Coronaviruses Detected in Bats in Close Contact with Humans in Rwanda
Identifieur interne : 000044 ( Pmc/Corpus ); précédent : 000043; suivant : 000045Coronaviruses Detected in Bats in Close Contact with Humans in Rwanda
Auteurs : Julius Nziza ; Tracey Goldstein ; Mike Cranfield ; Paul Webala ; Olivier Nsengimana ; Thierry Nyatanyi ; Antoine Mudakikwa ; Alexandre Tremeau-Bravard ; Dennis Byarugaba ; Jean Claude Tumushime ; Ivan Emil Mwikarago ; Isidore Gafarasi ; Jonna Mazet ; Kirsten GilardiSource :
- Ecohealth [ 1612-9202 ] ; 2019.
Abstract
Bats living in close contact with people in Rwanda were tested for evidence of infection with viruses of zoonotic potential. Mucosal swabs from 503 bats representing 17 species were sampled from 2010 to 2014 and screened by consensus PCR for 11 viral families. Samples were negative for all viral families except coronaviruses, which were detected in 27 bats belonging to eight species. Known coronaviruses detected included the betacorona viruses: Kenya bat coronaviruses, Eidolon bat coronavirus, and Bat coronavirus HKU9, as well as an alphacoronavirus, Chaerephon Bat coronavirus. Novel coronaviruses included two betacorona viruses clustering with SARS-CoV, a 2d coronavirus, and an alphacoronavirus.
Url:
DOI: 10.1007/s10393-019-01458-8
PubMed: 30756276
PubMed Central: 7088394
Links to Exploration step
PMC:7088394Le document en format XML
<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Coronaviruses Detected in Bats in Close Contact with Humans in Rwanda</title><author><name sortKey="Nziza, Julius" sort="Nziza, Julius" uniqKey="Nziza J" first="Julius" last="Nziza">Julius Nziza</name><affiliation><nlm:aff id="Aff1">Gorilla Doctors, P.O. Box 115, Musanze, Rwanda</nlm:aff></affiliation></author><author><name sortKey="Goldstein, Tracey" sort="Goldstein, Tracey" uniqKey="Goldstein T" first="Tracey" last="Goldstein">Tracey Goldstein</name><affiliation><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="GRID">grid.27860.3b</institution-id><institution-id institution-id-type="ISNI">0000 0004 1936 9684</institution-id><institution>Karen C. Drayer Wildlife Health Center, One Health Institute, School of Veterinary Medicine,</institution><institution>University of California Davis,</institution></institution-wrap>Davis, CA USA</nlm:aff></affiliation></author><author><name sortKey="Cranfield, Mike" sort="Cranfield, Mike" uniqKey="Cranfield M" first="Mike" last="Cranfield">Mike Cranfield</name><affiliation><nlm:aff id="Aff1">Gorilla Doctors, P.O. Box 115, Musanze, Rwanda</nlm:aff></affiliation></author><author><name sortKey="Webala, Paul" sort="Webala, Paul" uniqKey="Webala P" first="Paul" last="Webala">Paul Webala</name><affiliation><nlm:aff id="Aff3"><institution-wrap><institution-id institution-id-type="GRID">grid.449040.d</institution-id><institution>Department of Forestry and Wildlife Management,</institution><institution>Maasai Mara University,</institution></institution-wrap>P.O. Box 861, Narok, 20500 Kenya</nlm:aff></affiliation></author><author><name sortKey="Nsengimana, Olivier" sort="Nsengimana, Olivier" uniqKey="Nsengimana O" first="Olivier" last="Nsengimana">Olivier Nsengimana</name><affiliation><nlm:aff id="Aff4">Rwanda Wildlife Conservation Association, P.O. Box 5427, Kigali, Rwanda</nlm:aff></affiliation></author><author><name sortKey="Nyatanyi, Thierry" sort="Nyatanyi, Thierry" uniqKey="Nyatanyi T" first="Thierry" last="Nyatanyi">Thierry Nyatanyi</name><affiliation><nlm:aff id="Aff5"><institution-wrap><institution-id institution-id-type="GRID">grid.38142.3c</institution-id><institution-id institution-id-type="ISNI">000000041936754X</institution-id><institution>Department of Global Health and Social Medicine, School of Medicine,</institution><institution>Harvard University,</institution></institution-wrap>Boston, USA</nlm:aff></affiliation></author><author><name sortKey="Mudakikwa, Antoine" sort="Mudakikwa, Antoine" uniqKey="Mudakikwa A" first="Antoine" last="Mudakikwa">Antoine Mudakikwa</name><affiliation><nlm:aff id="Aff6">Rwanda Development Board, P.O. Box 6932, Kigali, Rwanda</nlm:aff></affiliation></author><author><name sortKey="Tremeau Bravard, Alexandre" sort="Tremeau Bravard, Alexandre" uniqKey="Tremeau Bravard A" first="Alexandre" last="Tremeau-Bravard">Alexandre Tremeau-Bravard</name><affiliation><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="GRID">grid.27860.3b</institution-id><institution-id institution-id-type="ISNI">0000 0004 1936 9684</institution-id><institution>Karen C. Drayer Wildlife Health Center, One Health Institute, School of Veterinary Medicine,</institution><institution>University of California Davis,</institution></institution-wrap>Davis, CA USA</nlm:aff></affiliation></author><author><name sortKey="Byarugaba, Dennis" sort="Byarugaba, Dennis" uniqKey="Byarugaba D" first="Dennis" last="Byarugaba">Dennis Byarugaba</name><affiliation><nlm:aff id="Aff7"><institution-wrap><institution-id institution-id-type="GRID">grid.11194.3c</institution-id><institution-id institution-id-type="ISNI">0000 0004 0620 0548</institution-id><institution>Makerere University Walter Reed Project, College of Veterinary Medicine, Animal Resources and Biosecurity,</institution><institution>Makerere University,</institution></institution-wrap>Kampala, Uganda</nlm:aff></affiliation></author><author><name sortKey="Tumushime, Jean Claude" sort="Tumushime, Jean Claude" uniqKey="Tumushime J" first="Jean Claude" last="Tumushime">Jean Claude Tumushime</name><affiliation><nlm:aff id="Aff1">Gorilla Doctors, P.O. Box 115, Musanze, Rwanda</nlm:aff></affiliation></author><author><name sortKey="Mwikarago, Ivan Emil" sort="Mwikarago, Ivan Emil" uniqKey="Mwikarago I" first="Ivan Emil" last="Mwikarago">Ivan Emil Mwikarago</name><affiliation><nlm:aff id="Aff8"><institution-wrap><institution-id institution-id-type="GRID">grid.452755.4</institution-id><institution-id institution-id-type="ISNI">0000 0004 0563 1469</institution-id><institution>National Reference Laboratory,</institution><institution>Rwanda Biomedical Center,</institution></institution-wrap>P.O. Box 83, Kigali, Rwanda</nlm:aff></affiliation></author><author><name sortKey="Gafarasi, Isidore" sort="Gafarasi, Isidore" uniqKey="Gafarasi I" first="Isidore" last="Gafarasi">Isidore Gafarasi</name><affiliation><nlm:aff id="Aff9"><institution-wrap><institution-id institution-id-type="GRID">grid.463563.1</institution-id><institution>Rwanda Agriculture Board,</institution></institution-wrap>P.O. Box 5016, Kigali, Rwanda</nlm:aff></affiliation></author><author><name sortKey="Mazet, Jonna" sort="Mazet, Jonna" uniqKey="Mazet J" first="Jonna" last="Mazet">Jonna Mazet</name><affiliation><nlm:aff id="Aff1">Gorilla Doctors, P.O. Box 115, Musanze, Rwanda</nlm:aff></affiliation><affiliation><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="GRID">grid.27860.3b</institution-id><institution-id institution-id-type="ISNI">0000 0004 1936 9684</institution-id><institution>Karen C. Drayer Wildlife Health Center, One Health Institute, School of Veterinary Medicine,</institution><institution>University of California Davis,</institution></institution-wrap>Davis, CA USA</nlm:aff></affiliation></author><author><name sortKey="Gilardi, Kirsten" sort="Gilardi, Kirsten" uniqKey="Gilardi K" first="Kirsten" last="Gilardi">Kirsten Gilardi</name><affiliation><nlm:aff id="Aff1">Gorilla Doctors, P.O. Box 115, Musanze, Rwanda</nlm:aff></affiliation><affiliation><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="GRID">grid.27860.3b</institution-id><institution-id institution-id-type="ISNI">0000 0004 1936 9684</institution-id><institution>Karen C. Drayer Wildlife Health Center, One Health Institute, School of Veterinary Medicine,</institution><institution>University of California Davis,</institution></institution-wrap>Davis, CA USA</nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">30756276</idno><idno type="pmc">7088394</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7088394</idno><idno type="RBID">PMC:7088394</idno><idno type="doi">10.1007/s10393-019-01458-8</idno><date when="2019">2019</date><idno type="wicri:Area/Pmc/Corpus">000044</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000044</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Coronaviruses Detected in Bats in Close Contact with Humans in Rwanda</title><author><name sortKey="Nziza, Julius" sort="Nziza, Julius" uniqKey="Nziza J" first="Julius" last="Nziza">Julius Nziza</name><affiliation><nlm:aff id="Aff1">Gorilla Doctors, P.O. Box 115, Musanze, Rwanda</nlm:aff></affiliation></author><author><name sortKey="Goldstein, Tracey" sort="Goldstein, Tracey" uniqKey="Goldstein T" first="Tracey" last="Goldstein">Tracey Goldstein</name><affiliation><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="GRID">grid.27860.3b</institution-id><institution-id institution-id-type="ISNI">0000 0004 1936 9684</institution-id><institution>Karen C. Drayer Wildlife Health Center, One Health Institute, School of Veterinary Medicine,</institution><institution>University of California Davis,</institution></institution-wrap>Davis, CA USA</nlm:aff></affiliation></author><author><name sortKey="Cranfield, Mike" sort="Cranfield, Mike" uniqKey="Cranfield M" first="Mike" last="Cranfield">Mike Cranfield</name><affiliation><nlm:aff id="Aff1">Gorilla Doctors, P.O. Box 115, Musanze, Rwanda</nlm:aff></affiliation></author><author><name sortKey="Webala, Paul" sort="Webala, Paul" uniqKey="Webala P" first="Paul" last="Webala">Paul Webala</name><affiliation><nlm:aff id="Aff3"><institution-wrap><institution-id institution-id-type="GRID">grid.449040.d</institution-id><institution>Department of Forestry and Wildlife Management,</institution><institution>Maasai Mara University,</institution></institution-wrap>P.O. Box 861, Narok, 20500 Kenya</nlm:aff></affiliation></author><author><name sortKey="Nsengimana, Olivier" sort="Nsengimana, Olivier" uniqKey="Nsengimana O" first="Olivier" last="Nsengimana">Olivier Nsengimana</name><affiliation><nlm:aff id="Aff4">Rwanda Wildlife Conservation Association, P.O. Box 5427, Kigali, Rwanda</nlm:aff></affiliation></author><author><name sortKey="Nyatanyi, Thierry" sort="Nyatanyi, Thierry" uniqKey="Nyatanyi T" first="Thierry" last="Nyatanyi">Thierry Nyatanyi</name><affiliation><nlm:aff id="Aff5"><institution-wrap><institution-id institution-id-type="GRID">grid.38142.3c</institution-id><institution-id institution-id-type="ISNI">000000041936754X</institution-id><institution>Department of Global Health and Social Medicine, School of Medicine,</institution><institution>Harvard University,</institution></institution-wrap>Boston, USA</nlm:aff></affiliation></author><author><name sortKey="Mudakikwa, Antoine" sort="Mudakikwa, Antoine" uniqKey="Mudakikwa A" first="Antoine" last="Mudakikwa">Antoine Mudakikwa</name><affiliation><nlm:aff id="Aff6">Rwanda Development Board, P.O. Box 6932, Kigali, Rwanda</nlm:aff></affiliation></author><author><name sortKey="Tremeau Bravard, Alexandre" sort="Tremeau Bravard, Alexandre" uniqKey="Tremeau Bravard A" first="Alexandre" last="Tremeau-Bravard">Alexandre Tremeau-Bravard</name><affiliation><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="GRID">grid.27860.3b</institution-id><institution-id institution-id-type="ISNI">0000 0004 1936 9684</institution-id><institution>Karen C. Drayer Wildlife Health Center, One Health Institute, School of Veterinary Medicine,</institution><institution>University of California Davis,</institution></institution-wrap>Davis, CA USA</nlm:aff></affiliation></author><author><name sortKey="Byarugaba, Dennis" sort="Byarugaba, Dennis" uniqKey="Byarugaba D" first="Dennis" last="Byarugaba">Dennis Byarugaba</name><affiliation><nlm:aff id="Aff7"><institution-wrap><institution-id institution-id-type="GRID">grid.11194.3c</institution-id><institution-id institution-id-type="ISNI">0000 0004 0620 0548</institution-id><institution>Makerere University Walter Reed Project, College of Veterinary Medicine, Animal Resources and Biosecurity,</institution><institution>Makerere University,</institution></institution-wrap>Kampala, Uganda</nlm:aff></affiliation></author><author><name sortKey="Tumushime, Jean Claude" sort="Tumushime, Jean Claude" uniqKey="Tumushime J" first="Jean Claude" last="Tumushime">Jean Claude Tumushime</name><affiliation><nlm:aff id="Aff1">Gorilla Doctors, P.O. Box 115, Musanze, Rwanda</nlm:aff></affiliation></author><author><name sortKey="Mwikarago, Ivan Emil" sort="Mwikarago, Ivan Emil" uniqKey="Mwikarago I" first="Ivan Emil" last="Mwikarago">Ivan Emil Mwikarago</name><affiliation><nlm:aff id="Aff8"><institution-wrap><institution-id institution-id-type="GRID">grid.452755.4</institution-id><institution-id institution-id-type="ISNI">0000 0004 0563 1469</institution-id><institution>National Reference Laboratory,</institution><institution>Rwanda Biomedical Center,</institution></institution-wrap>P.O. Box 83, Kigali, Rwanda</nlm:aff></affiliation></author><author><name sortKey="Gafarasi, Isidore" sort="Gafarasi, Isidore" uniqKey="Gafarasi I" first="Isidore" last="Gafarasi">Isidore Gafarasi</name><affiliation><nlm:aff id="Aff9"><institution-wrap><institution-id institution-id-type="GRID">grid.463563.1</institution-id><institution>Rwanda Agriculture Board,</institution></institution-wrap>P.O. Box 5016, Kigali, Rwanda</nlm:aff></affiliation></author><author><name sortKey="Mazet, Jonna" sort="Mazet, Jonna" uniqKey="Mazet J" first="Jonna" last="Mazet">Jonna Mazet</name><affiliation><nlm:aff id="Aff1">Gorilla Doctors, P.O. Box 115, Musanze, Rwanda</nlm:aff></affiliation><affiliation><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="GRID">grid.27860.3b</institution-id><institution-id institution-id-type="ISNI">0000 0004 1936 9684</institution-id><institution>Karen C. Drayer Wildlife Health Center, One Health Institute, School of Veterinary Medicine,</institution><institution>University of California Davis,</institution></institution-wrap>Davis, CA USA</nlm:aff></affiliation></author><author><name sortKey="Gilardi, Kirsten" sort="Gilardi, Kirsten" uniqKey="Gilardi K" first="Kirsten" last="Gilardi">Kirsten Gilardi</name><affiliation><nlm:aff id="Aff1">Gorilla Doctors, P.O. Box 115, Musanze, Rwanda</nlm:aff></affiliation><affiliation><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="GRID">grid.27860.3b</institution-id><institution-id institution-id-type="ISNI">0000 0004 1936 9684</institution-id><institution>Karen C. Drayer Wildlife Health Center, One Health Institute, School of Veterinary Medicine,</institution><institution>University of California Davis,</institution></institution-wrap>Davis, CA USA</nlm:aff></affiliation></author></analytic><series><title level="j">Ecohealth</title><idno type="ISSN">1612-9202</idno><idno type="eISSN">1612-9210</idno><imprint><date when="2019">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p id="Par1">Bats living in close contact with people in Rwanda were tested for evidence of infection with viruses of zoonotic potential. Mucosal swabs from 503 bats representing 17 species were sampled from 2010 to 2014 and screened by consensus PCR for 11 viral families. Samples were negative for all viral families except coronaviruses, which were detected in 27 bats belonging to eight species. Known coronaviruses detected included the betacorona viruses: Kenya bat coronaviruses, Eidolon bat coronavirus, and Bat coronavirus HKU9, as well as an alphacoronavirus, Chaerephon Bat coronavirus. Novel coronaviruses included two betacorona viruses clustering with SARS-CoV, a 2d coronavirus, and an alphacoronavirus.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Amman, Br" uniqKey="Amman B">BR Amman</name></author><author><name sortKey="Albari O, Cg" uniqKey="Albari O C">CG Albariño</name></author><author><name sortKey="Bird, Bh" uniqKey="Bird B">BH Bird</name></author><author><name sortKey="Nyakarahuka, L" uniqKey="Nyakarahuka L">L Nyakarahuka</name></author><author><name sortKey="Sealy, Tk" uniqKey="Sealy T">TK Sealy</name></author><author><name sortKey="Balinandi, S" uniqKey="Balinandi S">S Balinandi</name></author><author><name sortKey="Schuh, Aj" uniqKey="Schuh A">AJ Schuh</name></author><author><name sortKey="Campbell, Sm" uniqKey="Campbell S">SM Campbell</name></author><author><name sortKey="Stroher, U" uniqKey="Stroher U">U Ströher</name></author><author><name sortKey="Jones, Me" uniqKey="Jones M">ME 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Ecohealth</journal-id><journal-id journal-id-type="iso-abbrev">Ecohealth</journal-id><journal-title-group><journal-title>Ecohealth</journal-title></journal-title-group><issn pub-type="ppub">1612-9202</issn><issn pub-type="epub">1612-9210</issn><publisher><publisher-name>Springer US</publisher-name><publisher-loc>New York</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">30756276</article-id><article-id pub-id-type="pmc">7088394</article-id><article-id pub-id-type="publisher-id">1458</article-id><article-id pub-id-type="doi">10.1007/s10393-019-01458-8</article-id><article-categories><subj-group subj-group-type="heading"><subject>Short Communication</subject></subj-group></article-categories><title-group><article-title>Coronaviruses Detected in Bats in Close Contact with Humans in Rwanda</article-title></title-group><contrib-group><contrib contrib-type="author" corresp="yes"><name><surname>Nziza</surname><given-names>Julius</given-names></name><address><email>nzizavet@gmail.com</email><email>jnziza@gorilladoctors.org</email></address><xref ref-type="aff" rid="Aff1">1</xref></contrib><contrib contrib-type="author"><name><surname>Goldstein</surname><given-names>Tracey</given-names></name><xref ref-type="aff" rid="Aff2">2</xref></contrib><contrib contrib-type="author"><name><surname>Cranfield</surname><given-names>Mike</given-names></name><xref ref-type="aff" rid="Aff1">1</xref></contrib><contrib contrib-type="author"><name><surname>Webala</surname><given-names>Paul</given-names></name><xref ref-type="aff" rid="Aff3">3</xref></contrib><contrib contrib-type="author"><name><surname>Nsengimana</surname><given-names>Olivier</given-names></name><xref ref-type="aff" rid="Aff4">4</xref></contrib><contrib contrib-type="author"><name><surname>Nyatanyi</surname><given-names>Thierry</given-names></name><xref ref-type="aff" rid="Aff5">5</xref></contrib><contrib contrib-type="author"><name><surname>Mudakikwa</surname><given-names>Antoine</given-names></name><xref ref-type="aff" rid="Aff6">6</xref></contrib><contrib contrib-type="author"><name><surname>Tremeau-Bravard</surname><given-names>Alexandre</given-names></name><xref ref-type="aff" rid="Aff2">2</xref></contrib><contrib contrib-type="author"><name><surname>Byarugaba</surname><given-names>Dennis</given-names></name><xref ref-type="aff" rid="Aff7">7</xref></contrib><contrib contrib-type="author"><name><surname>Tumushime</surname><given-names>Jean Claude</given-names></name><xref ref-type="aff" rid="Aff1">1</xref></contrib><contrib contrib-type="author"><name><surname>Mwikarago</surname><given-names>Ivan Emil</given-names></name><xref ref-type="aff" rid="Aff8">8</xref></contrib><contrib contrib-type="author"><name><surname>Gafarasi</surname><given-names>Isidore</given-names></name><xref ref-type="aff" rid="Aff9">9</xref></contrib><contrib contrib-type="author"><name><surname>Mazet</surname><given-names>Jonna</given-names></name><xref ref-type="aff" rid="Aff1">1</xref><xref ref-type="aff" rid="Aff2">2</xref></contrib><contrib contrib-type="author"><name><surname>Gilardi</surname><given-names>Kirsten</given-names></name><xref ref-type="aff" rid="Aff1">1</xref><xref ref-type="aff" rid="Aff2">2</xref></contrib><aff id="Aff1"><label>1</label>Gorilla Doctors, P.O. Box 115, Musanze, Rwanda</aff><aff id="Aff2"><label>2</label><institution-wrap><institution-id institution-id-type="GRID">grid.27860.3b</institution-id><institution-id institution-id-type="ISNI">0000 0004 1936 9684</institution-id><institution>Karen C. Drayer Wildlife Health Center, One Health Institute, School of Veterinary Medicine,</institution><institution>University of California Davis,</institution></institution-wrap>Davis, CA USA</aff><aff id="Aff3"><label>3</label><institution-wrap><institution-id institution-id-type="GRID">grid.449040.d</institution-id><institution>Department of Forestry and Wildlife Management,</institution><institution>Maasai Mara University,</institution></institution-wrap>P.O. Box 861, Narok, 20500 Kenya</aff><aff id="Aff4"><label>4</label>Rwanda Wildlife Conservation Association, P.O. Box 5427, Kigali, Rwanda</aff><aff id="Aff5"><label>5</label><institution-wrap><institution-id institution-id-type="GRID">grid.38142.3c</institution-id><institution-id institution-id-type="ISNI">000000041936754X</institution-id><institution>Department of Global Health and Social Medicine, School of Medicine,</institution><institution>Harvard University,</institution></institution-wrap>Boston, USA</aff><aff id="Aff6"><label>6</label>Rwanda Development Board, P.O. Box 6932, Kigali, Rwanda</aff><aff id="Aff7"><label>7</label><institution-wrap><institution-id institution-id-type="GRID">grid.11194.3c</institution-id><institution-id institution-id-type="ISNI">0000 0004 0620 0548</institution-id><institution>Makerere University Walter Reed Project, College of Veterinary Medicine, Animal Resources and Biosecurity,</institution><institution>Makerere University,</institution></institution-wrap>Kampala, Uganda</aff><aff id="Aff8"><label>8</label><institution-wrap><institution-id institution-id-type="GRID">grid.452755.4</institution-id><institution-id institution-id-type="ISNI">0000 0004 0563 1469</institution-id><institution>National Reference Laboratory,</institution><institution>Rwanda Biomedical Center,</institution></institution-wrap>P.O. Box 83, Kigali, Rwanda</aff><aff id="Aff9"><label>9</label><institution-wrap><institution-id institution-id-type="GRID">grid.463563.1</institution-id><institution>Rwanda Agriculture Board,</institution></institution-wrap>P.O. Box 5016, Kigali, Rwanda</aff></contrib-group><pub-date pub-type="epub"><day>6</day><month>12</month><year>2019</year></pub-date><fpage>1</fpage><lpage>8</lpage><history><date date-type="received"><day>5</day><month>7</month><year>2019</year></date><date date-type="accepted"><day>10</day><month>11</month><year>2019</year></date></history><permissions><copyright-statement>© EcoHealth Alliance 2019</copyright-statement><license><license-p>This article is made available via the PMC Open Access Subset for unrestricted research re-use and secondary analysis in any form or by any means with acknowledgement of the original source. These permissions are granted for the duration of the World Health Organization (WHO) declaration of COVID-19 as a global pandemic.</license-p></license></permissions><abstract id="Abs1"><p id="Par1">Bats living in close contact with people in Rwanda were tested for evidence of infection with viruses of zoonotic potential. Mucosal swabs from 503 bats representing 17 species were sampled from 2010 to 2014 and screened by consensus PCR for 11 viral families. Samples were negative for all viral families except coronaviruses, which were detected in 27 bats belonging to eight species. Known coronaviruses detected included the betacorona viruses: Kenya bat coronaviruses, Eidolon bat coronavirus, and Bat coronavirus HKU9, as well as an alphacoronavirus, Chaerephon Bat coronavirus. Novel coronaviruses included two betacorona viruses clustering with SARS-CoV, a 2d coronavirus, and an alphacoronavirus.</p></abstract><kwd-group xml:lang="en"><title>Keywords</title><kwd>Rwanda</kwd><kwd>Bats</kwd><kwd>Coronaviruses</kwd><kwd>Human–wildlife interfaces</kwd></kwd-group></article-meta></front><body><sec id="Sec1"><title>Introduction</title><p id="Par2">Bats are natural reservoirs for a number of pathogens of public health concern (Plowright et al. <xref ref-type="bibr" rid="CR26">2015</xref>; Shi <xref ref-type="bibr" rid="CR33">2013</xref>). For example, in Southeast Asia, <italic>Pteropus</italic> fruit bats are the natural reservoirs of the zoonotic paramyxoviruses Hendra and Nipah (Chua et al. <xref ref-type="bibr" rid="CR9">2000</xref>). In 2002–2003, an epidemic of severe acute respiratory syndrome (SARS) caused by a novel coronavirus (SARS-CoV) emerged in China (Drosten et al. <xref ref-type="bibr" rid="CR13">2003</xref>, Ksiazek et al. <xref ref-type="bibr" rid="CR21">2003</xref>), and bats were determined to be natural reservoirs and the possible source of the virus (Ge et al. <xref ref-type="bibr" rid="CR14">2013</xref>; Lau et al. <xref ref-type="bibr" rid="CR22">2010</xref>). In 2012, a pathogenic paramyxovirus, Sosuga virus, which caused severe illness in a patient following contact with bats in Uganda, was subsequently detected in Egyptian fruit bats (<italic>Rousettus aegyptiacus</italic>) (Amman et al. <xref ref-type="bibr" rid="CR1">2015</xref>). In Africa, Egyptian fruit bats (<italic>R. aegyptiacus</italic>) are reservoirs of Marburg virus (Towner et al. <xref ref-type="bibr" rid="CR38">2008</xref>), and antibodies against Zaire ebola virus have been detected in the same species (Pourrut et al. <xref ref-type="bibr" rid="CR27">2009</xref>), while antibodies against <italic>Bombali ebolavirus</italic> have been detected in Little free-tailed bat (<italic>Chaerephon pumilus</italic>), Angolan free-tailed bat (<italic>Mops condylurus</italic>) (Goldstein et al. <xref ref-type="bibr" rid="CR16">2018</xref>).</p><p id="Par3">To assess the risk presented by human-bat contact, the USAID Emerging Pandemic Threats PREDICT project has been conducting viral surveillance in wildlife in more than 35 countries to detect viruses of zoonotic potential, including in Rwanda (<ext-link ext-link-type="uri" xlink:href="https://ohi.vetmed.ucdavis.edu/programs-projects/predict-project">https://ohi.vetmed.ucdavis.edu/programs-projects/predict-project</ext-link>).</p><p id="Par4">Rwanda is continental Africa’s most densely populated country (Butler <xref ref-type="bibr" rid="CR8">2004</xref>), and bats are frequently observed in/around urban centers and adjacent to wildlife protected areas. Ecotourism centered on mountain gorillas in Volcanoes National Park also drives tourism to the nearby bat roosting “Musanze Caves” (Spenceley et al. <xref ref-type="bibr" rid="CR34">2010</xref>; Joachim <xref ref-type="bibr" rid="CR18">2013</xref>).</p><p id="Par5">Between 2010 and 2014, biological sampling of bats was conducted at urban and rural sites in Rwanda characterized by an intense human–wildlife interface, including in and around Volcanoes National Park and the Musanze Caves. Anthropogenic activities around sampling sites were classified according to human livelihoods and activities, including ecotourism, crop farming, and national parks.</p><p id="Par6">A total of 503 bats belonging to 17 species were captured at 25 sites (Fig. <xref rid="Fig1" ref-type="fig">1</xref>) following established PREDICT protocols for bat capture and sampling (PREDICT <xref ref-type="bibr" rid="CR28">2017</xref>) (Table <xref rid="Tab1" ref-type="table">1</xref>). Following capture, bats were photographed, measured, and identified to species level as close as possible (Kingdon et al. <xref ref-type="bibr" rid="CR20">2013</xref>; Patterson and Webala <xref ref-type="bibr" rid="CR25">2012</xref>). Date, site name, season, apparent species, sex, age class (determined by the degree of epiphyseal-diaphyseal fusion) (Anthony <xref ref-type="bibr" rid="CR3">1988</xref>), reproductive status, and mass data were recorded. For handling and restraining larger fruit bats, light anesthesia was induced using inhalational isoflurane and oxygen (Fluriso™, Teva UK, Limited, Castleford, UK). Smaller fruit bats and insectivorous bats were physically restrained during sampling. All bats were released at the capture site within 3 h of capture.<fig id="Fig1"><label>Figure 1</label><caption><p>Coronaviruses phylogenetic analysis performed in Anthony et al. (<xref ref-type="bibr" rid="CR5">2017b</xref>). Sequences are collapsed into clades, representing operating taxonomic units (sequences sharing equal or more than 90%). The sequences included in this manuscript are indicated in the boxes.</p></caption><graphic xlink:href="10393_2019_1458_Fig1_HTML" id="MO1"></graphic></fig><table-wrap id="Tab1"><label>Table 1</label><caption><p>Bat Species Sampled at 25 Sites in Rwanda for 11 Viral Families, with Numbers and Percentages of Bats Testing Positive for CoV RNA.</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="left">Site no.*</th><th align="left">Species</th><th align="left">Risk interface</th><th align="left">Season</th><th align="left">Total tested (oral and rectal swabs)</th><th align="left">No. of positive</th><th align="left">% Positive</th></tr></thead><tbody><tr><td align="left">2</td><td align="left"><italic>Epomophorus labiatus</italic></td><td align="left">Homestead</td><td align="left">Rainy</td><td align="left">17</td><td align="left">0</td><td align="left">0</td></tr><tr><td align="left">25</td><td align="left"><italic>Mops condylurus</italic></td><td align="left">Homestead</td><td align="left">Rainy</td><td align="left">78</td><td align="left">0</td><td align="left">0</td></tr><tr><td align="left">18</td><td align="left">M. condylurus</td><td align="left">Homestead</td><td align="left">Dry</td><td align="left">20</td><td align="left">0</td><td align="left">0</td></tr><tr><td align="left" rowspan="4">12</td><td align="left"><italic>Hipposideros caffer</italic></td><td align="left">Ecotourism site</td><td align="left">Rainy</td><td align="left">15</td><td align="left">1</td><td align="left">7</td></tr><tr><td align="left"><italic>Rhinolophus clivosus</italic></td><td align="left">Ecotourism site</td><td align="left">Rainy</td><td align="left">19</td><td align="left">4</td><td align="left">21</td></tr><tr><td align="left"><italic>Rousettus aegyptiacus</italic></td><td align="left">Ecotourism site</td><td align="left">Rainy</td><td align="left">9</td><td align="left">0</td><td align="left">0</td></tr><tr><td align="left"><italic>Otomops martiensseni</italic></td><td align="left">Ecotourism site</td><td align="left">Rainy</td><td align="left">1</td><td align="left">0</td><td align="left">0</td></tr><tr><td align="left" rowspan="4">7</td><td align="left"><italic>R. clivosus</italic></td><td align="left">Ecotourism site</td><td align="left">Rainy</td><td align="left">5</td><td align="left">1</td><td align="left">20</td></tr><tr><td align="left"><italic>R. aegyptiacus</italic></td><td align="left">Ecotourism site</td><td align="left">Rainy</td><td align="left">13</td><td align="left">0</td><td align="left">0</td></tr><tr><td align="left"><italic>Hipposideros ruber</italic></td><td align="left">Ecotourism site</td><td align="left">Rainy</td><td align="left">2</td><td align="left">0</td><td align="left">0</td></tr><tr><td align="left"><italic>Nycteris hispida</italic></td><td align="left">Ecotourism site</td><td align="left">Rainy</td><td align="left">1</td><td align="left">0</td><td align="left">0</td></tr><tr><td align="left">3</td><td align="left"><italic>Eidolon helvum</italic></td><td align="left">Ecotourism site</td><td align="left">Rainy</td><td align="left">53</td><td align="left">4</td><td align="left">7,5</td></tr><tr><td align="left">16</td><td align="left"><italic>E. helvum</italic></td><td align="left">Homestead</td><td align="left">Dry</td><td align="left">15</td><td align="left">0</td><td align="left">0</td></tr><tr><td align="left">8</td><td align="left"><italic>E. helvum</italic></td><td align="left">Homestead</td><td align="left">Rainy</td><td align="left">9</td><td align="left">2</td><td align="left">22</td></tr><tr><td align="left">5</td><td align="left"><italic>E. helvum</italic></td><td align="left">Crop farming</td><td align="left">Rainy</td><td align="left">9</td><td align="left">6</td><td align="left">67</td></tr><tr><td align="left">6</td><td align="left"><italic>R. Aegyptiacus</italic></td><td align="left">Ecotourism site</td><td align="left">Rainy</td><td align="left">9</td><td align="left">2</td><td align="left">22</td></tr><tr><td align="left" rowspan="3">11</td><td align="left"><italic>Neoromicia tenuipinnis</italic></td><td align="left">National park</td><td align="left">Rainy</td><td align="left">5</td><td align="left">0</td><td align="left">0</td></tr><tr><td align="left"><italic>Myonicteris angolensis</italic></td><td align="left">National park</td><td align="left">Rainy</td><td align="left">6</td><td align="left">1</td><td align="left">17</td></tr><tr><td align="left"><italic>H. caffer</italic></td><td align="left">National park</td><td align="left">Rainy</td><td align="left">1</td><td align="left">0</td><td align="left">0</td></tr><tr><td align="left" rowspan="2">23</td><td align="left"><italic>Stenonycteris lanosus</italic></td><td align="left">National park</td><td align="left">Rainy</td><td align="left">1</td><td align="left">0</td><td align="left">0</td></tr><tr><td align="left"><italic>M. angolensis</italic></td><td align="left">National park</td><td align="left">Rainy</td><td align="left">23</td><td align="left">0</td><td align="left">0</td></tr><tr><td align="left" rowspan="3">10</td><td align="left"><italic>Epomophorus labiatus</italic></td><td align="left">Crop farming</td><td align="left">Rainy</td><td align="left">6</td><td align="left">0</td><td align="left">0</td></tr><tr><td align="left"><italic>S. lanosus</italic></td><td align="left">Crop farming</td><td align="left">Rainy</td><td align="left">5</td><td align="left">0</td><td align="left">0</td></tr><tr><td align="left"><italic>R. Aegyptiacus</italic></td><td align="left">Crop farming</td><td align="left">Dry</td><td align="left">5</td><td align="left">2</td><td align="left">40</td></tr><tr><td align="left">4</td><td align="left"><italic>E. helvum</italic></td><td align="left">Ecotourism site</td><td align="left">Rainy</td><td align="left">5</td><td align="left">1</td><td align="left">20</td></tr><tr><td align="left" rowspan="3">22</td><td align="left"><italic>N. hispida</italic></td><td align="left">Fishing area</td><td align="left">Rainy</td><td align="left">1</td><td align="left">0</td><td align="left">0</td></tr><tr><td align="left"><italic>E. Labiatus</italic></td><td align="left">Fishing area</td><td align="left">Rainy</td><td align="left">3</td><td align="left">0</td><td align="left">0</td></tr><tr><td align="left"><italic>Lavia frons</italic></td><td align="left">Fishing area</td><td align="left">Rainy</td><td align="left">1</td><td align="left">0</td><td align="left">0</td></tr><tr><td align="left" rowspan="2">21</td><td align="left"><italic>N. hispida</italic></td><td align="left">Ecotourism site</td><td align="left">Rainy</td><td align="left">1</td><td align="left">0</td><td align="left">0</td></tr><tr><td align="left"><italic>E. Labiatus</italic></td><td align="left">Ecotourism site</td><td align="left">Rainy</td><td align="left">2</td><td align="left">0</td><td align="left">0</td></tr><tr><td align="left">24</td><td align="left"><italic>M. condylurus</italic></td><td align="left">Homestead</td><td align="left">Rainy</td><td align="left">20</td><td align="left">0</td><td align="left">0</td></tr><tr><td align="left" rowspan="2">20</td><td align="left"><italic>Chaerephon pumilus</italic></td><td align="left">National park</td><td align="left">Rainy</td><td align="left">8</td><td align="left">0</td><td align="left">0</td></tr><tr><td align="left"><italic>M. condylurus</italic></td><td align="left">National park</td><td align="left">Rainy</td><td align="left">12</td><td align="left">0</td><td align="left">0</td></tr><tr><td align="left">9</td><td align="left"><italic>E. Labiatus</italic></td><td align="left">Homestead</td><td align="left">Rainy</td><td align="left">5</td><td align="left">0</td><td align="left">0</td></tr><tr><td align="left" rowspan="3">13</td><td align="left"><italic>E. Labiatus</italic></td><td align="left">Ecotourism site</td><td align="left">Rainy</td><td align="left">35</td><td align="left">0</td><td align="left">0</td></tr><tr><td align="left"><italic>N. tenuipinnis</italic></td><td align="left">Ecotourism site</td><td align="left">Rainy</td><td align="left">1</td><td align="left">0</td><td align="left">0</td></tr><tr><td align="left"><italic>Neoromicia cf. zuluensis\</italic></td><td align="left">Ecotourism site</td><td align="left">Rainy</td><td align="left">2</td><td align="left">0</td><td align="left">0</td></tr><tr><td align="left">17</td><td align="left"><italic>E. helvum</italic></td><td align="left">Homestead</td><td align="left">Rainy</td><td align="left">20</td><td align="left">0</td><td align="left">0</td></tr><tr><td align="left" rowspan="3">19</td><td align="left"><italic>Scotophilus viridis</italic></td><td align="left">Homestead</td><td align="left">Rainy</td><td align="left">4</td><td align="left">0</td><td align="left">0</td></tr><tr><td align="left"><italic>C. pumilus</italic></td><td align="left">Homestead</td><td align="left">Rainy</td><td align="left">3</td><td align="left">1</td><td align="left">33</td></tr><tr><td align="left"><italic>E. Labiatus</italic></td><td align="left">Homestead</td><td align="left">Rainy</td><td align="left">18</td><td align="left">0</td><td align="left">0</td></tr><tr><td align="left" rowspan="2">15</td><td align="left"><italic>E. Labiatus</italic></td><td align="left">Homestead</td><td align="left">Rainy</td><td align="left">2</td><td align="left">0</td><td align="left">0</td></tr><tr><td align="left"><italic>S. viridis</italic></td><td align="left">Homestead</td><td align="left">Rainy</td><td align="left">1</td><td align="left">0</td><td align="left">0</td></tr><tr><td align="left" rowspan="3">1</td><td align="left"><italic>M. Angolensis</italic></td><td align="left">Homestead</td><td align="left">Rainy</td><td align="left">16</td><td align="left">0</td><td align="left">0</td></tr><tr><td align="left"><italic>E. Labiatus</italic></td><td align="left">Homestead</td><td align="left">Rainy</td><td align="left">9</td><td align="left">1</td><td align="left">11</td></tr><tr><td align="left"><italic>S. viridis</italic></td><td align="left">Homestead</td><td align="left">Rainy</td><td align="left">1</td><td align="left">0</td><td align="left">0</td></tr><tr><td align="left">14</td><td align="left"><italic>N. hispida</italic></td><td align="left">Homestead</td><td align="left">Dry</td><td align="left">6</td><td align="left">0</td><td align="left">0</td></tr><tr><td align="left">Total</td><td align="left"></td><td align="left"></td><td align="left"></td><td align="left">503</td><td align="left">27</td><td align="left">54</td></tr></tbody></table><table-wrap-foot><p>*Bats sampling sites can be visualized in Figure <xref rid="Fig2" ref-type="fig">2</xref> by site number.</p></table-wrap-foot></table-wrap></p><p id="Par7">Sampling for viral family screening included collection oral and rectal mucosal or fecal swabs. Swabs were placed into viral transport media (BD Universal Viral Transport™ medium, Becton, Dickinson and Co., Sparks, Maryland) and NucliSENS Lysis Buffer (bioMerieux SA™, Marcy l’Etoile, France) and stored in liquid nitrogen for transport and transfer to a − 80 °C freezer.</p><p id="Par8">We extracted RNA from oral and rectal swab samples using the Qiamp Viral Mini kit™ (Qiagen Inc., Valencia, CA) and reverse transcribed into cDNA using SuperScript III™ (Invitrogen Corp, Carlsbad, CA). Primers targeting the housekeeping gene β-actin were used to ensure the presence of amplifiable nucleic acid in RNA extracts (Goldstein et al. <xref ref-type="bibr" rid="CR17">2004</xref>). Samples were screened by consensus PCR targeting conserved gene fragments using established assays know to detect corona (Quan et al. <xref ref-type="bibr" rid="CR29">2010</xref>; Watanabe et al. <xref ref-type="bibr" rid="CR41">2010</xref>), alpha (Sánchez-Seco et al. <xref ref-type="bibr" rid="CR32">2001</xref>), arena (Lozano et al. <xref ref-type="bibr" rid="CR23">1997</xref>), bunya (Briese et al. <xref ref-type="bibr" rid="CR7">2007</xref>), filo (Zhai et al. <xref ref-type="bibr" rid="CR43">2007</xref>), flavi (Moureau et al. <xref ref-type="bibr" rid="CR24">2007</xref>), hanta (Raboni et al. <xref ref-type="bibr" rid="CR30">2005</xref>), influenza (Anthony et al. <xref ref-type="bibr" rid="CR6">2012</xref>), paramyxo (Tong et al. <xref ref-type="bibr" rid="CR37">2008</xref>), lenti (Courgnaud et al. <xref ref-type="bibr" rid="CR10">2001</xref>), and rhabdo (Wray et al. <xref ref-type="bibr" rid="CR42">2016</xref>) viruses. Bands of the expected size were excised from 1% agarose and purified using the Qiaquick kit (Qiagen Inc.). Purified PCR products were cloned (pCR4-TOPO vector; Invitrogen Corp.) and sequenced (ABI 3730 Capillary Electrophoresis Genetic Analyzer; Applied Biosystems, Inc., Foster City, CA). Sequences were analyzed and edited using Geneious (Version 6.0.3) and compared with known sequences in the Genbank database. Species identification of PCR-positive individuals was confirmed by DNA bar coding of the cytochrome b (<italic>Cytb</italic>) and cytochrome oxidase subunit 1 (<italic>CO1</italic>) mitochondrial genes (Townzen et al. <xref ref-type="bibr" rid="CR39">2008</xref>). Fisher’s exact test was used to examine the association of viral positivity with age and season using STATA 13.0 software. The level of significance was set at <italic>P</italic> ≤ 0.05 (Raymond and Rousset <xref ref-type="bibr" rid="CR31">1995</xref>).</p><p id="Par9">No alpha, arena, bunya, filo, flavi, hanta, influenza, paramyxo, lenti, or rhabdo viruses were detected in oral or rectal swabs. Coronaviruses (CoV) were detected in 27 (5.4%) of the 503 bats sampled. Twenty-two of the 27 coronavirus positive bats belonged to three species: Straw-colored fruit bat (<italic>Eidolon helvum</italic>; 13 positives of 111 sampled, 11.7%), Geoffroy’s horseshoe bat (<italic>Rhinolophus clivosus</italic>; 5 of 24, 24.2%), and Egyptian fruit bat (<italic>Rousettus aegyptiacus;</italic> 4 of 36, 11.1%). Coronavirus positive bats were sampled at 11 different sites, including in the Musanze Caves (Table <xref rid="Tab1" ref-type="table">1</xref>). Subadult bats were more likely to be positive for CoV than adults (6/36 vs. 21/429; <italic>P </italic>= 0.04). No coronaviruses were detected in juvenile bats (<italic>n</italic> = 11). There were no observed differences between seasons (Dry/Rainy; 3/90 vs. 24/386; <italic>P</italic> = 0.445).</p><p id="Par10">Coronavirus sequences were classified as belonging to different viral species according to established cutoffs and methods (Anthony et al. <xref ref-type="bibr" rid="CR5">2017b</xref>). We detected four known coronaviruses (Table <xref rid="Tab2" ref-type="table">2</xref>) and four new coronaviruses (Table <xref rid="Tab3" ref-type="table">3</xref>; Fig. <xref rid="Fig1" ref-type="fig">1</xref>). One of the new betacoronaviruses, Coronavirus PREDICT_CoV-43, was detected in <italic>Hipposideros ruber</italic> and <italic>R. clivosus</italic> bats co-roosting in bat tourism caves (Site 10; Fig. <xref rid="Fig1" ref-type="fig">1</xref>; Table <xref rid="Tab3" ref-type="table">3</xref>). Comparison of the conserved polymerase gene fragment sequences to other known coronaviruses indicated that Coronavirus PREDICT_CoV-43 clustered near the SARS-like coronaviruses but suggests it may be a distinct virus based on the conserved fragment sequence, as it showed only 84% nucleotide similarity to SARS-CoV (Genbank accession no. NC_009694). The second new betacoronavirus, PREDICT_CoV-44, was detected in two <italic>Hipposideros caffer</italic> bats trapped in Nyungwe National Park (Site No. 11) and in a <italic>R</italic>. <italic>clivosus</italic> bat in tourism caves at Site No. 10 (Fig. <xref rid="Fig2" ref-type="fig">2</xref>). Although the conserved sequence fragment also clustered with other betacoronaviruses, it was quite divergent, showing only 79% nucleotide similarity to others in the group.<table-wrap id="Tab2"><label>Table 2</label><caption><p>Known Coronaviruses Detected in Bats by Species and Specimen Type.</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="left">Bat species</th><th align="left">c-PCR positive</th><th align="left">Sample tested</th><th align="left">Year of collection/season</th><th align="left">Site no</th><th align="left">Risk interface</th><th align="left">Virus name</th><th align="left">Genbank No.</th></tr></thead><tbody><tr><td align="left"><italic>Epomophorus labiatus</italic></td><td char="." align="char">1</td><td align="left">Rectal swab</td><td align="left">2013/Rainy</td><td char="." align="char">1</td><td align="left">Home stead</td><td align="left">Strain of Kenya bat coronavirus/BtKY56/BtKY55</td><td align="left">KX285830</td></tr><tr><td align="left"><italic>Chaerephon pumilus</italic></td><td char="." align="char">1</td><td align="left">Rectal swab</td><td align="left">2013/Rainy</td><td char="." align="char">6</td><td align="left">Ecotourism site</td><td align="left">Strain of Chaerephon bat/coronavirus/Kenya/KY22/2006</td><td align="left">KX285828</td></tr><tr><td align="left"><italic>Eidolon helvum</italic></td><td char="." align="char">4</td><td align="left">Rectal swab</td><td align="left">2012/Rainy</td><td char="." align="char">3</td><td align="left">Ecotourism site</td><td align="left">Strain of Eidolon bat coronavirus/Kenya/KY24/2006</td><td align="left">KX285106</td></tr><tr><td align="left"><italic>Eidolon helvum</italic></td><td char="." align="char">1</td><td align="left">Rectal swab</td><td align="left">2012/Rainy</td><td char="." align="char">4</td><td align="left">Ecotourism site</td><td align="left">Strain of Eidolon bat coronavirus/Kenya/KY24/2006</td><td align="left">KX285107</td></tr><tr><td align="left"><italic>Eidolon helvum</italic></td><td char="." align="char">6</td><td align="left">Rectal swab</td><td align="left">2013/Dry</td><td char="." align="char">5</td><td align="left">Crop farming</td><td align="left">Strain of Eidolon bat coronavirus/Kenya/KY24/2006</td><td align="left">KX285108</td></tr><tr><td align="left"><italic>Rousettus aegyptiacus</italic></td><td char="." align="char">2</td><td align="left">Rectal swab</td><td align="left">2013/Rainy</td><td char="." align="char">6</td><td align="left">Ecotourism site</td><td align="left">Strain of Bat coronavirus HKU9</td><td align="left">KX286259</td></tr><tr><td align="left"><italic>Rousettus aegyptiacus</italic></td><td char="." align="char">2</td><td align="left">Rectal swab</td><td align="left">2013/Rainy</td><td char="." align="char">1</td><td align="left">Home stead</td><td align="left">Strain of Kenya bat coronavirus/BtKY56/BtKY55</td><td align="left">KX285819</td></tr><tr><td align="left"><italic>Eidolon helvum</italic></td><td char="." align="char">2</td><td align="left">Rectal swab</td><td align="left">2012/Rainy</td><td char="." align="char">3</td><td align="left">Ecotourism site</td><td align="left">Strain of Eidolon bat coronavirus/Kenya/KY24/2006</td><td align="left">KX285822</td></tr><tr><td align="left"></td><td char="." align="char">19</td><td align="left"></td><td align="left"></td><td align="left"></td><td align="left"></td><td align="left"></td><td align="left"></td></tr></tbody></table></table-wrap><table-wrap id="Tab3"><label>Table 3</label><caption><p>Novel Coronaviruses Detected in Bats by Species and Specimen Type.</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="left">Bat species</th><th align="left">c-PCR positive</th><th align="left">Sample tested</th><th align="left">Year of collection/season</th><th align="left">Site no.</th><th align="left">Risk interface</th><th align="left">Virus name</th><th align="left">Genbank no.</th></tr></thead><tbody><tr><td align="left"><italic>Rhinolophus clivosus</italic></td><td char="." align="char">1</td><td align="left">Oral swab</td><td align="left">2011/Rainy</td><td char="." align="char">12</td><td align="left">Ecotourism sites</td><td align="left">PREDICT_CoV-43</td><td align="left">KX285821</td></tr><tr><td align="left"><italic>Rousettus angolensis</italic></td><td char="." align="char">1</td><td align="left">Rectal swab</td><td align="left">2013/Rainy</td><td char="." align="char">11</td><td align="left">National park</td><td align="left">PREDICT_CoV-66</td><td align="left">KX285426</td></tr><tr><td align="left"><italic>Hipposideros caffe</italic>r</td><td char="." align="char">1</td><td align="left">Rectal swab</td><td align="left">2011/Rainy</td><td char="." align="char">11</td><td align="left">National park</td><td align="left">PREDICT_CoV-44</td><td align="left">KX285826</td></tr><tr><td align="left"><italic>Rhinolophus clivosus</italic></td><td char="." align="char">1</td><td align="left">Rectal swab</td><td align="left">2013/Rainy</td><td char="." align="char">11</td><td align="left">National park</td><td align="left">PREDICT_CoV-44</td><td align="left">KX286327</td></tr><tr><td align="left"><italic>Hipposideros ruber</italic></td><td char="." align="char">1</td><td align="left">Rectal swab</td><td align="left">2013/Rainy</td><td char="." align="char">10</td><td align="left">Crop farming</td><td align="left">PREDICT_CoV-43</td><td align="left">KX286324</td></tr><tr><td align="left"><italic>Rhinolophus clivosus</italic></td><td char="." align="char">2</td><td align="left">Rectal swab</td><td align="left">2011/Rainy</td><td char="." align="char">12</td><td align="left">Ecotourism site</td><td align="left">PREDICT_CoV-43</td><td align="left">KX286325</td></tr><tr><td align="left"><italic>Rhinolophus clivosus</italic></td><td char="." align="char">1</td><td align="left">Rectal swab</td><td align="left">2011/Rainy</td><td char="." align="char">12</td><td align="left">Ecotourism site</td><td align="left">PREDICT_CoV-42</td><td align="left">KX285111</td></tr><tr><td align="left"></td><td char="." align="char">8</td><td align="left"></td><td align="left"></td><td align="left"></td><td align="left"></td><td align="left"></td><td align="left"></td></tr></tbody></table></table-wrap><fig id="Fig2"><label>Figure 2</label><caption><p>Map of Rwanda showing the bats sampling sites for corona viral surveillance during the study.</p></caption><graphic xlink:href="10393_2019_1458_Fig2_HTML" id="MO2"></graphic></fig></p><p id="Par11">The 2d betacoronavirus, PREDICT_CoV-66, was detected in one <italic>Rousettus angolensis</italic> bat in Nyungwe National Park (Site 11; Fig. <xref rid="Fig2" ref-type="fig">2</xref>) and showed 84% nucleotide similarity to the closest recognized coronavirus, Kenya bat Coronavirus BtKY84 (Genbank accession no. GU65428) found previously in <italic>E</italic>. <italic>helvum</italic>. The only alphacoronavirus PREDICT_CoV-42 was detected in a <italic>R</italic>. <italic>clivosus</italic> bat in tourism caves (Site No. 10). This virus sequence showed only 85% nucleotide similarity to the closest recognized coronavirus, Kenya bat Coronavirus BtKY69 (Genbank accession no. GU65413), found previously in horseshoe bats (<italic>Rhinolophus</italic> species).</p><p id="Par12">Phylogenetic analyses of complete genome sequences of coronaviruses from bats, humans, and other vertebrates suggest that bats may be the reservoir hosts from which all coronavirus lineages originated (Vijaykrishna et al. <xref ref-type="bibr" rid="CR40">2007</xref>; Anthony et al. <xref ref-type="bibr" rid="CR4">2017a</xref>), and several studies document the diversity of bat coronaviruses globally (Dominguez et al. <xref ref-type="bibr" rid="CR11">2007</xref>; Annan et al. <xref ref-type="bibr" rid="CR2">2013</xref>; Anthony et al. <xref ref-type="bibr" rid="CR5">2017b</xref>).</p><p id="Par13">In this study, sequences representing two novel coronaviruses that clustered with the SARS-like coronaviruses were detected in bat tourism caves and other sites where people and bats come into close contact in Rwanda. One virus (PREDICT CoV-43) was detected in both Sundevall’s roundleaf bat (<italic>H. ruber</italic>) and Geoffrey’s horseshoe bat (<italic>R</italic>. <italic>clivosus</italic>) that were co-roosting in the Musanze Caves (Site No. 10). The high sequence similarity of the viral fragment detected in both bat species suggests that this virus may have the ability to be maintained in more than one host or that cross-species transmission may occur. Studies have found that viral sharing and cross-species transmission may be important factors that contribute to emergence of novel coronaviruses and recombination of bat coronaviruses (Lau et al. <xref ref-type="bibr" rid="CR22">2010</xref>; Johnson et al. <xref ref-type="bibr" rid="CR19">2015</xref>).</p><p id="Par14">While the known coronaviruses detected in this study have been identified in other geographical areas and in different bat species (Tao et al. <xref ref-type="bibr" rid="CR36">2012</xref>; Drexler et al. <xref ref-type="bibr" rid="CR12">2010</xref>), we report their first detection in Rwanda. The bat coronavirus HKU9 was previously detected in <italic>Rousettus leschenaulti</italic> bats in China (Tang et al. <xref ref-type="bibr" rid="CR35">2006</xref>), and now a strain of this virus has been detected in bats in Rwanda. Similarly, Kenya bat coronavirus/BtKY56/BtKY55 in <italic>R</italic>. <italic>aegyptiacus</italic>, Chaerephon bat coronavirus/Kenya/KY22/2006 in <italic>Chaerephon pumilus</italic>, and Eidolon bat coronavirus/Kenya/KY24/2006 in <italic>Eidolon helvum</italic> were first detected in Kenya in 2006 (Tao et al. <xref ref-type="bibr" rid="CR36">2012</xref>). We report the presence of these viruses in these same bat species in Rwanda, indicating a wider geographic distribution of these viruses in Eastern Africa, likely due to the widespread distribution of their bat hosts (Drexler et al. <xref ref-type="bibr" rid="CR12">2010</xref>; Gloza-Rausch et al. <xref ref-type="bibr" rid="CR15">2008</xref>).</p><p id="Par15">In conclusion, bats in Rwanda carry novel and known coronaviruses, a family of viruses from which novel viruses have caused human pandemics. However, bats play important ecological roles and their elimination as a control measure is not recommended or warranted. We recommend additional surveillance and longitudinal studies to further understand the ecology of bat coronaviruses and the extent of human–bat interactions to identify strategies for public health protection and bat conservation.</p></sec></body><back><ack><p>We thank the government of Rwanda for permission to conduct this work. This study was made possible by the generous support of the American people through the United States Agency for International Development (USAID) Emerging Pandemic Threats PREDICT project (cooperative agreement number GHN-A-OO-09-00010-00). The results from the study do not indicate the opinion of the United States of America government. Sampling was conducted under a University of California, Davis Animal Care and Use Committee approved protocol (UC Davis IACUC Protocol No. 16048). 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