The First Case of Bovine Astrovirus-Associated Encephalitis in the Southern Hemisphere (Uruguay), Uncovers Evidence of Viral Introduction to the Americas From Europe

Astrovirus species members of the Mamastrovirus genus (family Astroviridae) have been increasingly recognized as neuroinvasive pathogens in various mammals, including humans, mink, cattle, sheep, and pigs. While cases of astrovirus-associated encephalitis have been reported in North America, Europe,...

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Main Authors: Federico Giannitti, Rubén Darío Caffarena, Patricia Pesavento, Francisco Alejandro Uzal, Leticia Maya, Martín Fraga, Rodney Colina, Matías Castells
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-06-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2019.01240/full
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author Federico Giannitti
Rubén Darío Caffarena
Rubén Darío Caffarena
Patricia Pesavento
Francisco Alejandro Uzal
Leticia Maya
Martín Fraga
Rodney Colina
Matías Castells
Matías Castells
author_facet Federico Giannitti
Rubén Darío Caffarena
Rubén Darío Caffarena
Patricia Pesavento
Francisco Alejandro Uzal
Leticia Maya
Martín Fraga
Rodney Colina
Matías Castells
Matías Castells
author_sort Federico Giannitti
collection DOAJ
description Astrovirus species members of the Mamastrovirus genus (family Astroviridae) have been increasingly recognized as neuroinvasive pathogens in various mammals, including humans, mink, cattle, sheep, and pigs. While cases of astrovirus-associated encephalitis have been reported in North America, Europe, and Asia, their presence has never been documented in the Southern hemisphere. This paper describes a case of astrovirus-associated encephalitis in cattle in Uruguay that broadens the geographic distribution and genetic diversity of neuroinvasive astroviruses and provides phylogeographic evidence of viral introduction to the Americas from Europe. A 22-month-old Holstein steer from a farm in Colonia Department, Uruguay developed progressive neurological signs over a 3-days period before dying. Histopathological examination of the brain and proximal cervical spinal cord revealed disseminated, moderate to severe lymphocytic, histiocytic, and plasmacytic poliomeningoencephalomyelitis with neuronal necrosis. A Mamastrovirus strain in the CH13/NeuroS1 clade, that we called bovine astrovirus (BoAstV)-Neuro-Uy, was identified by reverse transcriptase PCR followed by nearly complete genome sequencing. Additionally, BoAstV was detected intralesionally in the brain by chromogenic RNA in situ hybridization within neuronal perikarya, axons and dendrites. Phylogenetic analysis of BoAstV-Neuro-Uy revealed a close relationship to neurotropic BoAstVs within the Virginia/Human-Mink-Ovine clade, which contains a growing cadre of neuroinvasive astroviruses. Analyzing the complete coding region of neuroinvasive BoAstVs sequences available in GenBank, we estimated an evolutionary rate of 4.27 × 10-4 (95% HPD 2.19–6.46 × 10-4) nucleotide substitutions/site/year. Phylogeographic analysis suggests that the common viral ancestor circulated in Europe between 1794–1940, and was introduced in Uruguay between 1849–1967, to later spread to North America and Japan.
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spelling doaj.art-f2f443ba09d8442e9b448442b780bce22022-12-21T17:30:56ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2019-06-011010.3389/fmicb.2019.01240461598The First Case of Bovine Astrovirus-Associated Encephalitis in the Southern Hemisphere (Uruguay), Uncovers Evidence of Viral Introduction to the Americas From EuropeFederico Giannitti0Rubén Darío Caffarena1Rubén Darío Caffarena2Patricia Pesavento3Francisco Alejandro Uzal4Leticia Maya5Martín Fraga6Rodney Colina7Matías Castells8Matías Castells9Instituto Nacional de Investigación Agropecuaria (INIA), Plataforma de Investigación en Salud Animal, Estación Experimental INIA La Estanzuela, Colonia, UruguayInstituto Nacional de Investigación Agropecuaria (INIA), Plataforma de Investigación en Salud Animal, Estación Experimental INIA La Estanzuela, Colonia, UruguayFacultad de Veterinaria, Universidad de la República, Montevideo, UruguayPathology, Microbiology and Immunology Department, School of Veterinary Medicine, University of California, Davis, Davis, CA, United StatesPathology, Microbiology and Immunology Department, School of Veterinary Medicine, University of California, Davis, Davis, CA, United StatesLaboratorio de Virología Molecular, Centro Universitario Regional (CENUR) Litoral Norte, Universidad de la República, Salto, UruguayInstituto Nacional de Investigación Agropecuaria (INIA), Plataforma de Investigación en Salud Animal, Estación Experimental INIA La Estanzuela, Colonia, UruguayLaboratorio de Virología Molecular, Centro Universitario Regional (CENUR) Litoral Norte, Universidad de la República, Salto, UruguayInstituto Nacional de Investigación Agropecuaria (INIA), Plataforma de Investigación en Salud Animal, Estación Experimental INIA La Estanzuela, Colonia, UruguayLaboratorio de Virología Molecular, Centro Universitario Regional (CENUR) Litoral Norte, Universidad de la República, Salto, UruguayAstrovirus species members of the Mamastrovirus genus (family Astroviridae) have been increasingly recognized as neuroinvasive pathogens in various mammals, including humans, mink, cattle, sheep, and pigs. While cases of astrovirus-associated encephalitis have been reported in North America, Europe, and Asia, their presence has never been documented in the Southern hemisphere. This paper describes a case of astrovirus-associated encephalitis in cattle in Uruguay that broadens the geographic distribution and genetic diversity of neuroinvasive astroviruses and provides phylogeographic evidence of viral introduction to the Americas from Europe. A 22-month-old Holstein steer from a farm in Colonia Department, Uruguay developed progressive neurological signs over a 3-days period before dying. Histopathological examination of the brain and proximal cervical spinal cord revealed disseminated, moderate to severe lymphocytic, histiocytic, and plasmacytic poliomeningoencephalomyelitis with neuronal necrosis. A Mamastrovirus strain in the CH13/NeuroS1 clade, that we called bovine astrovirus (BoAstV)-Neuro-Uy, was identified by reverse transcriptase PCR followed by nearly complete genome sequencing. Additionally, BoAstV was detected intralesionally in the brain by chromogenic RNA in situ hybridization within neuronal perikarya, axons and dendrites. Phylogenetic analysis of BoAstV-Neuro-Uy revealed a close relationship to neurotropic BoAstVs within the Virginia/Human-Mink-Ovine clade, which contains a growing cadre of neuroinvasive astroviruses. Analyzing the complete coding region of neuroinvasive BoAstVs sequences available in GenBank, we estimated an evolutionary rate of 4.27 × 10-4 (95% HPD 2.19–6.46 × 10-4) nucleotide substitutions/site/year. Phylogeographic analysis suggests that the common viral ancestor circulated in Europe between 1794–1940, and was introduced in Uruguay between 1849–1967, to later spread to North America and Japan.https://www.frontiersin.org/article/10.3389/fmicb.2019.01240/fullbovine astroviruscattleencephalitisinfectious diseasesMamastrovirusphylogeography
spellingShingle Federico Giannitti
Rubén Darío Caffarena
Rubén Darío Caffarena
Patricia Pesavento
Francisco Alejandro Uzal
Leticia Maya
Martín Fraga
Rodney Colina
Matías Castells
Matías Castells
The First Case of Bovine Astrovirus-Associated Encephalitis in the Southern Hemisphere (Uruguay), Uncovers Evidence of Viral Introduction to the Americas From Europe
Frontiers in Microbiology
bovine astrovirus
cattle
encephalitis
infectious diseases
Mamastrovirus
phylogeography
title The First Case of Bovine Astrovirus-Associated Encephalitis in the Southern Hemisphere (Uruguay), Uncovers Evidence of Viral Introduction to the Americas From Europe
title_full The First Case of Bovine Astrovirus-Associated Encephalitis in the Southern Hemisphere (Uruguay), Uncovers Evidence of Viral Introduction to the Americas From Europe
title_fullStr The First Case of Bovine Astrovirus-Associated Encephalitis in the Southern Hemisphere (Uruguay), Uncovers Evidence of Viral Introduction to the Americas From Europe
title_full_unstemmed The First Case of Bovine Astrovirus-Associated Encephalitis in the Southern Hemisphere (Uruguay), Uncovers Evidence of Viral Introduction to the Americas From Europe
title_short The First Case of Bovine Astrovirus-Associated Encephalitis in the Southern Hemisphere (Uruguay), Uncovers Evidence of Viral Introduction to the Americas From Europe
title_sort first case of bovine astrovirus associated encephalitis in the southern hemisphere uruguay uncovers evidence of viral introduction to the americas from europe
topic bovine astrovirus
cattle
encephalitis
infectious diseases
Mamastrovirus
phylogeography
url https://www.frontiersin.org/article/10.3389/fmicb.2019.01240/full
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