1887

Journal of General Virology

Volume 97, Issue 2

Evidence for zoonotic origins of Middle East respiratory syndrome coronavirus Free

Abstract

Middle East respiratory syndrome (MERS) is an emerging infectious disease, caused by Middle East respiratory syndrome coronavirus (MERS-CoV) and is considered to be a zoonosis. However, the natural reservoirs of MERS-CoV remain obscure, with bats and camels as the most suspected sources. In this article, we review the evidence supporting a bat/camel origin of human MERS-CoV infection and current knowledge on the modes of camel-to-human transmission of MERS-CoV.

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2016-02-01
2021-08-04
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References

  1. Aburizaiza A. S., Mattes F. M., Azhar E. I., Hassan A. M., Memish Z. A., Muth D., Meyer B., Lattwein E., Müller M. A., Drosten C. 2014; Investigation of anti-middle East respiratory syndrome antibodies in blood donors and slaughterhouse workers in Jeddah and Makkah, Saudi Arabia, fall 2012. J Infect Dis 209:243–246 [View Article][PubMed]
     [Google Scholar]
  2. Adney D. R., van Doremalen N., Brown V. R., Bushmaker T., Scott D., de Wit E., Bowen R. A., Munster V. J. 2014; Replication and shedding of MERS-CoV in upper respiratory tract of inoculated dromedary camels. Emerg Infect Dis 20:1999–2005 [View Article][PubMed]
     [Google Scholar]
  3. Al-Yousef N., Gaafar A., Al-Otaibi B., Al-Jammaz I., Al-Hussein K., Aboussekhra A. 2012; Camel urine components display anti-cancer properties in vitro. J Ethnopharmacol 143:819–825 [View Article][PubMed]
     [Google Scholar]
  4. Alagaili A. N., Briese T., Mishra N., Kapoor V., Sameroff S. C., Burbelo P. D., de Wit E., Munster V. J., Hensley L. E., other authors. 2014; Middle East respiratory syndrome coronavirus infection in dromedary camels in Saudi Arabia. MBio 5:e00884–e00e14 [View Article][PubMed]
     [Google Scholar]
  5. Albarrak A. M., Stephens G. M., Hewson R., Memish Z. A. 2012; Recovery from severe novel coronavirus infection. Saudi Med J 33:1265–1269[PubMed]
     [Google Scholar]
  6. Annan A., Baldwin H. J., Corman V. M., Klose S. M., Owusu M., Nkrumah E. E., Badu E. K., Anti P., Agbenyega O., other authors. 2013; Human betacoronavirus 2c EMC/2012-related viruses in bats, Ghana and Europe. Emerg Infect Dis 19:456–459 [View Article][PubMed]
     [Google Scholar]
  7. Assiri A., McGeer A., Perl T. M., Price C. S., Al Rabeeah A. A., Cummings D. A., Alabdullatif Z. N., Assad M., Almulhim A., other authors. 2013; Hospital outbreak of Middle East respiratory syndrome coronavirus. N Engl J Med 369:407–416 [View Article][PubMed]
     [Google Scholar]
  8. Azhar E. I., El-Kafrawy S. A., Farraj S. A., Hassan A. M., Al-Saeed M. S., Hashem A. M., Madani T. A. 2014; Evidence for camel-to-human transmission of MERS coronavirus. N Engl J Med 370:2499–2505 [View Article][PubMed]
     [Google Scholar]
  9. Buchholz U., Muller M. A., Nitsche A., Sanewski A., Wevering N., Bauer-Balci T., Bonin F., Drosten C., Schweiger B., other authors. 2013; Contact investigation of a case of human novel coronavirus infection treated in a German hospital, October-November 2012. Euro Surveill 18:20406
     [Google Scholar]
  10. Chan R. W., Hemida M. G., Kayali G., Chu D. K., Poon L. L., Alnaeem A., Ali M. A., Tao K. P., Ng H. Y., other authors. 2014; Tropism and replication of Middle East respiratory syndrome coronavirus from dromedary camels in the human respiratory tract: an in-vitro and ex-vivo study. Lancet Respir Med 2:813–822 [View Article][PubMed]
     [Google Scholar]
  11. Chu D. K., Poon L. L., Gomaa M. M., Shehata M. M., Perera R. A., Abu Zeid D., El Rifay A. S., Siu L. Y., Guan Y., other authors. 2014; MERS coronaviruses in dromedary camels, Egypt. Emerg Infect Dis 20:1049–1053 [View Article][PubMed]
     [Google Scholar]
  12. Corman V. M., Ithete N. L., Richards L. R., Schoeman M. C., Preiser W., Drosten C., Drexler J. F. 2014a; Rooting the phylogenetic tree of Middle East respiratory syndrome coronavirus by characterization of a conspecific virus from an African bat. J Virol 88:11297–11303 [View Article][PubMed]
     [Google Scholar]
  13. Corman V. M., Jores J., Meyer B., Younan M., Liljander A., Said M. Y., Gluecks I., Lattwein E., Bosch B. J., other authors. 2014b; Antibodies against MERS coronavirus in dromedary camels, Kenya, 1992-2013. Emerg Infect Dis 20:1319–1322 [View Article][PubMed]
     [Google Scholar]
  14. de Groot R. J., Baker S. C., Baric R., Enjuanes L., Gorbalenya A. E., Holmes K. V., Perlman S., Poon L., Rottier P. J. M., other authors. 2011; Family Coronaviridae . In Virus Taxonomy, Ninth Report of the International Committee on Taxonomy of Viruses pp 806–828Edited by King A. M. Q., Adams M. J., Carstens E. B., Lefkowitz E. J. Oxford: Elsevier;
     [Google Scholar]
  15. Drosten C., Günther S., Preiser W., van der Werf S., Brodt H. R., Becker S., Rabenau H., Panning M., Kolesnikova L., other authors. 2003; Identification of a novel coronavirus in patients with severe acute respiratory syndrome. N Engl J Med 348:1967–1976 [View Article][PubMed]
     [Google Scholar]
  16. Drosten C., Seilmaier M., Corman V. M., Hartmann W., Scheible G., Sack S., Guggemos W., Kallies R., Muth D., other authors. 2013; Clinical features and virological analysis of a case of Middle East respiratory syndrome coronavirus infection. Lancet Infect Dis 13:745–751 [View Article][PubMed]
     [Google Scholar]
  17. Farag E. A., Reusken C. B., Haagmans B. L., Mohran K. A., Stalin Raj V., Pas S. D., Voermans J., Smits S. L., Godeke G. J., other authors. 2015; High proportion of MERS-CoV shedding dromedaries at slaughterhouse with a potential epidemiological link to human cases, Qatar 2014. Infect Ecol Epidemiol 5:28305[PubMed]
     [Google Scholar]
  18. Faye B., Madani H., El-Rouili S. 2014; Camel milk value chain in Northern Saudi Arabia. Emirates J Food Agric 26:359–365
     [Google Scholar]
  19. Ge X. Y., Li J. L., Yang X. L., Chmura A. A., Zhu G., Epstein J. H., Mazet J. K., Hu B., Zhang W., other authors. 2013; Isolation and characterization of a bat SARS-like coronavirus that uses the ACE2 receptor. Nature 503:535–538 [View Article][PubMed]
     [Google Scholar]
  20. Goh G. K., Dunker A. K., Uversky V. 2013 [View Article][PubMed] Prediction of intrinsic disorder in MERS-CoV/HCoV-EMC supports a high oral–fecal transmission. PLoS Curr Outbreaks
     [Google Scholar]
  21. Guan Y., Zheng B. J., He Y. Q., Liu X. L., Zhuang Z. X., Cheung C. L., Luo S. W., Li P. H., Zhang L. J., other authors. 2003; Isolation and characterization of viruses related to the SARS coronavirus from animals in southern China. Science 302:276–278 [View Article][PubMed]
     [Google Scholar]
  22. Haagmans B. L., Al Dhahiry S. H., Reusken C. B., Raj V. S., Galiano M., Myers R., Godeke G. J., Jonges M., Farag E., other authors. 2014; Middle East respiratory syndrome coronavirus in dromedary camels: an outbreak investigation. Lancet Infect Dis 14:140–145 [View Article][PubMed]
     [Google Scholar]
  23. Hemida M. G., Perera R. A., Wang P., Alhammadi M. A., Siu L. Y., Li M., Poon L. L., Saif L., Alnaeem A., Peiris M. 2013; Middle East Respiratory Syndrome (MERS) coronavirus seroprevalence in domestic livestock in Saudi Arabia, 2010 to 2013. Euro Surveill 18:20659 [CrossRef]
     [Google Scholar]
  24. Hemida M. G., Chu D. K., Poon L. L., Perera R. A., Alhammadi M. A., Ng H. Y., Siu L. Y., Guan Y., Alnaeem A., Peiris M. 2014; MERS coronavirus in dromedary camel herd, Saudi Arabia. Emerg Infect Dis 20:1231–1234 [View Article][PubMed]
     [Google Scholar]
  25. Hemida M. G., Al-Naeem A., Perera R. A., Chin A. W., Poon L. L., Peiris M. 2015; Lack of Middle East respiratory syndrome coronavirus transmission from infected camels. Emerg Infect Dis 21:699–701 [View Article][PubMed]
     [Google Scholar]
  26. Ithete N. L., Stoffberg S., Corman V. M., Cottontail V. M., Richards L. R., Schoeman M. C., Drosten C., Drexler J. F., Preiser W. 2013; Close relative of human Middle East respiratory syndrome coronavirus in bat, South Africa. Emerg Infect Dis 19:1697–1699 [View Article][PubMed]
     [Google Scholar]
  27. Ksiazek T. G., Erdman D., Goldsmith C. S., Zaki S. R., Peret T., Emery S., Tong S., Urbani C., Comer J. A., other authors. 2003; A novel coronavirus associated with severe acute respiratory syndrome. N Engl J Med 348:1953–1966 [View Article][PubMed]
     [Google Scholar]
  28. Lai M. M. C., Perlman S., Anderson L. J. 2007; Coronaviridae. In Fields Virology pp 1305–1336Edited by Knipe P. M. H. D. M., Griffin D. E., Martin M. A., Lamb R. A., Roizman B., Straus S. E. Philadelphia PA: Lippincott Williams, Wilkins;
     [Google Scholar]
  29. Lau S. K., Woo P. C., Li K. S., Huang Y., Tsoi H. W., Wong B. H., Wong S. S., Leung S. Y., Chan K. H., Yuen K. Y. 2005; Severe acute respiratory syndrome coronavirus-like virus in Chinese horseshoe bats. Proc Natl Acad Sci U S A 102:14040–14045 [View Article][PubMed]
     [Google Scholar]
  30. Lee S. S., Wong N. S. 2015; Probable transmission chains of MERS-CoV and the multiple generations of secondary infections in South Korea. Int J Infect Dis 38:65–67 [CrossRef]
     [Google Scholar]
  31. Li W., Shi Z., Yu M., Ren W., Smith C., Epstein J. H., Wang H., Crameri G., Hu Z., other authors. 2005; Bats are natural reservoirs of SARS-like coronaviruses. Science 310:676–679 [View Article][PubMed]
     [Google Scholar]
  32. Lu R., Yu X., Wang W., Duan X., Zhang L., Zhou W., Xu J., Xu L., Hu Q., other authors. 2012; Characterization of human coronavirus etiology in Chinese adults with acute upper respiratory tract infection by real-time RT-PCR assays. PLoS One 7:e38638 [View Article][PubMed]
     [Google Scholar]
  33. Memish Z. A., Mishra N., Olival K. J., Fagbo S. F., Kapoor V., Epstein J. H., Alhakeem R., Durosinloun A., Al Asmari M., other authors. 2013a; Middle East respiratory syndrome coronavirus in bats, Saudi Arabia. Emerg Infect Dis 19:1819–1823 [View Article][PubMed]
     [Google Scholar]
  34. Memish Z. A., Zumla A. I., Al-Hakeem R. F., Al-Rabeeah A. A., Stephens G. M. 2013b; Family cluster of Middle East respiratory syndrome coronavirus infections. N Engl J Med 368:2487–2494 [View Article][PubMed]
     [Google Scholar]
  35. Memish Z. A., Cotten M., Meyer B., Watson S. J., Alsahafi A. J., Al Rabeeah A. A., Corman V. M., Sieberg A., Makhdoom H. Q., other authors. 2014; Human infection with MERS coronavirus after exposure to infected camels, Saudi Arabia, 2013. Emerg Infect Dis 20:1012–1015 [View Article][PubMed]
     [Google Scholar]
  36. Memish Z. A., Alsahly A., Masri M. A., Heil G. L., Anderson B. D., Peiris M., Khan S. U., Gray G. C. 2015; Sparse evidence of MERS-CoV infection among animal workers living in Southern Saudi Arabia during 2012. Influenza Other Respi Viruses 9:64–67 [View Article][PubMed]
     [Google Scholar]
  37. Meyer B., Müller M. A., Corman V. M., Reusken C. B., Ritz D., Godeke G. J., Lattwein E., Kallies S., Siemens A., other authors. 2014; Antibodies against MERS coronavirus in dromedary camels, United Arab Emirates, 2003 and 2013. Emerg Infect Dis 20:552–559 [View Article][PubMed]
     [Google Scholar]
  38. Milne-Price S., Miazgowicz K. L., Munster V. J. 2014; The emergence of the Middle East respiratory syndrome coronavirus. Pathog Dis 71:121–136 [View Article][PubMed]
     [Google Scholar]
  39. Müller M. A., Raj V. S., Muth D., Meyer B., Kallies S., Smits S. L., Wollny R., Bestebroer T. M., Specht S., other authors. 2012; Human coronavirus EMC does not require the SARS-coronavirus receptor and maintains broad replicative capability in mammalian cell lines. MBio 3:e00515–e00512 [View Article][PubMed]
     [Google Scholar]
  40. Müller M. A., Corman V. M., Jores J., Meyer B., Younan M., Liljander A., Bosch B. J., Lattwein E., Hilali M., other authors. 2014; MERS coronavirus neutralizing antibodies in camels, Eastern Africa, 1983-1997. Emerg Infect Dis 20:2093–2095 [View Article][PubMed]
     [Google Scholar]
  41. Müller M. A., Meyer B., Corman V. M., Al-Masri M., Turkestani A., Ritz D., Sieberg A., Aldabbagh S., Bosch B. J., other authors. 2015; Presence of Middle East respiratory syndrome coronavirus antibodies in Saudi Arabia: a nationwide, cross-sectional, serological study. Lancet Infect Dis 15:559–564 [View Article][PubMed]
     [Google Scholar]
  42. Nowotny N., Kolodziejek J. 2014; Middle East respiratory syndrome coronavirus (MERS-CoV) in dromedary camels, Oman, 2013. Euro Surveill 19:20781 [CrossRef]
     [Google Scholar]
  43. Oboho I. K., Tomczyk S. M., Al-Asmari A. M., Banjar A. A., Al-Mugti H., Aloraini M. S., Alkhaldi K. Z., Almohammadi E. L., Alraddadi B. M., other authors. 2015; 2014 MERS-CoV outbreak in Jeddah – a link to health care facilities. N Engl J Med 372:846–854 [View Article][PubMed]
     [Google Scholar]
  44. Perera R. A., Wang P., Gomaa M. R., El-Shesheny R., Kandeil A., Bagato O., Siu L. Y., Shehata M. M., Kayed A. S., other authors. 2013; Seroepidemiology for MERS coronavirus using microneutralisation and pseudoparticle virus neutralisation assays reveal a high prevalence of antibody in dromedary camels in Egypt, June 2013. Euro Surveill 18:20574 [CrossRef]
     [Google Scholar]
  45. Raj V. S., Mou H., Smits S. L., Dekkers D. H., Müller M. A., Dijkman R., Muth D., Demmers J. A., Zaki A., other authors. 2013; Dipeptidyl peptidase 4 is a functional receptor for the emerging human coronavirus-EMC. Nature 495:251–254 [View Article][PubMed]
     [Google Scholar]
  46. Raj V. S., Farag E. A., Reusken C. B., Lamers M. M., Pas S. D., Voermans J., Smits S. L., Osterhaus A. D., Al-Mawlawi N., other authors. 2014; Isolation of MERS coronavirus from a dromedary camel, Qatar, 2014. Emerg Infect Dis 20:1339–1342 [View Article][PubMed]
     [Google Scholar]
  47. Reusken C. B., Ababneh M., Raj V. S., Meyer B., Eljarah A., Abutarbush S., Godeke G. J., Bestebroer T. M., Zutt I., other authors. 2013a; Middle East Respiratory Syndrome coronavirus (MERS-CoV) serology in major livestock species in an affected region in Jordan, June to September 2013. Euro Surveill 18:20662 [CrossRef]
     [Google Scholar]
  48. Reusken C. B., Haagmans B. L., Müller M. A., Gutierrez C., Godeke G. J., Meyer B., Muth D., Raj V. S., Smits-De Vries L., other authors. 2013b; Middle East respiratory syndrome coronavirus neutralising serum antibodies in dromedary camels: a comparative serological study. Lancet Infect Dis 13:859–866 [View Article][PubMed]
     [Google Scholar]
  49. Reusken C. B., Farag E. A., Jonges M., Godeke G. J., El-Sayed A. M., Pas S. D., Raj V. S., Mohran K. A., Moussa H. A., other authors. 2014a; Middle East respiratory syndrome coronavirus (MERS-CoV) RNA and neutralising antibodies in milk collected according to local customs from dromedary camels, Qatar, April 2014. Euro Surveill 19:20829 [CrossRef]
     [Google Scholar]
  50. Reusken C. B., Messadi L., Feyisa A., Ularamu H., Godeke G. J., Danmarwa A., Dawo F., Jemli M., Melaku S., other authors. 2014b; Geographic distribution of MERS coronavirus among dromedary camels, Africa. Emerg Infect Dis 20:1370–1374 [View Article][PubMed]
     [Google Scholar]
  51. Reusken C. B., Farag E. A., Haagmans B. L., Mohran K. A., Godeke G. J., Raj V, Alhajri S., Al-Marri F., Al-Romaihi S. A., other authors H. E. 2015; Occupational exposure to dromedaries and risk for MERS-CoV infection, Qatar, 2013-2014. Emerg Infect Dis 21:1422–1425 [View Article][PubMed]
     [Google Scholar]
  52. van Boheemen S., de Graaf M., Lauber C., Bestebroer T. M., Raj V. S., Zaki A. M., Osterhaus A. D., Haagmans B. L., Gorbalenya A. E., other authors. 2012; Genomic characterization of a newly discovered coronavirus associated with acute respiratory distress syndrome in humans. MBio 3:e00473–12 [View Article][PubMed]
     [Google Scholar]
  53. van der Hoek L., Pyrc K., Jebbink M. F., Vermeulen-Oost W., Berkhout R. J., Wolthers K. C., Wertheim-van Dillen P. M., Kaandorp J., Spaargaren J., Berkhout B. 2004; Identification of a new human coronavirus. Nat Med 10:368–373 [View Article][PubMed]
     [Google Scholar]
  54. van Doremalen N., Bushmaker T., Munster V. J. 2013; Stability of Middle East respiratory syndrome coronavirus (MERS-CoV) under different environmental conditions. Euro Surveill 18:20590 [CrossRef]
     [Google Scholar]
  55. van Doremalen N., Bushmaker T., Karesh W. B., Munster V. J. 2014; Stability of Middle East respiratory syndrome coronavirus in milk. Emerg Infect Dis 20:1263–1264 [View Article][PubMed]
     [Google Scholar]
  56. Wang Q., Qi J., Yuan Y., Xuan Y., Han P., Wan Y., Ji W., Li Y., Wu Y., other authors. 2014; Bat origins of MERS-CoV supported by bat coronavirus HKU4 usage of human receptor CD26. Cell Host Microbe 16:328–337 [View Article][PubMed]
     [Google Scholar]
  57. Wernery U., Corman V. M., Wong E. Y., Tsang A. K., Muth D., Lau S. K., Khazanehdari K., Zirkel F., Ali M., other authors. 2015; Acute Middle East respiratory syndrome coronavirus infection in livestock Dromedaries, Dubai, 2014. Emerg Infect Dis 21:1019–1022 [View Article][PubMed]
     [Google Scholar]
  58. Wevers B. A., van der Hoek L. 2009; Recently discovered human coronaviruses. Clin Lab Med 29:715–724 [View Article][PubMed]
     [Google Scholar]
  59. WHO 2004; Summary of probable SARS cases with onset of illness from 1 November 2002 to 31 July 2003. http://www.who.int/csr/sars/country/table2004_04_21/en/. Accessed 18 August 2015.
  60. WHO 2015; Middle East respiratory syndrome coronavirus (MERS-CoV): Summary of Current Situation, Literature Update and Risk Assessment – as of 7 July 2015. http://www.who.int/csr/disease/coronavirus_infections/risk-assessment-7july2015/en/. Accessed 18 August 2015.
  61. Woo P. C., Lau S. K., Chu C. M., Chan K. H., Tsoi H. W., Huang Y., Wong B. H., Poon R. W., Cai J. J., other authors. 2005; Characterization and complete genome sequence of a novel coronavirus, coronavirus HKU1, from patients with pneumonia. J Virol 79:884–895 [View Article][PubMed]
     [Google Scholar]
  62. Woo P. C., Lau S. K., Lam C. S., Lau C. C., Tsang A. K., Lau J. H., Bai R., Teng J. L., Tsang C. C., other authors. 2012; Discovery of seven novel Mammalian and avian coronaviruses in the genus deltacoronavirus supports bat coronaviruses as the gene source of alphacoronavirus and betacoronavirus and avian coronaviruses as the gene source of gammacoronavirus and deltacoronavirus. J Virol 86:3995–4008 [View Article][PubMed]
     [Google Scholar]
  63. Yang L., Wu Z., Ren X., Yang F., Zhang J., He G., Dong J., Sun L., Zhu Y., other authors. 2014; MERS-related betacoronavirus in Vespertilio superans bats, China. Emerg Infect Dis 20:1260–1262 [View Article][PubMed]
     [Google Scholar]
  64. Zaki A. M., van Boheemen S., Bestebroer T. M., Osterhaus A. D., Fouchier R. A. 2012; Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia. N Engl J Med 367:1814–1820 [View Article][PubMed]
     [Google Scholar]
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