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Enzootic Patterns of Middle East Respiratory Syndrome Coronavirus in Imported African and Local Arabian Dromedary Camels: a Prospective Genomic Study

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Enzootic Patterns of Middle East Respiratory Syndrome Coronavirus in Imported African and Local Arabian Dromedary Camels: a Prospective Genomic Study Articles Enzootic patterns of Middle East respiratory syndrome coronavirus in imported African and local Arabian dromedary camels: a prospective genomic study Sherif A El-Kafrawy*, Victor M Corman*, Ahmed M Tolah, Saad B Al Masaudi, Ahmed M Hassan, Marcel A Müller, Tobias Bleicker, Steve M Harakeh, Abdulrahman A Alzahrani, Ghaleb A Alsaaidi, Abdulaziz N Alagili, Anwar M Hashem, Alimuddin Zumla*, Christian Drosten*, Esam I Azhar* Summary Background The Middle East respiratory syndrome coronavirus (MERS-CoV) is a lethal zoonotic pathogen endemic to Lancet Planet Health 2019; the Arabian Peninsula. Dromedary camels are a likely source of infection and the virus probably originated in Africa. 3: e521–28 We studied the genetic diversity, geographical structure, infection prevalence, and age-associated prevalence among Published Online camels at the largest entry port of camels from Africa into the Arabian Peninsula. December 13, 2019 https://doi.org/10.1016/ S2542-5196(19)30243-8 Methods In this prospective genomic study, we took nasal samples from camels imported from Sudan and Djibouti *Contributed equally into the Port of Jeddah in Jeddah, Saudi Arabia, over an almost 2-year period and local Arabian camels over 2 months Special Infectious Agent Unit, in the year after surveillance of the port. We determined the prevalence of MERS-CoV infection, age-associated King Fahd Medical Research patterns of infection, and undertook phylogeographical and migration analyses to determine intercountry virus Center (S A El-Kafrawy PhD, transmission after local lineage establishment. We compared all virological characteristics between the local and A M Tolah PhD, A M Hassan PhD, S M Harakeh PhD, imported cohorts. We compared major gene deletions between African and Arabian strains of the virus. Reproductive A M Hashem PhD, numbers were inferred with Bayesian birth death skyline analyses. Prof E I Azhar FRCP), Department of Medical Findings Between Aug 10, 2016, and May 3, 2018, we collected samples from 1196 imported camels, of which Laboratory Technology, Faculty of Applied Medical Sciences 868 originated from Sudan and 328 from Djibouti, and between May 1, and June 25, 2018, we collected samples from (S A El-Kafrawy, S M Harakeh, 472 local camels, of which 189 were from Riyadh and 283 were from Jeddah, Saudi Arabia. Virus prevalence was higher Prof E I Azhar), Department of in local camels than in imported camels (224 [47·5%] of 472 vs 157 [13·1%] of 1196; p<0·0001). Infection prevalence Biological Science, Division of peaked among camels older than 1 year and aged up to 2 years in both groups, with 255 (66·9%) of 381 positive cases Microbiology, Faculty of Science (A M Tolah, in this age group. Although the overall geographical distribution of the virus corresponded with the phylogenetic tree S B Al Masaudi PhD), and topology, some virus exchange was observed between countries corresponding with trade routes in the region. East Department of Medical and west African strains of the virus appear to be geographically separated, with an origin of west African strains in Microbiology and Parasitology, east Africa. African strains of the virus were not re-sampled in Saudi Arabia despite sampling approximately 1 year Faculty of Medicine (A M Hashem), King Abdulaziz after importation from Africa. All local Arabian samples contained strains of the virus that belong to a novel University, Jeddah, Saudi recombinant clade (NRC) first detected in 2014 in Saudi Arabia. Reproduction number estimates informed by the Arabia; Charité- Universitätsmedizin Berlin, sequences suggest sustained endemicity of NRC, with a mean Re of 1·16. corporate member of Freie Universität Berlin, Humboldt- Interpretation Despite frequent imports of MERS-CoV with camels from Africa, African lineages of MERS-CoV do Universität zu Berlin, Germany not establish themselves in Saudi Arabia. Arabian strains of the virus should be tested for changes in virulence and (V M Corman MD, transmissibility. M A Müller PhD, T Bleicker, Prof C Drosten MD); Berlin Institute of Health, Institute of Funding German Ministry of Research and Education, EU Horizon 2020, and Emerging Diseases Clinical Trials Virology, Berlin, Germany Partnership. (V M Corman, M A Müller, T Bleicker, Prof C Drosten); Copyright German Centre for Infection © 2019 The Author(s). Published by Elsevier Ltd. This is an Open Access article under the CC BY 4.0 license. Research, associated partner Charité, Berlin, Germany Introduction South Korea in May, 2015, with 186 cases and 36 deaths (V M Corman, M A Müller, The Middle East respiratory syndrome coronavirus reported.2 The number of cases in Saudi Arabia and Prof C Drosten); Martsinovsky Institute of Medical (MERS-CoV) is a priority zoonotic pathogen listed in Oman has recently increased, with 126 cases reported in Parasitology, Tropical and the WHO R&D Blueprint for 2018 because of its January–March, 2019, compared with 189 cases reported Vector Borne Diseases, epidemic potential, high case fatality rate, and no from July, 2017, to June, 2018.2 Discovered in 2012, Sechenov University, Moscow, available treatment or vaccine.1 MERS-CoV continues to circulate in the Middle East and Russia (M A Müller); Directorate of Agriculture, Ministry of As of Aug 2, 2019, 2468 laboratory-confirmed cases of remains a threat to global health security. Despite many Environment Water and MERS, with 851 deaths (34·5% mortality) had been WHO scoping reviews and stake holder meetings Agriculture, Makkah Region, reported to WHO since September, 2012, globally.2 defining urgent priority research needs, major knowledge Saudi Arabia (A A Alzahrani PhD, 2090 (84%) of these cases occurred in Saudi Arabia and gaps in the epidemiology, transmission, pathogenesis, G A Alsaaidi PhD); Mammals Research Chair, Department of the largest outbreak outside of Saudi Arabia occurred in and evolu tion of MERS-CoV remain.1,3 www.thelancet.com/planetary-health Vol 3 December 2019 e521 Articles Zoology, College of Science, King Saud University, Riyadh, Research in context Saudi Arabia (A N Alagili PhD); Department of Infection, Evidence before this study from the African continent. Our data enhance the overall picture Division of Infection and We searched PubMed, Web of Science, and Google Scholar for of African strains of the virus, including the phylogenetic and Immunity, Centre for Clinical studies on the prevalence and diversity of Middle East geographical associations, which has enabled us to undertake Microbiology, University respiratory syndrome coronavirus (MERS-CoV) infection from comparisons of diversity against representatively large samples College London, London, UK (Prof A Zumla FRCP); and NIHR database inception until May 30, 2019, without language from the Arabian Peninsula. Our comparisons take sampling Biomedical Research Centre, restrictions. We used the term “MERS*” combined with any dates into account. We infer that Arabian and African strains of University College London single other term from the following list: “coronavirus*”, the virus have been separated for a time that exceeds the Hospitals, London, UK “camels*”, “dromedaries*”, “recombinant*”, “phylogeny*”, present observation period in all studies (ie, the virus strains (Prof A Zumla) “phylogeography”, “Africa*”, “sequenc*”, “prevalence”, “age”, have been separated since before 2012). We suggest that African Correspondence to: Prof Esam I Azar, and “transmission”. Since the discovery of MERS-CoV in 2012, strains of the virus are not transmitted in Arabian camels, Special Infectious Agents Unit, multiple sequencing studies have been done on viruses from despite large numbers of African camels frequently being King Fahd Medical Research camels and humans mainly in the Arabian Peninsula. Few imported into Saudi Arabia; and that Arabian strains of the virus Center, King Abdulaziz studies exist on sequences from Africa, but all of these might be self-sufficient in terms of their reproductive rate to University, P.O. Box 128442, Jeddah, 21362, Saudi Arabia sequences are from camels rather than from humans, whereas maintain endemic circulation. By sampling from local camels in [email protected] most of the sequences from the Arabian Peninsula are from Saudi Arabia, we found that a novel clade of MERS-CoV that or humans. Sampling bias is likely to affect all studies. The number emerged in 2014 remains the only detected viral variant in Prof Christian Drosten, Charité - of studies, and hence samples collected, from Africa is small camels from Saudi Arabia, suggesting that strains of this clade Universitätsmedizin Berlin, compared with those from the Arabian Peninsula. might be dominant over other viral strains that were co- Institute of Virology, Campus endemic in camels before 2014. Charité Mitte, D-10117, Berlin, Added value of this study Germany We took advantage of sampling opportunities at the Port of Implications of all the available evidence [email protected] Jeddah, in Jeddah, Saudi Arabia, where large numbers of camels Our results suggest that a recently emerged clade of MERS-CoV are continuously imported from Africa. By sampling before in Saudi Arabia should be compared with African strains of the offloading from ships we made sure to take samples from virus and with older Arabian strains to address the question of a animals that came directly from Africa and had no contact with potential increase in transmissibility and virulence. Change in local camels in Saudi Arabia. To our knowledge, the resulting transmissibility
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