Attenuated infection by a Pteropine orthoreovirus isolated from an Egyptian fruit bat in Zambia

Pteropine orthoreovirus (PRV) is an emerging bat-borne zoonotic virus that causes severe respiratory illness in humans. Although PRVs have been identified in fruit bats and humans in Australia and Asia, little is known about the prevalence of PRV infection in Africa. Therefore, this study performed...

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Veröffentlicht in:PLoS neglected tropical diseases 2021-09, Vol.15 (9), p.e0009768-e0009768
Hauptverfasser: Harima, Hayato, Sasaki, Michihito, Orba, Yasuko, Okuya, Kosuke, Qiu, Yongjin, Wastika, Christida E, Changula, Katendi, Kajihara, Masahiro, Simulundu, Edgar, Yamaguchi, Tomoyuki, Eto, Yoshiki, Mori-Kajihara, Akina, Sato, Akihiko, Taniguchi, Satoshi, Takada, Ayato, Saijo, Masayuki, Hang'ombe, Bernard M, Sawa, Hirofumi
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container_issue 9
container_start_page e0009768
container_title PLoS neglected tropical diseases
container_volume 15
creator Harima, Hayato
Sasaki, Michihito
Orba, Yasuko
Okuya, Kosuke
Qiu, Yongjin
Wastika, Christida E
Changula, Katendi
Kajihara, Masahiro
Simulundu, Edgar
Yamaguchi, Tomoyuki
Eto, Yoshiki
Mori-Kajihara, Akina
Sato, Akihiko
Taniguchi, Satoshi
Takada, Ayato
Saijo, Masayuki
Hang'ombe, Bernard M
Sawa, Hirofumi
description Pteropine orthoreovirus (PRV) is an emerging bat-borne zoonotic virus that causes severe respiratory illness in humans. Although PRVs have been identified in fruit bats and humans in Australia and Asia, little is known about the prevalence of PRV infection in Africa. Therefore, this study performed an PRV surveillance in fruit bats in Zambia. Egyptian fruit bats (Rousettus aegyptiacus, n = 47) and straw-colored fruit bats (Eidolon helvum, n = 33) captured in Zambia in 2017-2018 were screened for PRV infection using RT-PCR and serum neutralization tests. The complete genome sequence of an isolated PRV strain was determined by next generation sequencing and subjected to BLAST and phylogenetic analyses. Replication capacity and pathogenicity of the strain were investigated using Vero E6 cell cultures and BALB/c mice, respectively. An PRV strain, tentatively named Nachunsulwe-57, was isolated from one Egyptian fruit bat. Serological assays demonstrated that 98% of sera (69/70) collected from Egyptian fruit bats (n = 37) and straw-colored fruit bats (n = 33) had neutralizing antibodies against PRV. Genetic analyses revealed that all 10 genome segments of Nachunsulwe-57 were closely related to a bat-derived Kasama strain found in Uganda. Nachunsulwe-57 showed less efficiency in viral growth and lower pathogenicity in mice than another PRV strain, Miyazaki-Bali/2007, isolated from a patient. A high proportion of Egyptian fruit bats and straw-colored fruit bats were found to be seropositive to PRV in Zambia. Importantly, a new PRV strain (Nachunsulwe-57) was isolated from an Egyptian fruit bat in Zambia, which had relatively weak pathogenicity in mice. Taken together, our findings provide new epidemiological insights about PRV infection in bats and indicate the first isolation of an PRV strain that may have low pathogenicity to humans.
doi_str_mv 10.1371/journal.pntd.0009768
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Although PRVs have been identified in fruit bats and humans in Australia and Asia, little is known about the prevalence of PRV infection in Africa. Therefore, this study performed an PRV surveillance in fruit bats in Zambia. Egyptian fruit bats (Rousettus aegyptiacus, n = 47) and straw-colored fruit bats (Eidolon helvum, n = 33) captured in Zambia in 2017-2018 were screened for PRV infection using RT-PCR and serum neutralization tests. The complete genome sequence of an isolated PRV strain was determined by next generation sequencing and subjected to BLAST and phylogenetic analyses. Replication capacity and pathogenicity of the strain were investigated using Vero E6 cell cultures and BALB/c mice, respectively. An PRV strain, tentatively named Nachunsulwe-57, was isolated from one Egyptian fruit bat. Serological assays demonstrated that 98% of sera (69/70) collected from Egyptian fruit bats (n = 37) and straw-colored fruit bats (n = 33) had neutralizing antibodies against PRV. Genetic analyses revealed that all 10 genome segments of Nachunsulwe-57 were closely related to a bat-derived Kasama strain found in Uganda. Nachunsulwe-57 showed less efficiency in viral growth and lower pathogenicity in mice than another PRV strain, Miyazaki-Bali/2007, isolated from a patient. A high proportion of Egyptian fruit bats and straw-colored fruit bats were found to be seropositive to PRV in Zambia. Importantly, a new PRV strain (Nachunsulwe-57) was isolated from an Egyptian fruit bat in Zambia, which had relatively weak pathogenicity in mice. Taken together, our findings provide new epidemiological insights about PRV infection in bats and indicate the first isolation of an PRV strain that may have low pathogenicity to humans.</description><identifier>ISSN: 1935-2735</identifier><identifier>ISSN: 1935-2727</identifier><identifier>EISSN: 1935-2735</identifier><identifier>DOI: 10.1371/journal.pntd.0009768</identifier><identifier>PMID: 34492038</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Adsorption ; Animals ; Animals as carriers of disease ; Antibodies ; Bats ; Biology and Life Sciences ; Causes of ; Chiroptera ; Chiroptera - virology ; Chlorocebus aethiops ; Colon ; Colour ; Epidemiology ; Fruits ; Genetic analysis ; Genomes ; Health aspects ; Identification and classification ; Illnesses ; Infections ; Medicine and Health Sciences ; Mice ; Mice, Inbred BALB C ; Microbiological strains ; National parks ; Neutralization ; Next-generation sequencing ; Nucleotide sequence ; Orthoreovirus - isolation &amp; purification ; Pathogenicity ; Pathogens ; Patients ; PCR ; People and Places ; Phylogeny ; Polymerase chain reaction ; Public health ; Reoviridae Infections - epidemiology ; Reoviridae Infections - veterinary ; Reoviridae Infections - virology ; Reoviruses ; Research and Analysis Methods ; Respiratory diseases ; Respiratory disorders ; Risk factors ; RNA polymerase ; RNA virus infections ; Serum ; Statistics ; Strain ; Strain analysis ; Straw ; Tourism ; Tropical diseases ; Vero Cells ; Viruses ; Zambia - epidemiology ; Zoonoses</subject><ispartof>PLoS neglected tropical diseases, 2021-09, Vol.15 (9), p.e0009768-e0009768</ispartof><rights>COPYRIGHT 2021 Public Library of Science</rights><rights>2021 Harima et al. 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Genetic analyses revealed that all 10 genome segments of Nachunsulwe-57 were closely related to a bat-derived Kasama strain found in Uganda. Nachunsulwe-57 showed less efficiency in viral growth and lower pathogenicity in mice than another PRV strain, Miyazaki-Bali/2007, isolated from a patient. A high proportion of Egyptian fruit bats and straw-colored fruit bats were found to be seropositive to PRV in Zambia. Importantly, a new PRV strain (Nachunsulwe-57) was isolated from an Egyptian fruit bat in Zambia, which had relatively weak pathogenicity in mice. 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Sasaki, Michihito ; Orba, Yasuko ; Okuya, Kosuke ; Qiu, Yongjin ; Wastika, Christida E ; Changula, Katendi ; Kajihara, Masahiro ; Simulundu, Edgar ; Yamaguchi, Tomoyuki ; Eto, Yoshiki ; Mori-Kajihara, Akina ; Sato, Akihiko ; Taniguchi, Satoshi ; Takada, Ayato ; Saijo, Masayuki ; Hang'ombe, Bernard M ; Sawa, Hirofumi</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c734t-8b2da80cfeb4761289599cab6cf6bfb8e4aa43ca0352cd54466f9a76acc09c273</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Adsorption</topic><topic>Animals</topic><topic>Animals as carriers of disease</topic><topic>Antibodies</topic><topic>Bats</topic><topic>Biology and Life Sciences</topic><topic>Causes of</topic><topic>Chiroptera</topic><topic>Chiroptera - virology</topic><topic>Chlorocebus aethiops</topic><topic>Colon</topic><topic>Colour</topic><topic>Epidemiology</topic><topic>Fruits</topic><topic>Genetic analysis</topic><topic>Genomes</topic><topic>Health aspects</topic><topic>Identification and classification</topic><topic>Illnesses</topic><topic>Infections</topic><topic>Medicine and Health Sciences</topic><topic>Mice</topic><topic>Mice, Inbred BALB C</topic><topic>Microbiological strains</topic><topic>National parks</topic><topic>Neutralization</topic><topic>Next-generation sequencing</topic><topic>Nucleotide sequence</topic><topic>Orthoreovirus - isolation &amp; 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Fisheries Abstracts (ASFA) 1: Biological Sciences &amp; Living Resources</collection><collection>Aquatic Science &amp; Fisheries Abstracts (ASFA) 3: Aquatic Pollution &amp; Environmental Quality</collection><collection>ProQuest Health &amp; Medical Complete (Alumni)</collection><collection>Aquatic Science &amp; Fisheries Abstracts (ASFA) Professional</collection><collection>Health &amp; Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS neglected tropical diseases</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Harima, Hayato</au><au>Sasaki, Michihito</au><au>Orba, Yasuko</au><au>Okuya, Kosuke</au><au>Qiu, Yongjin</au><au>Wastika, Christida E</au><au>Changula, Katendi</au><au>Kajihara, Masahiro</au><au>Simulundu, Edgar</au><au>Yamaguchi, Tomoyuki</au><au>Eto, Yoshiki</au><au>Mori-Kajihara, Akina</au><au>Sato, Akihiko</au><au>Taniguchi, Satoshi</au><au>Takada, Ayato</au><au>Saijo, Masayuki</au><au>Hang'ombe, Bernard M</au><au>Sawa, Hirofumi</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Attenuated infection by a Pteropine orthoreovirus isolated from an Egyptian fruit bat in Zambia</atitle><jtitle>PLoS neglected tropical diseases</jtitle><addtitle>PLoS Negl Trop Dis</addtitle><date>2021-09-01</date><risdate>2021</risdate><volume>15</volume><issue>9</issue><spage>e0009768</spage><epage>e0009768</epage><pages>e0009768-e0009768</pages><issn>1935-2735</issn><issn>1935-2727</issn><eissn>1935-2735</eissn><abstract>Pteropine orthoreovirus (PRV) is an emerging bat-borne zoonotic virus that causes severe respiratory illness in humans. Although PRVs have been identified in fruit bats and humans in Australia and Asia, little is known about the prevalence of PRV infection in Africa. Therefore, this study performed an PRV surveillance in fruit bats in Zambia. Egyptian fruit bats (Rousettus aegyptiacus, n = 47) and straw-colored fruit bats (Eidolon helvum, n = 33) captured in Zambia in 2017-2018 were screened for PRV infection using RT-PCR and serum neutralization tests. The complete genome sequence of an isolated PRV strain was determined by next generation sequencing and subjected to BLAST and phylogenetic analyses. Replication capacity and pathogenicity of the strain were investigated using Vero E6 cell cultures and BALB/c mice, respectively. An PRV strain, tentatively named Nachunsulwe-57, was isolated from one Egyptian fruit bat. Serological assays demonstrated that 98% of sera (69/70) collected from Egyptian fruit bats (n = 37) and straw-colored fruit bats (n = 33) had neutralizing antibodies against PRV. Genetic analyses revealed that all 10 genome segments of Nachunsulwe-57 were closely related to a bat-derived Kasama strain found in Uganda. Nachunsulwe-57 showed less efficiency in viral growth and lower pathogenicity in mice than another PRV strain, Miyazaki-Bali/2007, isolated from a patient. A high proportion of Egyptian fruit bats and straw-colored fruit bats were found to be seropositive to PRV in Zambia. Importantly, a new PRV strain (Nachunsulwe-57) was isolated from an Egyptian fruit bat in Zambia, which had relatively weak pathogenicity in mice. Taken together, our findings provide new epidemiological insights about PRV infection in bats and indicate the first isolation of an PRV strain that may have low pathogenicity to humans.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>34492038</pmid><doi>10.1371/journal.pntd.0009768</doi><orcidid>https://orcid.org/0000-0002-7987-9884</orcidid><orcidid>https://orcid.org/0000-0003-2569-2755</orcidid><orcidid>https://orcid.org/0000-0001-8621-5472</orcidid><orcidid>https://orcid.org/0000-0002-2066-1979</orcidid><orcidid>https://orcid.org/0000-0001-9478-0439</orcidid><orcidid>https://orcid.org/0000-0001-9423-0816</orcidid><orcidid>https://orcid.org/0000-0002-4201-6401</orcidid><orcidid>https://orcid.org/0000-0003-4921-7860</orcidid><orcidid>https://orcid.org/0000-0003-1607-2175</orcidid><orcidid>https://orcid.org/0000-0001-6190-428X</orcidid><orcidid>https://orcid.org/0000-0003-2182-4319</orcidid><orcidid>https://orcid.org/0000-0003-1875-7223</orcidid><orcidid>https://orcid.org/0000-0001-6625-1679</orcidid><orcidid>https://orcid.org/0000-0001-5458-7298</orcidid><orcidid>https://orcid.org/0000-0003-2464-6642</orcidid><orcidid>https://orcid.org/0000-0001-9910-3912</orcidid><oa>free_for_read</oa></addata></record>
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identifier ISSN: 1935-2735
ispartof PLoS neglected tropical diseases, 2021-09, Vol.15 (9), p.e0009768-e0009768
issn 1935-2735
1935-2727
1935-2735
language eng
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source MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; PubMed Central Open Access; Public Library of Science (PLoS)
subjects Adsorption
Animals
Animals as carriers of disease
Antibodies
Bats
Biology and Life Sciences
Causes of
Chiroptera
Chiroptera - virology
Chlorocebus aethiops
Colon
Colour
Epidemiology
Fruits
Genetic analysis
Genomes
Health aspects
Identification and classification
Illnesses
Infections
Medicine and Health Sciences
Mice
Mice, Inbred BALB C
Microbiological strains
National parks
Neutralization
Next-generation sequencing
Nucleotide sequence
Orthoreovirus - isolation & purification
Pathogenicity
Pathogens
Patients
PCR
People and Places
Phylogeny
Polymerase chain reaction
Public health
Reoviridae Infections - epidemiology
Reoviridae Infections - veterinary
Reoviridae Infections - virology
Reoviruses
Research and Analysis Methods
Respiratory diseases
Respiratory disorders
Risk factors
RNA polymerase
RNA virus infections
Serum
Statistics
Strain
Strain analysis
Straw
Tourism
Tropical diseases
Vero Cells
Viruses
Zambia - epidemiology
Zoonoses
title Attenuated infection by a Pteropine orthoreovirus isolated from an Egyptian fruit bat in Zambia
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