | 10 January 2019 | Ceará | Abaiara | Female | 4 | 290,093 | 88.9 | Neurologic disorder and neuromotor impairment |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Fritsch, H.; Pereira, F.M.; Costa, E.A.; Fonseca, V.; Tosta, S.; Xavier, J.; Levy, F.; Oliveira, C.d.; Menezes, G.; Lima, J.; et al. Retrospective Investigation in Horses with Encephalitis Reveals Unnoticed Circulation of West Nile Virus in Brazil. Viruses 2022, 14, 1540. https://doi.org/10.3390/v14071540
Fritsch H, Pereira FM, Costa EA, Fonseca V, Tosta S, Xavier J, Levy F, Oliveira Cd, Menezes G, Lima J, et al. Retrospective Investigation in Horses with Encephalitis Reveals Unnoticed Circulation of West Nile Virus in Brazil. Viruses. 2022; 14(7):1540. https://doi.org/10.3390/v14071540
Chicago/Turabian StyleFritsch, Hegger, Felicidade Mota Pereira, Erica Azevedo Costa, Vagner Fonseca, Stephane Tosta, Joilson Xavier, Flavia Levy, Carla de Oliveira, Gabriela Menezes, Jaqueline Lima, and et al. 2022. "Retrospective Investigation in Horses with Encephalitis Reveals Unnoticed Circulation of West Nile Virus in Brazil" Viruses 14, no. 7: 1540. https://doi.org/10.3390/v14071540
APA StyleFritsch, H., Pereira, F. M., Costa, E. A., Fonseca, V., Tosta, S., Xavier, J., Levy, F., Oliveira, C. d., Menezes, G., Lima, J., Santos, L., Silva, L., Nardy, V., Astete, M. K. G., Santos, B. S. Á. d. S., Aguiar, N. R., Guedes, M. I. M. C., Faria, G. C. d., Furtini, R., ... Alcantara, L. C. J. (2022). Retrospective Investigation in Horses with Encephalitis Reveals Unnoticed Circulation of West Nile Virus in Brazil. Viruses, 14(7), 1540. https://doi.org/10.3390/v14071540