Drivers of MERS-CoV transmission: What do we know?

Expert Review of Respiratory Medicine

Volumn 10, Issue 3, 2016, Pages 331-338

  Al Tawfiq, Jaffar A ^a,b   Memish, Ziad A ^c,d  

^a DHAHRAN HEALTH CENTER   (Saudi Arabia)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c MINISTRY OF HEALTH   (Saudi Arabia)

^d ALFAISAL UNIVERSITY   (Saudi Arabia)

Author keywords

Coronavirus; Health Care Facilities; MERS CoV; Prevention; Transmission

Indexed keywords

ENVIRONMENTAL FACTOR; HEALTH CARE PERSONNEL; HEALTHCARE ASSOCIATED INFECTION; HUMAN; INFECTION CONTROL; MIDDLE EAST RESPIRATORY SYNDROME CORONAVIRUS; NONHUMAN; REVIEW; RISK FACTOR; SEASONAL VARIATION; VIRUS SHEDDING; VIRUS TRANSMISSION; ANIMAL; COMMUNITY-ACQUIRED INFECTIONS; CORONAVIRUS INFECTIONS; CROSS INFECTION; EPIDEMIC; HOST PATHOGEN INTERACTION; PATHOGENICITY; PROCEDURES; TRANSMISSION; VIROLOGY; ZOONOSES;

ANIMALS; COMMUNITY-ACQUIRED INFECTIONS; CORONAVIRUS INFECTIONS; CROSS INFECTION; DISEASE OUTBREAKS; HOST-PATHOGEN INTERACTIONS; HUMANS; INFECTION CONTROL; MIDDLE EAST RESPIRATORY SYNDROME CORONAVIRUS; RISK FACTORS; ZOONOSES;

EID: 84960371400     PISSN: 17476348     EISSN: 17476356     Source Type: Journal    
DOI: 10.1586/17476348.2016.1150784     Document Type: Review

References (98)

1. World Health Organization. Available from: http://www.who.int/emergencies/mers-cov/en/
2. Memish ZA, Zumla AI, Al-Hakeem RF, et al. Family cluster of middle east respiratory syndrome coronavirus infections. N Engl J Med. 2013;368(26):2487-2494.
3. Omrani AS, Matin MA, Haddad Q, et al. A family cluster of middle east respiratory syndrome coronavirus infections related to a likely unrecognized asymptomatic or mild case. Int J Infect Dis. 2013;17 (9):e668-e672.
4. Abroug F, Slim A, Ouanes-Besbes L, et al. Family cluster of middle east respiratory syndrome coronavirus infections, Tunisia, 2013. Emerg Infect Dis. 2014;20(9):1527-1530.
5. Oboho IK, Tomczyk SM, Al-Asmari AM, et al. 2014 MERS-CoV outbreak in Jeddah-a link to health care facilities. N Engl J Med. 2015;372(9):846-854.
6. Khalid M, Khan B, Al Rabiah F, et al. Middle eastern respiratory syndrome corona virus (MERS CoV): case reports from a tertiary care hospital in Saudi Arabia. Ann Saudi Med. 2014;34(5):396-400.
7. Assiri A, Al-Tawfiq JA, Al-Rabeeah AA, et al. Epidemiological, demographic, and clinical characteristics of 47 cases of middle east respiratory syndrome coronavirus disease from Saudi Arabia: a descriptive study. The Lancet Infectious Diseases. 2013;13:752-761.
8. Saad M, Omrani AS, Baig K, et al. Clinical aspects and outcomes of 70 patients with middle east respiratory syndrome coronavirus infection: a single-center experience in Saudi Arabia. Int J Infect Dis. 2014;29:301-306.
9. Al-Tawfiq JA, Hinedi K, Ghandour J, et al. Middle east respiratory syndrome-coronavirus (MERS-CoV): a case-control study of hospitalized patients. Clin Infect Dis. 2014;59(2):160-165.
10. Fagbo SF, Skakni L, Chu DK, et al. Molecular epidemiology of hospital outbreak of middle east respiratory syndrome, Riyadh, Saudi Arabia, 2014. Emerg Infect Dis. 2015;21(11):1981-1988.
11. Al-Hameed F, Wahla AS, Siddiqui S, et al. Characteristics and outcomes of middle east respiratory syndrome coronavirus patients admitted to an intensive care unit in Jeddah, Saudi Arabia. J Intensive Care Med. 2015 Apr 9. pii: 0885066615579858. [Epub ahead of print].
12. Arabi YM, Arifi AA, Balkhy HH, et al. Clinical course and outcomes of critically ill patients with middle east respiratory syndrome coronavirus infection. Ann Intern Med. 2014;160(6):389-397.
13. Assiri A, McGeer A, Perl TM, et al. Hospital outbreak of middle east respiratory syndrome coronavirus. N Engl J Med. 2013;369(5):407-416.
14. Omrani AS, Saad MM, Baig K, et al. Ribavirin and interferon alfa-2a for severe middle east respiratory syndrome coronavirus infection: a retrospective cohort study. Lancet Infect Dis. 2014;14(11):1090-1095.
15. Shalhoub S, Farahat F, Al-Jiffri A, et al. IFN-alpha2a or IFN-beta1a in combination with ribavirin to treat middle east respiratory syndrome coronavirus pneumonia: a retrospective study. J Antimicrob Chemother. 2015;70(7):2129-2132.
16. Feikin DR, Alraddadi B, Qutub M, et al. Association of higher MERSCoV virus load with severe disease and death, Saudi Arabia, 2014. Emerg Infect Dis. 2015;21(11):2029-2035.
17. Mizumoto K, Endo A, Chowell G, et al. Real-time characterization of risks of death associated with the middle east respiratory syndrome (MERS) in the Republic of Korea, 2015. BMC Med. 2015; 13:228. doi:10.1186/s12916-015-0468-3.
18. Memish ZA, Al-Tawfiq JA, Assiri A, et al. Middle east respiratory syndrome coronavirus disease in children. Pediatr Infect Dis J. 2014;33(9):904-906.
19. Khuri-Bulos N, Payne DC, Lu X, et al. Middle east respiratory syndrome coronavirus not detected in children hospitalized with acute respiratory illness in Amman, Jordan, March 2010 to September 2012. Clin Microbiol Infect. 2014;20(7):678-682.
20. Korea Centers for Disease Control and Prevention. Middle east respiratory syndrome coronavirus outbreak in the Republic of Korea, 2015. Osong Public Health Res Perspect. 2015;6(4):269-278.
21. Memish ZA, Al-Tawfiq JA, Makhdoom HQ, et al. Respiratory tract samples, viral load, and genome fraction yield in patients with middle east respiratory syndrome. J Infect Dis. 2014;210(10):1590-1594.
22. Corman VM, Albarrak AM, Omrani AS, et al. Viral shedding and antibody response in 37 patients with MERS-coronavirus infection. Clin Infect Dis. 2016 Feb 15;62(4):477-483.
23. Buchholz U, Muller MA, Nitsche A, et al. Contact investigation of a case of human novel coronavirus infection treated in a German hospital, October-November 2012. Euro Surveill. 2013;18(8). pii: 20406.
24. Müller MA, Meyer B, Corman VM, et al. Presence of middle east respiratory syndrome coronavirus antibodies in Saudi Arabia: a nationwide, cross-sectional, serological study. Lancet Infect Dis. 2015;15(5):559-564.
25. Drosten C, Meyer B, Müller MA, et al. Transmission of MERS-coronavirus in household contacts. N Engl J Med. 2014;371(9):828-835.
26. Reusken CB, Farag EA, Haagmans BL, et al. Occupational exposure to dromedaries and risk for MERS-CoV infection, Qatar, 2013-2014. Emerg Infect Dis. 2015;21(8):1422-1425.
27. Park SW, Perera RA, Choe PG, et al. Comparison of serological assays in human middle east respiratory syndrome (MERS)-coronavirus infection. Euro Surveill. 2015;20(41). doi:10.2807/1560-7917. ES.2015.20.41.30042.
28. Perera RA, Wang P, Gomaa MR, et al., et al. Seroepidemiology for MERS coronavirus using microneutralisation and pseudoparticle virus neutralization assays reveal a high prevalence of antibody in dromedary camels in Egypt, June 2013. Euro Surveill. 2013;18 (36):20574. doi:10.2807/1560-7917.ES2013.18.36.20574.
29. Hemida MG, Perera RA, Al Jassim RA, et al., et al. Seroepidemiology of middle east respiratory syndrome (MERS) coronavirus in Saudi Arabia (1993) and Australia (2014) and characterisation of assay specificity. Euro Surveill. 2014;19(23):20828. doi:10.2807/1560-7917. ES2014.19.23.20828.
30. Hemida MG, Al-Naeem A, Perera RA, et al. Lack of middle east respiratory syndrome coronavirus transmission from infected camels. Emerg Infect Dis. 2015;21(4):699-701. doi:10.3201/eid2104.141949.
31. Al-Tawfiq JA, Memish ZA. Managing MERS-CoV in the healthcare setting. Hosp Pract. 1995;43(3):158-163.
32. Al-Tawfiq JA, Perl TM. Middle east respiratory syndrome coronavirus in healthcare settings. Curr Opin Infect Dis. 2015;28(4):392-396.
33. Al-Tawfiq JA, Memish ZA. An update on middle east respiratory syndrome: 2 years later. Expert Rev Respir Med. 2015;9(3):327-335.
34. Memish ZA, Al-Tawfiq JA. Middle east respiratory syndrome coronavirus infection control: the missing piece? Am J Infect Control. 2014;42(12):1258-1260.
35. Al-Tawfiq JA, Memish ZA. Middle east respiratory syndrome coronavirus: transmission and phylogenetic evolution. Trends Microbiol. 2014;22(10):573-579.
36. Al-Tawfiq JA, Zumla A, Memish ZA. Coronaviruses: severe acute respiratory syndrome coronavirus and middle east respiratory syndrome coronavirus in travelers. Curr Opin Infect Dis. 2014;27 (5):411-417.
37. Al-Tawfiq JA, Memish ZA. Emerging respiratory viral infections: MERS-CoV and influenza. Lancet Respir Med. 2014;2(1):23-25.
38. Al-Tawfiq JA. Middle east respiratory syndrome-coronavirus infection: an overview. J Infect Public Health. 2013;6(5):319-322.
39. Saudi Ministry of Health. Available from: http://www.moh.gov.sa/en/CCC/PressReleases/Pages/Statistics-2015-11-05-001.aspx
40. Haagmans BL, Al Dhahiry SH, Reusken CB, et al. Middle east respiratory syndrome coronavirus in dromedary camels: an outbreak investigation. Lancet Infect Dis. 2014;14(2):140-145.
41. Memish ZA, Cotten M, Meyer B, et al. Human infection with MERS coronavirus after exposure to infected camels, Saudi Arabia, 2013. Emerg Infect Dis. 2014;20(6):1012-1015.
42. Hemida MG, Perera RA, Wang P, et al. Middle east respiratory syndrome (MERS) coronavirus seroprevalence in domestic livestock in Saudi Arabia, 2010 to 2013. Euro Surveill. 2013;18:20659.
43. Reusken CB, Ababneh M, Raj VS, et al. Middle east respiratory syndrome coronavirus (MERS-CoV) serology in major livestock species in an affected region in Jordan, June to September 2013. Euro Surveill. 2013;18:20662.
44. Meyer B, Müller MA, Corman VM, et al. Antibodies against MERS coronavirus in dromedary camels, United Arab Emirates, 2003 and 2013. Emerg Infect Dis. 2014;20:552-559.
45. Hemida MG, Elmoslemany A, Al-Hizab F, et al. Dromedary camels and the transmission of middle east respiratory syndrome coronavirus (MERS-CoV). Transbound Emerg Dis. 2015 Aug 10. doi:10.1111/tbed.12401. [Epub ahead of print].
46. Briese T, Mishra N, Jain K, et al. Middle east respiratory syndrome coronavirus quasispecies that include homologues of human isolates revealed through whole-genome analysis and virus cultured from dromedary camels in Saudi Arabia. MBio. 2014;5:e01146-14.
47. Nowotny N, Kolodziejek J. Middle east respiratory syndrome coronavirus (MERS-CoV) in dromedary camels, Oman, 2013. Euro Surveill. 2014;19:20781.
48. Chu DK, Poon LL, Gomaa MM, et al. MERS coronaviruses in dromedary camels, Egypt. Emerg Infect Dis. 2014;20:1049-1053.
49. Hemida MG, Chu DK, Poon LL, et al. MERS coronavirus in dromedary camel herd, Saudi Arabia. Emerg Infect Dis. 2014;20:1231-1234.
50. Raj VS, Farag EA, Reusken CB, et al. Isolation of MERS coronavirus from a dromedary camel, Qatar, 2014. Emerg Infect Dis. 2014;20:1339-1342.
51. Azhar EI, El-Kafrawy SA, Farraj SA, et al. Evidence for camel-tohuman transmission of MERS coronavirus. N Engl J Med. 2014;370:2499-2505.
52. Alraddadi BM, Watson JT, Almarashi A, et al. Risk factors for primary middle east respiratory syndrome coronavirus illness in humans, Saudi Arabia, 2014. Emerg Infect Dis. 2016;22(1):49-55. doi:10.3201/eid2201.151340.
53. Memish ZA, Mishra N, Olival KJ, et al. Middle east respiratory syndrome coronavirus in bats, Saudi Arabia. Emerg Infect Dis. 2013;19(11):1819-1823.
54. MERS-Coronavirus Molecular Epidemiology and Genetic Analysis - Origin and Evolution. Available from: http://epidemic.bio.ed.ac.uk
55. World Health Organization. Available from: http://www.who.int/csr/disease/coronavirus-infections/MERS-CoV-RA-20140424.pdf
56. World Health Organization. Available from: http://www.who.int/csr/disease/coronavirus-infections/mers-5-february-2015.pdf
57. Drosten C, Muth D, Corman VM, et al. An observational, laboratorybased study of outbreaks of middle east respiratory syndrome coronavirus in Jeddah and Riyadh, kingdom of Saudi Arabia, 2014. Clin Infect Dis. 2015;60(3):369-377.
58. Hijawi B, Abdallat M, Sayaydeh A, et al. Novel coronavirus infections in Jordan, April 2012: epidemiological findings from a retrospective investigation. East Mediterr Health J. 2013;19(Suppl 1): S12-S18.
59. Memish ZA, Al-Tawfiq JA, Alhakeem RF, et al. Middle east respiratory syndrome coronavirus (MERS-CoV): A cluster analysis with implications for global management of suspected cases. Travel Med Infect Dis. 2015;13(4):311-314.
60. Kraaij-Dirkzwager M, Timen A, Dirksen K, et al., et al. Middle east respiratory syndrome coronavirus (MERS-CoV) infections in two returning travellers in the Netherlands, May 2014. Euro Surveill. 2014;19(23). pii: 20829.
61. Fanoy EB, Van Der Sande MA, Kraaij-Dirkzwager M, et al. Travelrelated MERS-CoV cases: an assessment of exposures and risk factors in a group of Dutch travellers returning from the Kingdom of Saudi Arabia, May 2014. Emerg Themes Epidemiol. 2014;11:16.
62. Pro MED-mail. MERS-CoV - eastern Mediterranean (73): Saudi Arabia, Algeria, Jordan, WHO, RFI. Archive Number: 20140601.2512766. Published Date: 2014-06-0119:27:25
63. Pro MED-mail. MERS-CoV - eastern Mediterranean (80): S Arabia, Iran, Algeria, Tunisia. Archive Number: 20140612.2534478. Published Date: 2014-06-12 10:00:39
64. Pro MED-mail. MERS-CoV (01): Bangladesh, KSA, Algeria, UAE, Iran, WHO, RFI. Archive Number: 20140616.2541707. Published Date: 2014-06-16 15:12:09
65. Lee SS, Wong NS. Probable transmission chains of middle east respiratory syndrome coronavirus and the multiple generations of secondary infection in South Korea. Int J Infect Dis. 2015;38:65-67.
66. Ki M. 2015 MERS outbreak in Korea: hospital-to-hospital transmission. Epidemiol Health. 2015;37:e2015033.
67. Park HY, Lee EJ, Ryu YW, et al. Epidemiological investigation of MERS-CoV spread in a single hospital in South Korea, May to June 2015. Eurosurveillance. 2015;20:21169.
68. Petersen E, Pollack MM, Madoff LC. Health-care associate transmission of middle east respiratory syndrome corona virus, MERS-CoV, in the Kingdom of Saudi Arabia. Int J Infect Dis. 2014;29:299-300.
69. Hall AJ, Tokars JI, Badreddine SA, et al. Health care worker contact with MERS patient, Saudi Arabia. Emerg Infect Dis. 2014;20 (12):2148-2151.
70. Al-Abdallat MM, Payne DC, Alqasrawi S, et al. Hospital-associated outbreak of middle east respiratory syndrome coronavirus: a serologic, epidemiologic, and clinical description. Clin Infect Dis. 2014;59(9):1225-1233.
71. Assiri A, Abedi GR, Bin Saeed AA, et al., et al. Multifacility outbreak of middle east respiratory syndrome in Taif, Saudi Arabia. Emerg Infect Dis. 2016;22:32-40. doi:10.3201/eid2201.151370.
72. Memish ZA, Cotten M, Watson SJ, et al. Community case clusters of middle east respiratory syndrome coronavirus in Hafr Al-Batin, Kingdom of Saudi Arabia: a descriptive genomic study. Int J Infect Dis. 2014;23:63-68.
73. Memish ZA, Al-Tawfiq JA, Makhdoom HQ, et al. Screening for middle east respiratory syndrome coronavirus infection in hospital patients and their healthcare worker and family contacts: a prospective descriptive study. Clin Microbiol Infect. 2014;20(5):469-474.
74. Cotten M, Watson SJ, Kellam P, et al., et al. Transmission and evolution of the middle east respiratory syndrome coronavirus in Saudi Arabia: a descriptive genomic study. Lancet. 2013;382 (9909):1993-2002.
75. World Health Organization. Middle east respiratory syndrome coronavirus (MERS-CoV) summary and literature update as of 9 May 2014. Available from: www.who.int/csr/disease/coronavirus-infections/MERS-CoV-Update-09-May-2014.pdf?ua=1
76. WHO. Middle east respiratory syndrome coronavirus (MERS-CoV) - Republic of Korea. Available from: http://www.who.int/csr/don/30-may-2015-mers-korea/en/
77. Flu Trackers. South Korea coronavirus MERS case list - including imported and exported cases. Available from: https://flutrackers.com/forum/forum/novel-coronavirus-ncov-mers-2012-2014/novelcoronavirus-who-chp-wpro-ecdc-oie-fao-moa-reports-and-updates/south-korea-coronavirus/732065-south-korea-coronavirus-merscase-list-including-imported-and-exported-cases
78. World Health Organization. Middle east respiratory syndrome coronavirus (MERS-CoV): summary and risk assessment of current situation in the Republic of Korea and China - as of 19 June 2015. Available from: http://www.who.int/emergencies/mers-cov/mers-cov-republic-of-korea-and-china-risk-assessment-19-June- 2015.pdf?ua=1
79. World health organization. Middle east respiratory syndrome coronavirus (MERS-CoV). MERS-CoV in Republic of Korea at a glance. Available from: http://www.wpro.who.int/outbreaks-emergencies/wpro-coronavirus/en/
80. Cowling BJ, Park M, Fang VJ, et al. Preliminary epidemiological assessment of MERS-CoV outbreak in South Korea, May to June 2015. Euro Surveill. 2015;20(25):7-13.
81. Hsieh Y-H. 2015 middle east respiratory syndrome coronavirus (MERS-CoV) nosocomial outbreak in South Korea: insights from modeling. Peer J. 2015;3:e1505.
82. Shen Z, Ning F, Zhou W, et al. Superspreading SARS events, Beijing, 2003. Emerg Infect Dis. 2004;10(2):256-260.
83. Lloyd-Smith JO, Schreiber SJ, Kopp PE, et al. Superspreading and the effect of individual variation on disease emergence. Nature. 2005;438(7066):355-359.
84. James A, Pitchford JW, Plank MJ. An event-based model of superspreading in epidemics. Proc Biol Sci. 2007;274(1610):741-747.
85. Gopinath S, Lichtman JS, Bouley DM, et al. Role of disease-associated tolerance in infectious superspreaders. Proc Natl Acad Sci USA. 2014;111:15780-15785.
86. Leavy O. Infectious disease: the tolerance of superspreaders. Nat Rev Immunol. 2014;14(12):776-777.
87. WHO (World Health Organization). Severe acute respiratory syndrome (SARS): status of the outbreak and lessons for the immediate future. Report; Geneva. 2003 [cited 2003 May 20]. Available from: http://www.who.int/csr/media/sars-wha.pdf
88. Oh M-D, Choe PG, Oh HS, et al. Middle east respiratory syndrome coronavirus superspreading event involving 81 persons, Korea 2015. J Korean Med Sci. 2015;30(11):1701-1705.
89. Memish ZA, Assiri AM, Al-Tawfiq JA. Middle east respiratory syndrome coronavirus (MERS-CoV) viral shedding in the respiratory tract: an observational analysis with infection control implications. Int J Infect Dis. 2014;29:307-308.
90. Kim YJ, Cho YJ, Kim DW, et al. Complete genome sequence of middle east respiratory syndrome coronavirus KOR/KNIH/002-05-2015, isolated in South Korea. Genome Announc. 2015;3. doi:10.1128/genomeA.00787-15.
91. Lu R, Wang Y, Wang W, et al., et al. Complete genome sequence of middle east respiratory syndrome coronavirus (MERS-CoV) from the first imported MERS-CoV case in China. Genome Announc. 2015;3: e00818-15. doi:10.1128/genomeA.00818-15.
92. Wang Y, Liu D, Shi W, et al. Origin and possible genetic recombination of the middle east respiratory syndrome coronavirus from the first imported case in China: phylogenetics and coalescence analysis. MBio. 2015;6:e01280-15. doi:10.1128/mBio.01280-1.
93. Al-Gethamy M, Corman VM, Hussain R, et al. A case of long-term excretion and subclinical infection with middle east respiratory syndrome coronavirus in a healthcare worker. Clin Infect Dis. 2015;60(6):973-974.
94. Van Doremalen N, Bushmaker T, Munster VJ. Stability of middle east respiratory syndrome coronavirus (MERS-CoV) under different environmental conditions. Euro Surveill. 2013;18(38):20590. pii: 20590.
95. Bin Seo Y, Heo JY, Song MS, et al. Environmental contamination and viral shedding in MERS patients during MERS-CoV outbreak in South Korea. Clin Infect Dis. 2015 Dec 17. pii: civ1020. [Epub ahead of print].
96. Wong G, Liu W, Liu Y, et al. MERS, SARS, and Ebola: the role of super-spreaders in infectious disease. Cell Host Microbe. 2015;18 (4):398-401.
97. Wortmann GW. Middle east respiratory syndrome: SARS redux? Cleve Clin J Med. 2015;82(9):584-588.
98. Spanakis N, Tsiodras S, Haagmans BL, et al. Virological and serological analysis of a recent middle east respiratory syndrome coronavirus infection case on a triple combination antiviral regimen. Int J Antimicrob Agents. 2014;44(6):528-532.