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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Published inPLoS neglected tropical diseases Vol. 15; no. 9; p. e0009768
Main Authors 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
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 01.09.2021
Public Library of Science (PLoS)
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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.
AbstractList 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.
Background 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. Methods 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. Results 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. Conclusions 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.
BackgroundPteropine 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.MethodsEgyptian 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.ResultsAn 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.ConclusionsA 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.
Background 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. Methods 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. Results 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. Conclusions 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.
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.BACKGROUNDPteropine 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.METHODSEgyptian 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.RESULTSAn 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.CONCLUSIONSA 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.
Pteropine orthoreovirus (PRV) is a causative agent of acute respiratory illness in humans in tropical and sub-tropical regions in Southeast Asia. PRVs have been originally isolated from fruit bats, and it is assumed that PRVs spread to humans by both bat-to-human and human-to-human transmission. Recently, an PRV was also detected from a fruit bat in the Afrotropical region and might potentially cause an emerging infection of the bat-borne zoonotic virus in Africa. However, little is known about the prevalence of PRV infection in Africa. In this study, we demonstrated the high prevalence of PRV infection in bat populations in Zambia and isolated a new strain of PRV from Egyptian fruit bats. In addition, we found that the bat-derived PRV strain had lower pathogenicity in mice than a human-derived PRV strain isolated from a patient in Southeast Asia. Our findings provide new epidemiological information about PRV in fruit bats in the Afrotropical region and indicate the first isolation of an PRV strain that may cause attenuated infection in humans.
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.
Audience Academic
Author Qiu, Yongjin
Simulundu, Edgar
Taniguchi, Satoshi
Saijo, Masayuki
Sasaki, Michihito
Takada, Ayato
Wastika, Christida E.
Changula, Katendi
Mori-Kajihara, Akina
Eto, Yoshiki
Okuya, Kosuke
Sato, Akihiko
Orba, Yasuko
Yamaguchi, Tomoyuki
Kajihara, Masahiro
Sawa, Hirofumi
Hang’ombe, Bernard M.
Harima, Hayato
AuthorAffiliation 9 Drug Discovery & Disease Research Laboratory, Shionogi & Co., Ltd., Osaka, Japan
11 Africa Center of Excellence for Infectious Diseases of Humans and Animals, the University of Zambia, Lusaka, Zambia
3 International Collaboration Unit, Research Center for Zoonosis Control, Hokkaido University, Sapporo, Japan
4 Division of Global Epidemiology, Research Center for Zoonosis Control, Hokkaido University, Sapporo, Japan
13 One Health Research Center, Hokkaido University, Sapporo, Japan
8 Division of Bioresources, Research Center for Zoonosis Control, Hokkaido University, Sapporo, Japan
5 Department of Para-clinical Studies, School of Veterinary Medicine, the University of Zambia, Lusaka, Zambia
12 Global Virus Network, Baltimore, Maryland, United States of America
6 Department of Disease Control, School of Veterinary Medicine, the University of Zambia, Lusaka, Zambia
2 Division of Molecular Pathobiology, Research Center for Zoonosis Control, Hokkaido University, Sapporo, Japan
Colorado State Univer
AuthorAffiliation_xml – name: 11 Africa Center of Excellence for Infectious Diseases of Humans and Animals, the University of Zambia, Lusaka, Zambia
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– name: 2 Division of Molecular Pathobiology, Research Center for Zoonosis Control, Hokkaido University, Sapporo, Japan
– name: 5 Department of Para-clinical Studies, School of Veterinary Medicine, the University of Zambia, Lusaka, Zambia
– name: 10 Department of Virology I, National Institute of Infectious Diseases, Shinjuku, Tokyo, Japan
– name: Colorado State University, UNITED STATES
– name: 1 Hokudai Center for Zoonosis Control in Zambia, Research Center for Zoonosis Control, Hokkaido University, Sapporo, Japan
– name: 6 Department of Disease Control, School of Veterinary Medicine, the University of Zambia, Lusaka, Zambia
– name: 8 Division of Bioresources, Research Center for Zoonosis Control, Hokkaido University, Sapporo, Japan
– name: 9 Drug Discovery & Disease Research Laboratory, Shionogi & Co., Ltd., Osaka, Japan
– name: 7 Macha Research Trust, Choma, Zambia
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– name: 13 One Health Research Center, Hokkaido University, Sapporo, Japan
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  surname: Orba
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  surname: Kajihara
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  surname: Yamaguchi
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  givenname: Yoshiki
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  surname: Eto
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– sequence: 12
  givenname: Akina
  surname: Mori-Kajihara
  fullname: Mori-Kajihara, Akina
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  givenname: Akihiko
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  surname: Sato
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  givenname: Satoshi
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  surname: Taniguchi
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  surname: Hang’ombe
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– sequence: 18
  givenname: Hirofumi
  orcidid: 0000-0003-2569-2755
  surname: Sawa
  fullname: Sawa, Hirofumi
BackLink https://www.ncbi.nlm.nih.gov/pubmed/34492038$$D View this record in MEDLINE/PubMed
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– notice: 2021 Harima et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
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Snippet Pteropine orthoreovirus (PRV) is an emerging bat-borne zoonotic virus that causes severe respiratory illness in humans. Although PRVs have been identified in...
Background Pteropine orthoreovirus (PRV) is an emerging bat-borne zoonotic virus that causes severe respiratory illness in humans. Although PRVs have been...
Pteropine orthoreovirus (PRV) is a causative agent of acute respiratory illness in humans in tropical and sub-tropical regions in Southeast Asia. PRVs have...
BackgroundPteropine orthoreovirus (PRV) is an emerging bat-borne zoonotic virus that causes severe respiratory illness in humans. Although PRVs have been...
Background Pteropine orthoreovirus (PRV) is an emerging bat-borne zoonotic virus that causes severe respiratory illness in humans. Although PRVs have been...
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SubjectTerms 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
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Title Attenuated infection by a Pteropine orthoreovirus isolated from an Egyptian fruit bat in Zambia
URI https://www.ncbi.nlm.nih.gov/pubmed/34492038
https://www.proquest.com/docview/2582585393
https://www.proquest.com/docview/2570375427
https://pubmed.ncbi.nlm.nih.gov/PMC8448348
https://doaj.org/article/0eac1e1367d64eb8ac15fd685e9c3f21
http://dx.doi.org/10.1371/journal.pntd.0009768
Volume 15
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