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Semin Respir Crit Care Med 2020; 41(04): 568-578
DOI: 10.1055/s-0040-1709160
Review Article
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Middle East Respiratory Syndrome Coronavirus and Severe Acute Respiratory Syndrome Coronavirus

Jaffar A. Al-Tawfiq
1   Johns Hopkins Aramco Healthcare, Dhahran, Saudi Arabia
2   Infectious Disease Division, Department of Medicine, Indiana University School of Medicine, Indianapolis, Indiana
3   Infectious Disease Division, Department of Medicine, Johns Hopkins University School of Medicine, Baltimore, Maryland
,
Ziad A. Memish
4   Director Research & Innovation Center, Research Center Department, King Saud Medical City, Ministry of Health, Riyadh, Saudi Arabia
5   Department of Medicine, Al-Faisal University, Riyadh, Saudi Arabia
6   Hubert Department of Global Health, Rollins School of Public Health, Emory University, Atlanta, Georgia
› Author Affiliations
Further Information

Publication History

Publication Date:
18 April 2020 (online)

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Abstract

Emerging infectious diseases continue to be of a significant importance worldwide with the potential to cause major outbreaks and global pandemics. In 2002, the world had witnessed the appearance of the severe acute respiratory syndrome coronavirus in China which disappeared abruptly within 6 months. About a decade later, a new and emerging novel coronavirus named the Middle East respiratory syndrome coronavirus (MERS-CoV) was described in a patient from Saudi Arabia. These two coronaviruses shared multiple similarities in the epidemiology, clinical presentations, and posed challenges in its prevention and management. Seven years since its discovery, MERS-CoV continues to be a lethal zoonotic pathogen capable of causing severe pneumonia with high case fatality rates and the ability to cause large health care-associated outbreaks.

Keywords

MERS - Middle East respiratory syndrome coronavirus - epidemiology - control measures - transmission - Saudi Arabia
 

  • References

  • 1 Lee N, Hui D, Wu A. , et al. A major outbreak of severe acute respiratory syndrome in Hong Kong. N Engl J Med 2003; 348 (20) 1986-1994
    CrossrefPubMedGoogle Scholar
  • 2 Shaw K. The 2003 SARS outbreak and its impact on infection control practices. Public Health 2006; 120 (01) 8-14
    PubMedGoogle Scholar
  • 3 Zaki AM, van Boheemen S, Bestebroer TM, Osterhaus AD, Fouchier RA. Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia. N Engl J Med 2012; 367 (19) 1814-1820
    CrossrefPubMedGoogle Scholar
  • 4 Corman VM, Eckerle I, Bleicker T. , et al. Detection of a novel human coronavirus by real-time reverse-transcription polymerase chain reaction. Euro Surveill 2012; 17 (39) 17
    CrossrefPubMedGoogle Scholar
  • 5 de Groot RJ, Baker SC, Baric RS. , et al. Middle East respiratory syndrome coronavirus (MERS-CoV): announcement of the Coronavirus Study Group. J Virol 2013; 87 (14) 7790-7792
    CrossrefPubMedGoogle Scholar
  • 6 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 (05) 411-417
    CrossrefPubMedGoogle Scholar
  • 7 Al-Tawfiq JA, Zumla A, Gautret P. , et al. Surveillance for emerging respiratory viruses. Lancet Infect Dis 2014; 14 (10) 992-1000
    CrossrefPubMedGoogle Scholar
  • 8 Wolfe ND, Dunavan CP, Diamond J. Origins of major human infectious diseases. Nature 2007; 447 (7142): 279-283
    PubMedGoogle Scholar
  • 9 Tyrrell DA, Bynoe ML. Cultivation of a novel type of common-cold virus in organ cultures. BMJ 1965; 1 (5448): 1467-1470
    CrossrefPubMedGoogle Scholar
  • 10 Chan JF, Lau SK, To KK, Cheng VC, Woo PC, Yuen K-Y. Middle East respiratory syndrome coronavirus: another zoonotic betacoronavirus causing SARS-like disease. Clin Microbiol Rev 2015; 28 (02) 465-522
    CrossrefPubMedGoogle Scholar
  • 11 Drosten C, Günther S, Preiser W. , et al. Identification of a novel coronavirus in patients with severe acute respiratory syndrome. N Engl J Med 2003; 348 (20) 1967-1976
    CrossrefPubMedGoogle Scholar
  • 12 Kuiken T, Fouchier RA, Schutten M. , et al. Newly discovered coronavirus as the primary cause of severe acute respiratory syndrome. Lancet 2003; 362 (9380): 263-270
    CrossrefPubMedGoogle Scholar
  • 13 van Boheemen S, de Graaf M, Lauber C. , et al. Genomic characterization of a newly discovered coronavirus associated with acute respiratory distress syndrome in humans. MBio 2012; 3 (06) e00473-e12
    CrossrefPubMedGoogle Scholar
  • 14 Cheng VC, Lau SK, Woo PC, Yuen KY. Severe acute respiratory syndrome coronavirus as an agent of emerging and reemerging infection. Clin Microbiol Rev 2007; 20 (04) 660-694
    CrossrefPubMedGoogle Scholar
  • 15 Ksiazek TG, Erdman D, Goldsmith CS. , et al; SARS Working Group. A novel coronavirus associated with severe acute respiratory syndrome. N Engl J Med 2003; 348 (20) 1953-1966
    CrossrefPubMedGoogle Scholar
  • 16 Leung GM, Hedley AJ, Ho L-M. , et al. The epidemiology of severe acute respiratory syndrome in the 2003 Hong Kong epidemic: an analysis of all 1755 patients. Ann Intern Med 2004; 141 (09) 662-673
    CrossrefPubMedGoogle Scholar
  • 17 Tsang KW, Ho PL, Ooi GC. , et al. A cluster of cases of severe acute respiratory syndrome in Hong Kong. N Engl J Med 2003; 348 (20) 1977-1985
    CrossrefPubMedGoogle Scholar
  • 18 Poutanen SM, Low DE, Henry B. , et al; National Microbiology Laboratory, Canada; Canadian Severe Acute Respiratory Syndrome Study Team. Identification of severe acute respiratory syndrome in Canada. N Engl J Med 2003; 348 (20) 1995-2005
    CrossrefPubMedGoogle Scholar
  • 19 Centers for Disease Control and Prevention (CDC). Outbreak of severe acute respiratory syndrome–worldwide, 2003. MMWR Morb Mortal Wkly Rep 2003; 52 (11) 226-228
    PubMedGoogle Scholar
  • 20 Centers for Disease Control and Prevention (CDC). Preliminary clinical description of severe acute respiratory syndrome. MMWR Morb Mortal Wkly Rep 2003; 52 (12) 255-256
    PubMedGoogle Scholar
  • 21 Centers for Disease Control and Prevention (CDC). Update: severe acute respiratory syndrome–United States, June 4, 2003. MMWR Morb Mortal Wkly Rep 2003; 52 (22) 525-526
    PubMedGoogle Scholar
  • 22 Centers for Disease Control and Prevention (CDC). Severe acute respiratory syndrome (SARS) and coronavirus testing–United States, 2003. MMWR Morb Mortal Wkly Rep 2003; 52 (14) 297-302
    PubMedGoogle Scholar
  • 23 Centers for Disease Control and Prevention (CDC). Severe acute respiratory syndrome–Singapore, 2003. MMWR Morb Mortal Wkly Rep 2003; 52 (18) 405-411
    PubMedGoogle Scholar
  • 24 Parashar UD, Anderson LJ. Severe acute respiratory syndrome: review and lessons of the 2003 outbreak. Int J Epidemiol 2004; 33 (04) 628-634
    CrossrefPubMedGoogle Scholar
  • 25 World Health Organization (WHO). Summary of probable SARS cases with onset of illness from 1 November 2002 to 31 July 2003. WHO; 2015
    Google Scholar
  • 26 Chiang C-H, Shih J-F, Su W-J, Perng R-P. Eight-month prospective study of 14 patients with hospital-acquired severe acute respiratory syndrome. Mayo Clin Proc 2004; 79 (11) 1372-1379
    CrossrefPubMedGoogle Scholar
  • 27 Sung JJ, Wu A, Joynt GM. , et al. Severe acute respiratory syndrome: report of treatment and outcome after a major outbreak. Thorax 2004; 59 (05) 414-420
    CrossrefPubMedGoogle Scholar
  • 28 Hsu L-Y, Lee C-C, Green JA. , et al. Severe acute respiratory syndrome (SARS) in Singapore: clinical features of index patient and initial contacts. Emerg Infect Dis 2003; 9 (06) 713-717
    CrossrefPubMedGoogle Scholar
  • 29 Peiris JS, Chu CM, Cheng VC. , et al; HKU/UCH SARS Study Group. Clinical progression and viral load in a community outbreak of coronavirus-associated SARS pneumonia: a prospective study. Lancet 2003; 361 (9371): 1767-1772
    CrossrefPubMedGoogle Scholar
  • 30 Booth CM, Matukas LM, Tomlinson GA. , et al. Clinical features and short-term outcomes of 144 patients with SARS in the greater Toronto area. [see comment] [erratum appears in JAMA 2003 Jul 16;290(3):334] JAMA 2003; 289 (21) 2801-2809
    CrossrefPubMedGoogle Scholar
  • 31 Kwan YW, Leung CW, Chiu MC. Diarrhoea as the presenting sign in an adolescent suffering from severe acute respiratory syndrome. Eur J Pediatr 2005; 164 (04) 227-230
    CrossrefPubMedGoogle Scholar
  • 32 Nuttall I, Dye C. Epidemiology. The SARS wake-up call. Science 2013; 339 (6125): 1287-1288
    CrossrefPubMedGoogle Scholar
  • 33 Nuttall I, Dye C. Epidemiology. The SARS wake-up call. Science 2013; 339 (6125): 1287-1288
    CrossrefPubMedGoogle Scholar
  • 34 Cameron PA, Rainer TH. SARS: a wake up call for a health care system under stress. Emerg Med (Fremantle) 2003; 15 (5-6): 409-412
    CrossrefPubMedGoogle Scholar
  • 35 Lapinsky SE, Granton JT. Critical care lessons from severe acute respiratory syndrome. Curr Opin Crit Care 2004; 10 (01) 53-58
    CrossrefPubMedGoogle Scholar
  • 36 Leung CW, Chiu WK. Clinical picture, diagnosis, treatment and outcome of severe acute respiratory syndrome (SARS) in children. Paediatr Respir Rev 2004; 5 (04) 275-288
    CrossrefPubMedGoogle Scholar
  • 37 Guan Y, Zheng BJ, He YQ. , et al. Isolation and characterization of viruses related to the SARS coronavirus from animals in southern China. Science 2003; 302 (5643): 276-278
    CrossrefPubMedGoogle Scholar
  • 38 Centers for Disease Control and Prevention (CDC). Prevalence of IgG antibody to SARS-associated coronavirus in animal traders–Guangdong Province, China, 2003. MMWR Morb Mortal Wkly Rep 2003; 52 (41) 986-987
    PubMedGoogle Scholar
  • 39 Tsai M-H, Lin T-Y, Chiu C-H. , et al. Seroprevalence of SARS coronavirus among residents near a hospital with a nosocomial outbreak. J Formos Med Assoc 2008; 107 (11) 885-891
    CrossrefPubMedGoogle Scholar
  • 40 Ip M, Chan PK, Lee N. , et al. Seroprevalence of antibody to severe acute respiratory syndrome (SARS)-associated coronavirus among health care workers in SARS and non-SARS medical wards. Clin Infect Dis 2004; 38 (12) e116-e118
    CrossrefPubMedGoogle Scholar
  • 41 Leung GM, Lim WW, Ho LM. , et al. Seroprevalence of IgG antibodies to SARS-coronavirus in asymptomatic or subclinical population groups. Epidemiol Infect 2006; 134 (02) 211-221
    CrossrefPubMedGoogle Scholar
  • 42 Momattin H, Mohammed K, Zumla A, Memish ZA, Al-Tawfiq JA. Therapeutic options for Middle East respiratory syndrome coronavirus (MERS-CoV)–possible lessons from a systematic review of SARS-CoV therapy. Int J Infect Dis 2013; 17 (10) e792-e798
    CrossrefPubMedGoogle Scholar
  • 43 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
    PubMedGoogle Scholar
  • 44 Reusken CB, Haagmans BL, Müller MA. , et al. Middle East respiratory syndrome coronavirus neutralising serum antibodies in dromedary camels: a comparative serological study. Lancet Infect Dis 2013; 13 (10) 859-866
    CrossrefPubMedGoogle Scholar
  • 45 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 (50) 20662 . Available at: https://www.omicsonline.org/open-access/the-most-effective-therapeutic-regimen-for-patients-with-severe-middle-eastrespiratory-syndrome-coronavirus-merscov-infection-2332-0877-1000223.php?aid=59207
    CrossrefPubMedGoogle Scholar
  • 46 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 (50) 20659
    CrossrefPubMedGoogle Scholar
  • 47 Alexandersen S, Kobinger GP, Soule G, Wernery U. Middle East respiratory syndrome coronavirus antibody reactors among camels in Dubai, United Arab Emirates, in 2005. Transbound Emerg Dis 2014; 61 (02) 105-108
    CrossrefPubMedGoogle Scholar
  • 48 Reusken CB, Messadi L, Feyisa A. , et al. Geographic distribution of MERS coronavirus among dromedary camels, Africa. Emerg Infect Dis 2014; 20 (08) 1370-1374
    CrossrefPubMedGoogle Scholar
  • 49 Nowotny N, Kolodziejek J. Middle East respiratory syndrome coronavirus (MERS-CoV) in dromedary camels, Oman, 2013. Euro Surveill 2014; 19 (16) 20781
    PubMedGoogle Scholar
  • 50 Corman VM, Jores J, Meyer B. , et al. Antibodies against MERS coronavirus in dromedary camels, Kenya, 1992-2013. Emerg Infect Dis 2014; 20 (08) 1319-1322
    PubMedGoogle Scholar
  • 51 Hemida MG, Perera RA, Al Jassim RA. , 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) 19
    PubMedGoogle Scholar
  • 52 Alagaili AN, Briese T, Mishra N. , et al. Middle East respiratory syndrome coronavirus infection in dromedary camels in Saudi Arabia. MBio 2014; 5 (02) e00884-e14
    PubMedGoogle Scholar
  • 53 Hemida MG, Alnaeem A, Chu DK. , et al. Longitudinal study of Middle East respiratory syndrome coronavirus infection in dromedary camel herds in Saudi Arabia, 2014-2015. Emerg Microbes Infect 2017; 6 (06) e56
    PubMedGoogle Scholar
  • 54 Wernery U, Corman VM, Wong EY. , et al. Acute Middle East respiratory syndrome coronavirus infection in livestock Dromedaries, Dubai, 2014. Emerg Infect Dis 2015; 21 (06) 1019-1022
    CrossrefPubMedGoogle Scholar
  • 55 Khalafalla AI, Lu X, Al-Mubarak AI, Dalab AH, Al-Busadah KA, Erdman DD. MERS-CoV in upper respiratory tract and lungs of dromedary camels, Saudi Arabia, 2013-2014. Emerg Infect Dis 2015; 21 (07) 1153-1158
    CrossrefPubMedGoogle Scholar
  • 56 Farag EA, Reusken CB, Haagmans BL. , et al. High proportion of MERS-CoV shedding dromedaries at slaughterhouse with a potential epidemiological link to human cases, Qatar 2014. Infect Ecol Epidemiol 2015; 5: 28305
    PubMedGoogle Scholar
  • 57 Raj VS, Farag EA, Reusken CB. , et al. Isolation of MERS coronavirus from a dromedary camel, Qatar, 2014. Emerg Infect Dis 2014; 20 (08) 1339-1342
    PubMedGoogle Scholar
  • 58 Yusof MF, Eltahir YM, Serhan WS. , et al. Prevalence of Middle East respiratory syndrome coronavirus (MERS-CoV) in dromedary camels in Abu Dhabi Emirate, United Arab Emirates. Virus Genes 2015; 50 (03) 509-513
    CrossrefPubMedGoogle Scholar
  • 59 Hemida MG, Chu DK, Poon LL. , et al. MERS coronavirus in dromedary camel herd, Saudi Arabia. Emerg Infect Dis 2014; 20 (07) 1231-1234
    PubMedGoogle Scholar
  • 60 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 (03) e01146-e14
    PubMedGoogle Scholar
  • 61 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 (02) 140-145
    CrossrefPubMedGoogle Scholar
  • 62 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 (06) 1012-1015
    CrossrefPubMedGoogle Scholar
  • 63 Azhar EI, El-Kafrawy SA, Farraj SA. , et al. Evidence for camel-to-human transmission of MERS coronavirus. N Engl J Med 2014; 370 (26) 2499-2505
    CrossrefPubMedGoogle Scholar
  • 64 Al Hammadi ZM, Chu DK, Eltahir YM. , et al. Asymptomatic MERS-CoV infection in humans possibly linked to infected dromedaries imported from Oman to United Arab Emirates, May 2015. Emerg Infect Dis 2015; 21 (12) 2197-2200
    CrossrefPubMedGoogle Scholar
  • 65 Lau SKP, Wong ACP, Lau TCK, Woo PCY. Molecular evolution of MERS coronavirus: dromedaries as a recent intermediate host or long-time animal reservoir?. Int J Mol Sci 2017; 18 (10) E2138
    CrossrefPubMedGoogle Scholar
  • 66 Cotten M, Watson SJ, Zumla AI. , et al. Spread, circulation, and evolution of the Middle East respiratory syndrome coronavirus. MBio 2014; 5 (01) e01062-e13
    PubMedGoogle Scholar
  • 67 Cotten M, Watson SJ, Kellam P. , 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
    CrossrefPubMedGoogle Scholar
  • 68 Shalhoub S, Farahat F, Al-Jiffri A. , et al. IFN-α2a or IFN-β1a in combination with ribavirin to treat Middle East respiratory syndrome coronavirus pneumonia: a retrospective study. J Antimicrob Chemother 2015; 70 (07) 2129-2132
    CrossrefPubMedGoogle Scholar
  • 69 Assiri A, McGeer A, Perl TM. , et al; KSA MERS-CoV Investigation Team. Hospital outbreak of Middle East respiratory syndrome coronavirus. N Engl J Med 2013; 369 (05) 407-416
    CrossrefPubMedGoogle Scholar
  • 70 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
    CrossrefPubMedGoogle Scholar
  • 71 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. Lancet Infect Dis 2013; 13 (09) 752-761
    CrossrefPubMedGoogle Scholar
  • 72 Al-Tawfiq JA, Hinedi K, Ghandour J. , et al. Middle East respiratory syndrome coronavirus: a case-control study of hospitalized patients. Clin Infect Dis 2014; 59 (02) 160-165
    CrossrefPubMedGoogle Scholar
  • 73 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 (06) 389-397
    PubMedGoogle Scholar
  • 74 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
    CrossrefPubMedGoogle Scholar
  • 75 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 2016; 31 (05) 344-348
    CrossrefPubMedGoogle Scholar
  • 76 Al-Tawfiq JA, Alfaraj SH, Altuwaijri TA, Memish ZA. A cohort-study of patients suspected for MERS-CoV in a referral hospital in Saudi Arabia. J Infect 2017; 75 (04) 378-379
    CrossrefPubMedGoogle Scholar
  • 77 The WHO Mers-Cov Research Group. State of Knowledge and Data Gaps of Middle East Respiratory Syndrome Coronavirus (MERS-CoV) in Humans. PLoS Curr 2013; 5: pii : ecurrents.outbreaks.0bf719e352e7478f8ad85fa30
    PubMedGoogle Scholar
  • 78 Nam H-S, Park JW, Ki M, Yeon M-Y, Kim J, Kim SW. High fatality rates and associated factors in two hospital outbreaks of MERS in Daejeon, the Republic of Korea. Int J Infect Dis 2017; 58: 37-42
    CrossrefPubMedGoogle Scholar
  • 79 Kim KH, Tandi TE, Choi JW, Moon JM, Kim MS. Middle East respiratory syndrome coronavirus (MERS-CoV) outbreak in South Korea, 2015: epidemiology, characteristics and public health implications. J Hosp Infect 2017; 95 (02) 207-213
    CrossrefPubMedGoogle Scholar
  • 80 Choi WS, Kang C-I, Kim Y. , et al; Korean Society of Infectious Diseases. Clinical presentation and outcomes of Middle East respiratory syndrome in the Republic of Korea. Infect Chemother 2016; 48 (02) 118-126
    CrossrefPubMedGoogle Scholar
  • 81 Al-Tawfiq JA, Memish ZA. Drivers of MERS-CoV transmission: what do we know?. Expert Rev Respir Med 2016; 10 (03) 331-338
    CrossrefPubMedGoogle Scholar
  • 82 Al-Tawfiq JA, Memish ZA. Middle East respiratory syndrome coronavirus: epidemiology and disease control measures. Infect Drug Resist 2014; 7: 281-287
    PubMedGoogle Scholar
  • 83 Penttinen PM, Kaasik-Aaslav K, Friaux A. , et al. Taking stock of the first 133 MERS coronavirus cases globally–is the epidemic changing?. Euro Surveill 2013; 18 (39) 18
    CrossrefPubMedGoogle Scholar
  • 84 Mohd HA, Memish ZA, Alfaraj SH. , et al. Predictors of MERS-CoV infection: a large case control study of patients presenting with ILI at a MERS-CoV referral hospital in Saudi Arabia. Travel Med Infect Dis 2016; 14 (05) 464-470
    CrossrefPubMedGoogle Scholar
  • 85 Garbati MA, Fagbo SF, Fang VJ. , et al. A comparative study of clinical presentation and risk factors for adverse outcome in patients hospitalised with acute respiratory disease due to MERS coronavirus or other causes. PLoS One 2016; 11 (11) e0165978
    CrossrefPubMedGoogle Scholar
  • 86 Command and Control Center Ministry of Health Kingdom of Saudi Arabia Scientific Advisory Board. Infection Prevention and Control Guidelines for the Middle East Respiratory Syndrome Coronavirus (MERS-CoV) Infection, 4th Edition. 2017 . Available at: http://www.moh.gov.sa/endepts/Infection/Documents/Guidelines-for-MERS-CoV.PDF . Accessed May 12, 2017
    PubMedGoogle Scholar
  • 87 Saeed AA, Abedi GR, Alzahrani AG. , et al. Surveillance and testing for Middle East respiratory syndrome coronavirus, Saudi Arabia, April 2015-February 2016. Emerg Infect Dis 2017; 23 (04) 682-685
    CrossrefPubMedGoogle Scholar
  • 88 Alfaraj SH, Al-Tawfiq JA, Gautret P, Alenazi MG, Asiri AY, Memish ZA. Evaluation of visual triage for screening of Middle East respiratory syndrome coronavirus patients. New Microbes New Infect 2018; 26: 49-52
    CrossrefPubMedGoogle Scholar
  • 89 Ahmed AE. The predictors of 3- and 30-day mortality in 660 MERS-CoV patients. BMC Infect Dis 2017; 17 (01) 615
    CrossrefPubMedGoogle Scholar
  • 90 Arabi YM, Mandourah Y, Al-Hameed F. , et al; Saudi Critical Care Trial Group. Corticosteroid therapy for critically ill patients with Middle East respiratory syndrome. Am J Respir Crit Care Med 2018; 197 (06) 757-767
    CrossrefPubMedGoogle Scholar
  • 91 Alfaraj SH, Al-Tawfiq JA, Assiri AY, Alzahrani NA, Alanazi AA, Memish ZA. Clinical predictors of mortality of Middle East respiratory syndrome coronavirus (MERS-CoV) infection: a cohort study. Travel Med Infect Dis 2019; 29: 48-50
    CrossrefPubMedGoogle Scholar
  • 92 Cha R-H, Joh J-S, Jeong I. , et al; Critical Care Team of National Medical Center. Renal complications and their prognosis in Korean patients with Middle East respiratory syndrome-coronavirus from the Central MERS-CoV Designated Hospital. J Korean Med Sci 2015; 30 (12) 1807-1814
    CrossrefPubMedGoogle Scholar
  • 93 Arabi YM, Al-Omari A, Mandourah Y. , et al; Saudi Critical Care Trial Group. Critically ill patients with the Middle East respiratory syndrome: a multicenter retrospective cohort study. Crit Care Med 2017; 45 (10) 1683-1695
    CrossrefPubMedGoogle Scholar
  • 94 Alshahrani MS, Sindi A, Alshamsi F. , et al. Extracorporeal membrane oxygenation for severe Middle East respiratory syndrome coronavirus. Ann Intensive Care 2018; 8 (01) 3
    CrossrefPubMedGoogle Scholar
  • 95 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
    CrossrefPubMedGoogle Scholar
  • 96 Al-Tawfiq JA, Hinedi K. The calm before the storm: clinical observations of Middle East respiratory syndrome (MERS) patients. J Chemother 2018; 30 (03) 179-182
    CrossrefPubMedGoogle Scholar
  • 97 Alfaraj SH, Al-Tawfiq JA, Memish ZA. Middle East respiratory syndrome coronavirus intermittent positive cases: implications for infection control. Am J Infect Control 2019; 47 (03) 290-293
    CrossrefPubMedGoogle Scholar
  • 98 Corman VM, Müller MA, Costabel U. , et al. Assays for laboratory confirmation of novel human coronavirus (hCoV-EMC) infections. Euro Surveill 2012; 17 (49) 49
    PubMedGoogle Scholar
  • 99 World Health Organization (WHO). Middle East respiratory syndrome coronavirus: case definition for reporting to WHO. WHO; 2017
    Google Scholar
  • 100 Buchholz U, Müller 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 (08) 18
    CrossrefPubMedGoogle Scholar
  • 101 Drosten C, Meyer B, Müller MA. , et al. Transmission of MERS-coronavirus in household contacts. N Engl J Med 2014; 371 (09) 828-835
    CrossrefPubMedGoogle Scholar
  • 102 Drosten C, Seilmaier M, Corman VM. , et al. Clinical features and virological analysis of a case of Middle East respiratory syndrome coronavirus infection. Lancet Infect Dis 2013; 13 (09) 745-751
    CrossrefPubMedGoogle Scholar
  • 103 Omrani AS, Matin MA, Haddad Q, Al-Nakhli D, Memish ZA, Albarrak AM. 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 (09) e668-e672
    CrossrefPubMedGoogle Scholar
  • 104 Rahman A, Sarkar A. Risk factors for fatal Middle East respiratory syndrome coronavirus infections in Saudi Arabia: analysis of the WHO line list, 2013-2018. Am J Public Health 2019; 109 (09) 1288-1293
    CrossrefPubMedGoogle Scholar
  • 105 Hakawi A, Rose EB, Biggs HM. , et al. Middle East respiratory syndrome coronavirus, Saudi Arabia, 2017-2018. Emerg Infect Dis 2019; 25 (11) 2149-2151
    CrossrefPubMedGoogle Scholar
  • 106 Van Kerkhove MD, Alaswad S, Assiri A. , et al. Transmissibility of MERS-CoV infection in closed setting, Riyadh, Saudi Arabia, 2015. Emerg Infect Dis 2019; 25 (10) 1802-1809
    CrossrefPubMedGoogle Scholar
  • 107 Drosten C, Muth D, Corman VM. , et al. An observational, laboratory-based study of outbreaks of Middle East respiratory syndrome coronavirus in Jeddah and Riyadh, kingdom of Saudi Arabia, 2014. Clin Infect Dis 2015; 60 (03) 369-377
    CrossrefPubMedGoogle Scholar
  • 108 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 (04) 311-314
    CrossrefPubMedGoogle Scholar
  • 109 El Bushra HE, Abdalla MN, Al Arbash H. , et al. An outbreak of Middle East respiratory syndrome (MERS) due to coronavirus in Al-Ahssa Region, Saudi Arabia, 2015. East Mediterr Health J 2016; 22 (07) 468-475
    PubMedGoogle Scholar
  • 110 Balkhy HH, Alenazi TH, Alshamrani MM. , et al. Notes from the field: nosocomial outbreak of Middle East respiratory syndrome in a large tertiary care hospital–Riyadh, Saudi Arabia, 2015. MMWR Morb Mortal Wkly Rep 2016; 65 (06) 163-164
    CrossrefPubMedGoogle Scholar
  • 111 Balkhy HH, Alenazi TH, Alshamrani MM. , et al. Description of a hospital outbreak of Middle East respiratory syndrome in a large tertiary care hospital in Saudi Arabia. Infect Control Hosp Epidemiol 2016; 37 (10) 1147-1155
    CrossrefPubMedGoogle Scholar
  • 112 Assiri AM, Biggs HM, Abedi GR. , et al. Increase in Middle East respiratory syndrome-coronavirus cases in Saudi Arabia linked to hospital outbreak with continued circulation of recombinant virus, July 1-August 31, 2015. Open Forum Infect Dis 2016; 3: ofw165
    CrossrefPubMedGoogle Scholar
  • 113 Nazer RI. Outbreak of Middle East respiratory syndrome-coronavirus causes high fatality after cardiac operations. Ann Thorac Surg 2017; 104 (02) e127-e129
    CrossrefPubMedGoogle Scholar
  • 114 Assiri A, Abedi GR, Bin Saeed AA. , et al. Multifacility outbreak of Middle East respiratory syndrome in Taif, Saudi Arabia. Emerg Infect Dis 2016; 22 (01) 32-40
    CrossrefPubMedGoogle Scholar
  • 115 Hunter JC, Nguyen D, Aden B. , et al. Transmission of Middle East respiratory syndrome coronavirus infections in healthcare settings, Abu Dhabi. Emerg Infect Dis 2016; 22 (04) 647-656
    CrossrefPubMedGoogle Scholar
  • 116 Cauchemez S, Van Kerkhove MD, Riley S, Donnelly CA, Fraser C, Ferguson NM. Transmission scenarios for Middle East respiratory syndrome coronavirus (MERS-CoV) and how to tell them apart. Euro Surveill 2013; 18 (24) 20503
    PubMedGoogle Scholar
  • 117 Cauchemez S, Fraser C, Van Kerkhove MD. , et al. Middle East respiratory syndrome coronavirus: quantification of the extent of the epidemic, surveillance biases, and transmissibility. Lancet Infect Dis 2014; 14 (01) 50-56
    CrossrefPubMedGoogle Scholar
  • 118 Chowell G, Abdirizak F, Lee S. , et al. Transmission characteristics of MERS and SARS in the healthcare setting: a comparative study. BMC Med 2015; 13: 210
    CrossrefPubMedGoogle Scholar
  • 119 Al-Abdallat MM, Payne DC, Alqasrawi S. , et al; Jordan MERS-CoV Investigation Team. Hospital-associated outbreak of Middle East respiratory syndrome coronavirus: a serologic, epidemiologic, and clinical description. Clin Infect Dis 2014; 59 (09) 1225-1233
    CrossrefPubMedGoogle Scholar
  • 120 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. 01) S12-S18
    CrossrefPubMedGoogle Scholar
  • 121 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 (09) 846-854
    CrossrefPubMedGoogle Scholar
  • 122 Alraddadi B, Bawareth N, Omar H. , et al. Patient characteristics infected with Middle East respiratory syndrome coronavirus infection in a tertiary hospital. Ann Thorac Med 2016; 11 (02) 128-131
    CrossrefPubMedGoogle Scholar
  • 123 Almekhlafi GA, Albarrak MM, Mandourah Y. , et al. Presentation and outcome of Middle East respiratory syndrome in Saudi intensive care unit patients. Crit Care 2016; 20 (01) 123
    CrossrefPubMedGoogle Scholar
  • 124 Kim YS, Aigerim A, Park U. , et al. Sequential emergence and wide spread of neutralization escape Middle East respiratory syndrome coronavirus mutants, South Korea, 2015. Emerg Infect Dis 2019; 25 (06) 1161-1168
    CrossrefPubMedGoogle Scholar
  • 125 Al-Tawfiq JA, Auwaerter PG. Healthcare-associated Infections: the hallmark of the Middle East respiratory syndrome coronavirus (MERS-CoV) with review of the literature. J Hosp Infect 2019; 101 (01) 20-29
    CrossrefPubMedGoogle Scholar
  • 126 Alfaraj SH, Al-Tawfiq JA, Altuwaijri TA, Alanazi M, Alzahrani N, Memish ZA. Middle East respiratory syndrome coronavirus transmission among health care workers: implication for infection control. Am J Infect Control 2018; 46 (02) 165-168
    CrossrefPubMedGoogle Scholar
  • 127 Kim C-J, Choi WS, Jung Y. , et al. Surveillance of the Middle East respiratory syndrome (MERS) coronavirus (CoV) infection in healthcare workers after contact with confirmed MERS patients: incidence and risk factors of MERS-CoV seropositivity. Clin Microbiol Infect 2016; 22 (10) 880-886
    CrossrefPubMedGoogle Scholar
  • 128 Wiboonchutikul S, Manosuthi W, Sangsajja C. Zero transmission of Middle East respiratory syndrome: lessons learned from Thailand. Clin Infect Dis 2017; 64 (Suppl. 02) S167-S170
    CrossrefPubMedGoogle Scholar
  • 129 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
    CrossrefPubMedGoogle Scholar
  • 130 Kim SG. Healthcare workers infected with Middle East respiratory syndrome coronavirus and infection control. J Korean Med Assoc 2015; 58: 647-654
    CrossrefPubMedGoogle Scholar
  • 131 Alraddadi BM, Al-Salmi HS, Jacobs-Slifka K. , et al. Risk factors for Middle East respiratory syndrome coronavirus infection among healthcare personnel. Emerg Infect Dis 2016; 22 (11) 1915-1920
    CrossrefPubMedGoogle Scholar
  • 132 Noorwali AA, Turkistani AM, Asiri SI. , et al. Descriptive epidemiology and characteristics of confirmed cases of Middle East respiratory syndrome coronavirus infection in the Makkah Region of Saudi Arabia, March to June 2014. Ann Saudi Med 2015; 35 (03) 203-209
    CrossrefPubMedGoogle Scholar
  • 133 Zumla A, Azhar EI, Arabi Y. , et al. Host-directed therapies for improving poor treatment outcomes associated with the Middle East respiratory syndrome coronavirus infections. Int J Infect Dis 2015; 40: 71-74
    CrossrefPubMedGoogle Scholar
  • 134 Gossner C, Danielson N, Gervelmeyer A. , et al. Human-dromedary camel interactions and the risk of acquiring zoonotic Middle East respiratory syndrome coronavirus infection. Zoonoses Public Health 2016; 63 (01) 1-9
    CrossrefPubMedGoogle Scholar
  • 135 Kasem S, Qasim I, Al-Doweriej A. , et al. The prevalence of Middle East respiratory syndrome coronavirus (MERS-CoV) infection in livestock and temporal relation to locations and seasons. J Infect Public Health 2018; 11 (06) 884-888
    CrossrefPubMedGoogle Scholar
  • 136 Aly M, Elrobh M, Alzayer M, Aljuhani S, Balkhy H. Occurrence of the Middle East respiratory syndrome coronavirus (MERS-CoV) across the Gulf Corporation Council countries: four years update. PLoS One 2017; 12 (10) e0183850
    CrossrefPubMedGoogle Scholar
  • 137 Al-Tawfiq JA, Memish ZA. Lack of seasonal variation of Middle East respiratory syndrome coronavirus (MERS-CoV). Travel Med Infect Dis 2019; 27: 125-126
    CrossrefPubMedGoogle Scholar
  • 138 Hart BJ, Dyall J, Postnikova E. , et al. Interferon-β and mycophenolic acid are potent inhibitors of Middle East respiratory syndrome coronavirus in cell-based assays. J Gen Virol 2014; 95 (Pt 3): 571-577
    CrossrefPubMedGoogle Scholar
  • 139 de Wilde AH, Raj VS, Oudshoorn D. , et al. MERS-coronavirus replication induces severe in vitro cytopathology and is strongly inhibited by cyclosporin A or interferon-α treatment. J Gen Virol 2013; 94 (Pt 8): 1749-1760
    CrossrefPubMedGoogle Scholar
  • 140 Falzarano D, de Wit E, Martellaro C, Callison J, Munster VJ, Feldmann H. Inhibition of novel β coronavirus replication by a combination of interferon-α2b and ribavirin. Sci Rep 2013; 3: 1686
    CrossrefPubMedGoogle Scholar
  • 141 Al-Tawfiq JA, Momattin H, Dib J, Memish ZA. Ribavirin and interferon therapy in patients infected with the Middle East respiratory syndrome coronavirus: an observational study. Int J Infect Dis 2014; 20: 42-46
    CrossrefPubMedGoogle Scholar
  • 142 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
    CrossrefPubMedGoogle Scholar
  • 143 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 (06) 528-532
    CrossrefPubMedGoogle Scholar
  • 144 Khalid M, Al Rabiah F, Khan B, Al Mobeireek A, Butt TS, Al Mutairy E. Ribavirin and interferon-α2b as primary and preventive treatment for Middle East respiratory syndrome coronavirus: a preliminary report of two cases. Antivir Ther 2015; 20 (01) 87-91
    PubMedGoogle Scholar
  • 145 Tawalah H, Al-Qabandi S, Sadiq M, Chehadeh C, Al-Hujailan G, Al-Qaseer M. The most effective therapeutic regimen for patients with severe Middle East respiratory syndrome coronavirus (MERS-CoV) infection. J Infect Dis Ther 2015; 03: 1-5
    CrossrefPubMedGoogle Scholar
  • 146 Al Ghamdi M, Alghamdi KM, Ghandoora Y. , et al. Treatment outcomes for patients with Middle Eastern Respiratory Syndrome Coronavirus (MERS CoV) infection at a coronavirus referral center in the Kingdom of Saudi Arabia. BMC Infect Dis 2016; 16: 174
    CrossrefPubMedGoogle Scholar
  • 147 Arabi YM, Alothman A, Balkhy HH. , et al; And the MIRACLE trial group. Treatment of Middle East respiratory syndrome with a combination of lopinavir-ritonavir and interferon-β1b (MIRACLE trial): study protocol for a randomized controlled trial. Trials 2018; 19 (01) 81
    CrossrefPubMedGoogle Scholar
  • 148 Aburizaiza AS, Mattes FM, Azhar EI. , et al. 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 2014; 209 (02) 243-246
    CrossrefPubMedGoogle Scholar
  • 149 Gierer S, Hofmann-Winkler H, Albuali WH. , et al. Lack of MERS coronavirus neutralizing antibodies in humans, eastern province, Saudi Arabia. Emerg Infect Dis 2013; 19 (12) 2034-2036
    CrossrefPubMedGoogle Scholar
  • 150 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 (05) 559-564
    CrossrefPubMedGoogle Scholar
  • 151 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
    CrossrefPubMedGoogle Scholar
  • 152 Leclercq I, Batéjat C, Burguière AM, Manuguerra JC. Heat inactivation of the Middle East respiratory syndrome coronavirus. Influenza Other Respir Viruses 2014; 8 (05) 585-586
    CrossrefPubMedGoogle Scholar
  • 153 WHO. WHO|Infection prevention and control of epidemic-and pandemic prone acute respiratory infections in health care. WHO; 2015
    PubMedGoogle Scholar
  • 154 World Health Organization (WHO). Infection prevention and control of epidemic-and pandemic prone acute respiratory infections in health care. WHO; 2015
    PubMedGoogle Scholar
  • 155 CDC. Interim Infection Prevention and Control Recommendations for Hospitalized Patients with Middle East Respiratory Syndrome Coronavirus (MERS-CoV). 2015 . Available at: https://www.cdc.gov/coronavirus/mers/infection-prevention-control.html . Accessed March 9, 2017
    PubMedGoogle Scholar
  • 156 Kandeil A, Gomaa M, Nageh A. , et al. Middle East respiratory syndrome coronavirus (MERS-CoV) in dromedary camels in Africa and Middle East. Viruses 2019; 11 (08) 717
    CrossrefPubMedGoogle Scholar
  • 157 Ali MA, Shehata MM, Gomaa MR. , et al. Systematic, active surveillance for Middle East respiratory syndrome coronavirus in camels in Egypt. Emerg Microbes Infect 2017; 6 (01) e1
    PubMedGoogle Scholar
  • 158 Kasem S, Qasim I, Al-Hufofi A. , et al. Cross-sectional study of MERS-CoV-specific RNA and antibodies in animals that have had contact with MERS patients in Saudi Arabia. J Infect Public Health 2018; 11 (03) 331-338
    CrossrefPubMedGoogle Scholar
  • 159 Chu DK, Poon LL, Gomaa MM. , et al. MERS coronaviruses in dromedary camels, Egypt. Emerg Infect Dis 2014; 20 (06) 1049-1053
    CrossrefPubMedGoogle Scholar
  • 160 Farag EA, Haagmans BL, Al-Romaihi H. , et al. Failure to detect MERS-CoV RNA in urine of naturally infected dromedary camels. Zoonoses Public Health 2019; 66 (05) 437-438
    CrossrefPubMedGoogle Scholar
  • 161 Hui DS, Memish ZA, Zumla A. Severe acute respiratory syndrome versus the Middle East respiratory syndrome. Curr Opin Pulm Med 2014; 20: 233-241
    PubMedGoogle Scholar