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Enzootic patterns of Middle East respiratory syndrome coronavirus in imported African and local Arabian dromedary camels: a prospective genomic study.
Lancet Planet Health. 2019 12; 3(12):e521-e528.LP

Abstract

BACKGROUND

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.

METHODS

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.

FINDINGS

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 vs 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 Re of 1·16.

INTERPRETATION

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.

FUNDING

German Ministry of Research and Education, EU Horizon 2020, and Emerging Diseases Clinical Trials Partnership.

Authors+Show Affiliations

Special Infectious Agent Unit, King Fahd Medical Research Center, King Abdulaziz University, Jeddah, Saudi Arabia; Department of Medical Laboratory Technology, Faculty of Applied Medical Sciences, King Abdulaziz University, Jeddah, Saudi Arabia.Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, Germany; Berlin Institute of Health, Institute of Virology, Berlin, Germany; German Centre for Infection Research, associated partner Charité, Berlin, Germany.Special Infectious Agent Unit, King Fahd Medical Research Center, King Abdulaziz University, Jeddah, Saudi Arabia; Department of Biological Science, Division of Microbiology, Faculty of Science, King Abdulaziz University, Jeddah, Saudi Arabia.Department of Biological Science, Division of Microbiology, Faculty of Science, King Abdulaziz University, Jeddah, Saudi Arabia.Special Infectious Agent Unit, King Fahd Medical Research Center, King Abdulaziz University, Jeddah, Saudi Arabia.Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, Germany; Berlin Institute of Health, Institute of Virology, Berlin, Germany; German Centre for Infection Research, associated partner Charité, Berlin, Germany; Martsinovsky Institute of Medical Parasitology, Tropical and Vector Borne Diseases, Sechenov University, Moscow, Russia.Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, Germany; Berlin Institute of Health, Institute of Virology, Berlin, Germany.Special Infectious Agent Unit, King Fahd Medical Research Center, King Abdulaziz University, Jeddah, Saudi Arabia; Department of Medical Laboratory Technology, Faculty of Applied Medical Sciences, King Abdulaziz University, Jeddah, Saudi Arabia.Directorate of Agriculture, Ministry of Environment Water and Agriculture, Makkah Region, Saudi Arabia.Directorate of Agriculture, Ministry of Environment Water and Agriculture, Makkah Region, Saudi Arabia.Mammals Research Chair, Department of Zoology, College of Science, King Saud University, Riyadh, Saudi Arabia.Special Infectious Agent Unit, King Fahd Medical Research Center, King Abdulaziz University, Jeddah, Saudi Arabia; Department of Medical Microbiology and Parasitology, Faculty of Medicine, King Abdulaziz University, Jeddah, Saudi Arabia.Department of Infection, Division of Infection and Immunity, Centre for Clinical Microbiology, University College London, London, UK; NIHR Biomedical Research Centre, University College London Hospitals, London, UK.Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, Germany; Berlin Institute of Health, Institute of Virology, Berlin, Germany; German Centre for Infection Research, associated partner Charité, Berlin, Germany. Electronic address: christian.drosten@charite.de.Special Infectious Agent Unit, King Fahd Medical Research Center, King Abdulaziz University, Jeddah, Saudi Arabia; Department of Medical Laboratory Technology, Faculty of Applied Medical Sciences, King Abdulaziz University, Jeddah, Saudi Arabia. Electronic address: eazhar@kau.edu.sa.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

31843456

Citation

El-Kafrawy, Sherif A., et al. "Enzootic Patterns of Middle East Respiratory Syndrome Coronavirus in Imported African and Local Arabian Dromedary Camels: a Prospective Genomic Study." The Lancet. Planetary Health, vol. 3, no. 12, 2019, pp. e521-e528.
El-Kafrawy SA, Corman VM, Tolah AM, et al. Enzootic patterns of Middle East respiratory syndrome coronavirus in imported African and local Arabian dromedary camels: a prospective genomic study. Lancet Planet Health. 2019;3(12):e521-e528.
El-Kafrawy, S. A., Corman, V. M., Tolah, A. M., Al Masaudi, S. B., Hassan, A. M., Müller, M. A., Bleicker, T., Harakeh, S. M., Alzahrani, A. A., Alsaaidi, G. A., Alagili, A. N., Hashem, A. M., Zumla, A., Drosten, C., & Azhar, E. I. (2019). Enzootic patterns of Middle East respiratory syndrome coronavirus in imported African and local Arabian dromedary camels: a prospective genomic study. The Lancet. Planetary Health, 3(12), e521-e528. https://doi.org/10.1016/S2542-5196(19)30243-8
El-Kafrawy SA, et al. Enzootic Patterns of Middle East Respiratory Syndrome Coronavirus in Imported African and Local Arabian Dromedary Camels: a Prospective Genomic Study. Lancet Planet Health. 2019;3(12):e521-e528. PubMed PMID: 31843456.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Enzootic patterns of Middle East respiratory syndrome coronavirus in imported African and local Arabian dromedary camels: a prospective genomic study. AU - El-Kafrawy,Sherif A, AU - Corman,Victor M, AU - Tolah,Ahmed M, AU - Al Masaudi,Saad B, AU - Hassan,Ahmed M, AU - Müller,Marcel A, AU - Bleicker,Tobias, AU - Harakeh,Steve M, AU - Alzahrani,Abdulrahman A, AU - Alsaaidi,Ghaleb A, AU - Alagili,Abdulaziz N, AU - Hashem,Anwar M, AU - Zumla,Alimuddin, AU - Drosten,Christian, AU - Azhar,Esam I, Y1 - 2019/12/16/ PY - 2019/07/08/received PY - 2019/11/19/revised PY - 2019/11/20/accepted PY - 2019/12/18/pubmed PY - 2020/7/14/medline PY - 2019/12/18/entrez SP - e521 EP - e528 JF - The Lancet. Planetary health JO - Lancet Planet Health VL - 3 IS - 12 N2 - BACKGROUND: 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. METHODS: 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. FINDINGS: 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 vs 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 Re of 1·16. INTERPRETATION: 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. FUNDING: German Ministry of Research and Education, EU Horizon 2020, and Emerging Diseases Clinical Trials Partnership. SN - 2542-5196 UR - https://www.unboundmedicine.com/medline/citation/31843456/Enzootic_patterns_of_Middle_East_respiratory_syndrome_coronavirus_in_imported_African_and_local_Arabian_dromedary_camels:_a_prospective_genomic_study_ L2 - https://linkinghub.elsevier.com/retrieve/pii/S2542-5196(19)30243-8 DB - PRIME DP - Unbound Medicine ER -