Enzootic patterns of Middle East respiratory syndrome coronavirus in imported African and local Arabian dromedary camels: a prospective genomic study
Identifieur interne : 000594 ( Main/Curation ); précédent : 000593; suivant : 000595Enzootic patterns of Middle East respiratory syndrome coronavirus in imported African and local Arabian dromedary camels: a prospective genomic study
Auteurs : Sherif A. El-Kafrawy [Arabie saoudite] ; Victor M. Corman [Allemagne] ; Ahmed M. Tolah [Arabie saoudite] ; Saad B. Al Masaudi [Arabie saoudite] ; Ahmed M. Hassan [Arabie saoudite] ; Marcel A. Müller [Allemagne, Russie] ; Tobias Bleicker [Allemagne] ; Steve M. Harakeh [Arabie saoudite] ; Abdulrahman A. Alzahrani [Arabie saoudite] ; Ghaleb A. Alsaaidi [Arabie saoudite] ; Abdulaziz N. Alagili [Arabie saoudite] ; Anwar M. Hashem [Arabie saoudite] ; Alimuddin Zumla [Royaume-Uni] ; Christian Drosten [Allemagne] ; Esam I. Azhar [Arabie saoudite]Source :
- The Lancet. Planetary Health [ 2542-5196 ] ; 2019.
Abstract
The Middle East respiratory syndrome coronavirus (MERS-CoV) is a lethal zoonotic pathogen endemic to the Arabian Peninsula. Dromedary camels are a likely source of infection and the virus probably originated in Africa. We studied the genetic diversity, geographical structure, infection prevalence, and age-associated prevalence among camels at the largest entry port of camels from Africa into the Arabian Peninsula.
In this prospective genomic study, we took nasal samples from camels imported from Sudan and Djibouti into the Port of Jeddah in Jeddah, Saudi Arabia, over an almost 2-year period and local Arabian camels over 2 months in the year after surveillance of the port. We determined the prevalence of MERS-CoV infection, age-associated patterns of infection, and undertook phylogeographical and migration analyses to determine intercountry virus transmission after local lineage establishment. We compared all virological characteristics between the local and imported cohorts. We compared major gene deletions between African and Arabian strains of the virus. Reproductive numbers were inferred with Bayesian birth death skyline analyses.
Between Aug 10, 2016, and May 3, 2018, we collected samples from 1196 imported camels, of which 868 originated from Sudan and 328 from Djibouti, and between May 1, and June 25, 2018, we collected samples from 472 local camels, of which 189 were from Riyadh and 283 were from Jeddah, Saudi Arabia. Virus prevalence was higher in local camels than in imported camels (224 [47·5%] of 472
Despite frequent imports of MERS-CoV with camels from Africa, African lineages of MERS-CoV do not establish themselves in Saudi Arabia. Arabian strains of the virus should be tested for changes in virulence and transmissibility.
German Ministry of Research and Education, EU Horizon 2020, and Emerging Diseases Clinical Trials Partnership.
Url:
DOI: 10.1016/S2542-5196(19)30243-8
PubMed: 31843456
PubMed Central: 6926486
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<affiliation wicri:level="1"><nlm:aff id="aff3">Department of Biological Science, Division of Microbiology, Faculty of Science, King Abdulaziz University, Jeddah, Saudi Arabia</nlm:aff>
<country xml:lang="fr">Arabie saoudite</country>
<wicri:regionArea>Department of Biological Science, Division of Microbiology, Faculty of Science, King Abdulaziz University, Jeddah</wicri:regionArea>
<wicri:noRegion>Jeddah</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="Al Masaudi, Saad B" sort="Al Masaudi, Saad B" uniqKey="Al Masaudi S" first="Saad B" last="Al Masaudi">Saad B. Al Masaudi</name>
<affiliation wicri:level="1"><nlm:aff id="aff3">Department of Biological Science, Division of Microbiology, Faculty of Science, King Abdulaziz University, Jeddah, Saudi Arabia</nlm:aff>
<country xml:lang="fr">Arabie saoudite</country>
<wicri:regionArea>Department of Biological Science, Division of Microbiology, Faculty of Science, King Abdulaziz University, Jeddah</wicri:regionArea>
<wicri:noRegion>Jeddah</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="Hassan, Ahmed M" sort="Hassan, Ahmed M" uniqKey="Hassan A" first="Ahmed M" last="Hassan">Ahmed M. Hassan</name>
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<country xml:lang="fr">Arabie saoudite</country>
<wicri:regionArea>Special Infectious Agent Unit, King Fahd Medical Research Center, King Abdulaziz University, Jeddah</wicri:regionArea>
<wicri:noRegion>Jeddah</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="Muller, Marcel A" sort="Muller, Marcel A" uniqKey="Muller M" first="Marcel A" last="Müller">Marcel A. Müller</name>
<affiliation wicri:level="1"><nlm:aff id="aff5">Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, Germany</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin</wicri:regionArea>
<wicri:noRegion>Humboldt-Universität zu Berlin</wicri:noRegion>
<wicri:noRegion>Humboldt-Universität zu Berlin</wicri:noRegion>
<wicri:noRegion>Humboldt-Universität zu Berlin</wicri:noRegion>
</affiliation>
<affiliation wicri:level="3"><nlm:aff id="aff6">Berlin Institute of Health, Institute of Virology, Berlin, Germany</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Berlin Institute of Health, Institute of Virology, Berlin</wicri:regionArea>
<placeName><region type="land" nuts="3">Berlin</region>
<settlement type="city">Berlin</settlement>
</placeName>
</affiliation>
<affiliation wicri:level="3"><nlm:aff id="aff7">German Centre for Infection Research, associated partner Charité, Berlin, Germany</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>German Centre for Infection Research, associated partner Charité, Berlin</wicri:regionArea>
<placeName><region type="land" nuts="3">Berlin</region>
<settlement type="city">Berlin</settlement>
</placeName>
</affiliation>
<affiliation wicri:level="3"><nlm:aff id="aff8">Martsinovsky Institute of Medical Parasitology, Tropical and Vector Borne Diseases, Sechenov University, Moscow, Russia</nlm:aff>
<country xml:lang="fr">Russie</country>
<wicri:regionArea>Martsinovsky Institute of Medical Parasitology, Tropical and Vector Borne Diseases, Sechenov University, Moscow</wicri:regionArea>
<placeName><settlement type="city">Moscou</settlement>
<region>District fédéral central</region>
</placeName>
</affiliation>
</author>
<author><name sortKey="Bleicker, Tobias" sort="Bleicker, Tobias" uniqKey="Bleicker T" first="Tobias" last="Bleicker">Tobias Bleicker</name>
<affiliation wicri:level="1"><nlm:aff id="aff5">Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, Germany</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin</wicri:regionArea>
<wicri:noRegion>Humboldt-Universität zu Berlin</wicri:noRegion>
<wicri:noRegion>Humboldt-Universität zu Berlin</wicri:noRegion>
<wicri:noRegion>Humboldt-Universität zu Berlin</wicri:noRegion>
</affiliation>
<affiliation wicri:level="3"><nlm:aff id="aff6">Berlin Institute of Health, Institute of Virology, Berlin, Germany</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Berlin Institute of Health, Institute of Virology, Berlin</wicri:regionArea>
<placeName><region type="land" nuts="3">Berlin</region>
<settlement type="city">Berlin</settlement>
</placeName>
</affiliation>
</author>
<author><name sortKey="Harakeh, Steve M" sort="Harakeh, Steve M" uniqKey="Harakeh S" first="Steve M" last="Harakeh">Steve M. Harakeh</name>
<affiliation wicri:level="1"><nlm:aff id="aff1">Special Infectious Agent Unit, King Fahd Medical Research Center, King Abdulaziz University, Jeddah, Saudi Arabia</nlm:aff>
<country xml:lang="fr">Arabie saoudite</country>
<wicri:regionArea>Special Infectious Agent Unit, King Fahd Medical Research Center, King Abdulaziz University, Jeddah</wicri:regionArea>
<wicri:noRegion>Jeddah</wicri:noRegion>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff2">Department of Medical Laboratory Technology, Faculty of Applied Medical Sciences, King Abdulaziz University, Jeddah, Saudi Arabia</nlm:aff>
<country xml:lang="fr">Arabie saoudite</country>
<wicri:regionArea>Department of Medical Laboratory Technology, Faculty of Applied Medical Sciences, King Abdulaziz University, Jeddah</wicri:regionArea>
<wicri:noRegion>Jeddah</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="Alzahrani, Abdulrahman A" sort="Alzahrani, Abdulrahman A" uniqKey="Alzahrani A" first="Abdulrahman A" last="Alzahrani">Abdulrahman A. Alzahrani</name>
<affiliation wicri:level="1"><nlm:aff id="aff9">Directorate of Agriculture, Ministry of Environment Water and Agriculture, Makkah Region, Saudi Arabia</nlm:aff>
<country xml:lang="fr">Arabie saoudite</country>
<wicri:regionArea>Directorate of Agriculture, Ministry of Environment Water and Agriculture, Makkah Region</wicri:regionArea>
<wicri:noRegion>Makkah Region</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="Alsaaidi, Ghaleb A" sort="Alsaaidi, Ghaleb A" uniqKey="Alsaaidi G" first="Ghaleb A" last="Alsaaidi">Ghaleb A. Alsaaidi</name>
<affiliation wicri:level="1"><nlm:aff id="aff9">Directorate of Agriculture, Ministry of Environment Water and Agriculture, Makkah Region, Saudi Arabia</nlm:aff>
<country xml:lang="fr">Arabie saoudite</country>
<wicri:regionArea>Directorate of Agriculture, Ministry of Environment Water and Agriculture, Makkah Region</wicri:regionArea>
<wicri:noRegion>Makkah Region</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="Alagili, Abdulaziz N" sort="Alagili, Abdulaziz N" uniqKey="Alagili A" first="Abdulaziz N" last="Alagili">Abdulaziz N. Alagili</name>
<affiliation wicri:level="1"><nlm:aff id="aff10">Mammals Research Chair, Department of Zoology, College of Science, King Saud University, Riyadh, Saudi Arabia</nlm:aff>
<country xml:lang="fr">Arabie saoudite</country>
<wicri:regionArea>Mammals Research Chair, Department of Zoology, College of Science, King Saud University, Riyadh</wicri:regionArea>
<wicri:noRegion>Riyadh</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="Hashem, Anwar M" sort="Hashem, Anwar M" uniqKey="Hashem A" first="Anwar M" last="Hashem">Anwar M. Hashem</name>
<affiliation wicri:level="1"><nlm:aff id="aff1">Special Infectious Agent Unit, King Fahd Medical Research Center, King Abdulaziz University, Jeddah, Saudi Arabia</nlm:aff>
<country xml:lang="fr">Arabie saoudite</country>
<wicri:regionArea>Special Infectious Agent Unit, King Fahd Medical Research Center, King Abdulaziz University, Jeddah</wicri:regionArea>
<wicri:noRegion>Jeddah</wicri:noRegion>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff4">Department of Medical Microbiology and Parasitology, Faculty of Medicine, King Abdulaziz University, Jeddah, Saudi Arabia</nlm:aff>
<country xml:lang="fr">Arabie saoudite</country>
<wicri:regionArea>Department of Medical Microbiology and Parasitology, Faculty of Medicine, King Abdulaziz University, Jeddah</wicri:regionArea>
<wicri:noRegion>Jeddah</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="Zumla, Alimuddin" sort="Zumla, Alimuddin" uniqKey="Zumla A" first="Alimuddin" last="Zumla">Alimuddin Zumla</name>
<affiliation wicri:level="4"><nlm:aff id="aff11">Department of Infection, Division of Infection and Immunity, Centre for Clinical Microbiology, University College London, London, UK</nlm:aff>
<country xml:lang="fr">Royaume-Uni</country>
<wicri:regionArea>Department of Infection, Division of Infection and Immunity, Centre for Clinical Microbiology, University College London, London</wicri:regionArea>
<placeName><settlement type="city">Londres</settlement>
<region type="country">Angleterre</region>
<region type="région" nuts="1">Grand Londres</region>
</placeName>
<orgName type="university">University College de Londres</orgName>
</affiliation>
<affiliation wicri:level="3"><nlm:aff id="aff12">NIHR Biomedical Research Centre, University College London Hospitals, London, UK</nlm:aff>
<country xml:lang="fr">Royaume-Uni</country>
<wicri:regionArea>NIHR Biomedical Research Centre, University College London Hospitals, London</wicri:regionArea>
<placeName><settlement type="city">Londres</settlement>
<region type="country">Angleterre</region>
<region type="région" nuts="1">Grand Londres</region>
</placeName>
</affiliation>
</author>
<author><name sortKey="Drosten, Christian" sort="Drosten, Christian" uniqKey="Drosten C" first="Christian" last="Drosten">Christian Drosten</name>
<affiliation wicri:level="1"><nlm:aff id="aff5">Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, Germany</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin</wicri:regionArea>
<wicri:noRegion>Humboldt-Universität zu Berlin</wicri:noRegion>
<wicri:noRegion>Humboldt-Universität zu Berlin</wicri:noRegion>
<wicri:noRegion>Humboldt-Universität zu Berlin</wicri:noRegion>
</affiliation>
<affiliation wicri:level="3"><nlm:aff id="aff6">Berlin Institute of Health, Institute of Virology, Berlin, Germany</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Berlin Institute of Health, Institute of Virology, Berlin</wicri:regionArea>
<placeName><region type="land" nuts="3">Berlin</region>
<settlement type="city">Berlin</settlement>
</placeName>
</affiliation>
<affiliation wicri:level="3"><nlm:aff id="aff7">German Centre for Infection Research, associated partner Charité, Berlin, Germany</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>German Centre for Infection Research, associated partner Charité, Berlin</wicri:regionArea>
<placeName><region type="land" nuts="3">Berlin</region>
<settlement type="city">Berlin</settlement>
</placeName>
</affiliation>
</author>
<author><name sortKey="Azhar, Esam I" sort="Azhar, Esam I" uniqKey="Azhar E" first="Esam I" last="Azhar">Esam I. Azhar</name>
<affiliation wicri:level="1"><nlm:aff id="aff1">Special Infectious Agent Unit, King Fahd Medical Research Center, King Abdulaziz University, Jeddah, Saudi Arabia</nlm:aff>
<country xml:lang="fr">Arabie saoudite</country>
<wicri:regionArea>Special Infectious Agent Unit, King Fahd Medical Research Center, King Abdulaziz University, Jeddah</wicri:regionArea>
<wicri:noRegion>Jeddah</wicri:noRegion>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff2">Department of Medical Laboratory Technology, Faculty of Applied Medical Sciences, King Abdulaziz University, Jeddah, Saudi Arabia</nlm:aff>
<country xml:lang="fr">Arabie saoudite</country>
<wicri:regionArea>Department of Medical Laboratory Technology, Faculty of Applied Medical Sciences, King Abdulaziz University, Jeddah</wicri:regionArea>
<wicri:noRegion>Jeddah</wicri:noRegion>
</affiliation>
</author>
</analytic>
<series><title level="j">The Lancet. Planetary Health</title>
<idno type="eISSN">2542-5196</idno>
<imprint><date when="2019">2019</date>
</imprint>
</series>
</biblStruct>
</sourceDesc>
</fileDesc>
<profileDesc><textClass></textClass>
</profileDesc>
</teiHeader>
<front><div type="abstract" xml:lang="en"><title>Summary</title>
<sec><title>Background</title>
<p>The Middle East respiratory syndrome coronavirus (MERS-CoV) is a lethal zoonotic pathogen endemic to the Arabian Peninsula. Dromedary camels are a likely source of infection and the virus probably originated in Africa. We studied the genetic diversity, geographical structure, infection prevalence, and age-associated prevalence among camels at the largest entry port of camels from Africa into the Arabian Peninsula.</p>
</sec>
<sec><title>Methods</title>
<p>In this prospective genomic study, we took nasal samples from camels imported from Sudan and Djibouti into the Port of Jeddah in Jeddah, Saudi Arabia, over an almost 2-year period and local Arabian camels over 2 months in the year after surveillance of the port. We determined the prevalence of MERS-CoV infection, age-associated patterns of infection, and undertook phylogeographical and migration analyses to determine intercountry virus transmission after local lineage establishment. We compared all virological characteristics between the local and imported cohorts. We compared major gene deletions between African and Arabian strains of the virus. Reproductive numbers were inferred with Bayesian birth death skyline analyses.</p>
</sec>
<sec><title>Findings</title>
<p>Between Aug 10, 2016, and May 3, 2018, we collected samples from 1196 imported camels, of which 868 originated from Sudan and 328 from Djibouti, and between May 1, and June 25, 2018, we collected samples from 472 local camels, of which 189 were from Riyadh and 283 were from Jeddah, Saudi Arabia. Virus prevalence was higher in local camels than in imported camels (224 [47·5%] of 472 <italic>vs</italic>
157 [13·1%] of 1196; p<0·0001). Infection prevalence peaked among camels older than 1 year and aged up to 2 years in both groups, with 255 (66·9%) of 381 positive cases in this age group. Although the overall geographical distribution of the virus corresponded with the phylogenetic tree topology, some virus exchange was observed between countries corresponding with trade routes in the region. East and west African strains of the virus appear to be geographically separated, with an origin of west African strains in east Africa. African strains of the virus were not re-sampled in Saudi Arabia despite sampling approximately 1 year after importation from Africa. All local Arabian samples contained strains of the virus that belong to a novel recombinant clade (NRC) first detected in 2014 in Saudi Arabia. Reproduction number estimates informed by the sequences suggest sustained endemicity of NRC, with a mean R<sub>e</sub>
of 1·16.</p>
</sec>
<sec><title>Interpretation</title>
<p>Despite frequent imports of MERS-CoV with camels from Africa, African lineages of MERS-CoV do not establish themselves in Saudi Arabia. Arabian strains of the virus should be tested for changes in virulence and transmissibility.</p>
</sec>
<sec><title>Funding</title>
<p>German Ministry of Research and Education, EU Horizon 2020, and Emerging Diseases Clinical Trials Partnership.</p>
</sec>
</div>
</front>
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