Dear Editor,
In a recent paper published in Travel Medicine and Infectious Disease, Al-Tawfiq and colleagues state with reason that despite a great concern regarding the potential for the Hajj to cause a global epidemic of Middle East Syndrome Coronavirus (MERS-CoV); only a limited number of travel-associated cases were reported with no major event related to the Hajj [1]. Screening for MERS-CoV carriage was conducted among cohorts of Hajj pilgrims in 2012 and 2013 and resulted negative [2], [3], [4]. Up to 1 November 2014, 21 cases of travel-associated MERS have been reported from various sources including ProMED (http://www.promedmail.org/), WHO (http://www.who.int/csr/outbreaknetwork/en/), ECDC (http://www.ecdc.europa.eu/en/Pages/home.aspx) and USCDC (http://www.cdc.gov/) updates, some of which were also reported in the medical literature as summarized recently by Pavli and colleagues [5].
In Table 1 , we are describing the MERS cases identified out of the Middle Eastern countries among individuals who traveled to and/or from the Middle Eastern countries. All cases but two were confirmed by polymerase chain reaction on at least two specific genomic targets. The majority of cases were in Europe (10 cases), North Africa (5 cases) and Asia (4). Two cases were imported to the US. Likely place of exposure was in the Kingdom of Saudi Arabia (KSA) in the majority of cases. Three patients were Middle East nationals transferred to European hospitals for medical care. Seven cases were among expatriates living in the Middle East and traveling back to their country of origin, including one patient living in Qatar who participated to the Umrah in KSA (a shorter pilgrimage to Mecca that can be undergone at any time). Ten cases were among short-term travelers with a mean time of stay in the Middle East of 18 days (range 3 h–40 days). Among short-travelers, 7 participated to the Umrah, one traveled for holidays, one was in transit in Abu Dhabi airport and the information is missing in one case. Nine patients died, nine recovered, one was asymptomatic and the information missing in two cases. Possible source of infection was identified in some patients including exposure to camels or their products (four cases) or bats (one case), exposure to MERS patients (six cases of which three were health care workers) and visit to Saudi hospitals (two cases).
Table 1.
Characteristics of travel-associated cases of Middle East coronavirus syndrome (2012–2014)a.
| Country of diagnostic | Country of current residence | Year | Age (years)/gender | Likely place of exposure | Travel duration (days) | Reason for travel | Outcome | Possible source of infection | PCR target genes | Referencesa |
|---|---|---|---|---|---|---|---|---|---|---|
| UK | Qatar | 2012 | 49/M | Qatar and KSA | NA | Medical transfert | Died | Visited a camel farm | UpE and ORF1 | [1,2] |
| Germany (Essen) | Qatar | 2012 | 45/M | Qatar | NA | Medical transfert | Recovered | Contacts with camels | UpE and ORF1 | [3,4] |
| Germany (Munich) | UAE | 2013 | 73/M | UAE | NA | Medical transfert | Died | Contacts with camels | UpE and ORF1 | [5,6] |
| France | France | 2013 | 64/M | UAE | 8 | ND | Died | ND | UpE and ORF1 | [7,8] |
| Italy | Italy | 2013 | 45/M | Jordan | 40 | Holiday | Recovered | ND | UpE | [9] |
| Tunisia | Tunisia | 2013 | 66/M | Qatar and KSA | 31 in Qatar and 8 in KSA | Visit family + Umrah | Died | None identified | ORF1 and N2 | [10] |
| Tunisia | Qatar (expatriate) | 2013 | 30/F | Qatar and KSA | NA | Umrah + attended funerals in Tunisia | Recovered | Exposure to MERS patient | UpE and ORF1 | [10] |
| UK | UK | 2013 | 55/M | Pakistan and KSA | 35 in Pakistan, 8 in KSA | Visit family + Umrah | Died | None identified | UpE and two other genes | [11] |
| Netherlands | Netherlands | 2014 | 70/M | KSA | 16 | Umrah | Recovered | Hospitalization in Saudi Arabia | UpE, N and ORF1 | [12,13] |
| Netherlands | Netherlands | 2014 | 73/F | KSA | 16 | Umrah | Recovered | Exposure to MERS patient | UpE, N and ORF1 | [12,13] |
| Algeria | Algeria | 2014 | 66/M | KSA | 14 | Umrah | Recovered | ND | UpE, N and ORF1 | [14-16] |
| Algeria | Algeria | 2014 | 59/M | KSA | 24 | Umrah | Died | ND | UpE, N and ORF1 | [14-16] |
| Greece | KSA (expatriate) | 2014 | 69/M | KSA | NA | Visit to citizenship country | Died | Visited hospitals in Saudi Arabia and had indirect contacts with bats | UpE, N and ORF1 | [17,18] |
| US (Indiana) | KSA (expatriate) | 2014 | 65/M | KSA | NA | Visit to citizenship country | Recovered | Exposure to MERS patients (HCW) | ORF1 and N2 | [19,20] |
| US (Florida) | KSA (expatriate) | 2014 | 44/M | KSA | NA | Visit to citizenship country | Recovered | Exposure to MERS patients (HCW) | ORF1 and N2 | [20] |
| Malaysia | Malaysia | 2014 | 55/M | KSA | 13 | Umrah | Died | Drank raw camel milk | UpE, N and ORF1 | [21] |
| Egypt | KSA (expatriate) | 2014 | 27/M | KSA | NA | Visit to citizenship country | Recovered | Exposure to MERS patients | Confirmed according to ECDC report | [22,23] |
| Philippines | UAE (expatriate) | 2014 | ND/M | UAE | NA | Visit to citizenship country | Asymptomatic | Exposure to MERS patients (HCW) | Confirmed according to ECDC report | [24] |
| Bangladesh | US | 2014 | 53/M | UAE | 3 h transit in Abu Dhabi airport | Visit to citizenship country | ND | ND | ND | [16] |
| Turkey | KSA (expatriate) | 2014 | ND/M | KSA | NA | Visit to citizenship country | Death | ND | ND | [25,26] |
| Austria | KSA | 2014 | 29/F | KSA | NA | ND | ND | ND | Confirmed according to ECDC report | [27,28] |
See online appendix.
From this figure, it is notable that 8 out of 21 travel-associated cases were in patients who participated to the Umrah (38%), a proportion which culminate to 70% among short-term travelers. Among the 8 patients participating to the Umrah, two were exposed to MERS patients, one was hospitalized in Saudi Arabia prior contracting MERS and one drank camel milk in KSA. No risk factor was identified in two patients and the information was missing in two cases.
These 8 Umrah-associated MERS cases over an estimated 20 million pilgrims who visited Mecca from 2012 through 2014 are not significant in terms of public health. The high prevalence of participation to Umrah among the few travel-associated MERS cases in short-term travelers likely reflects the fact that tourism in the region is significantly dependent on religious tourism. According to the Saudi Tourism and Antiquities Committee (SCTA) data, of the 17 million international tourists who visited Saudi Arabia in 2013, 6.9 million (40.6%) did so for religious reasons. From a clinical perspective, physicians should have a high degree of suspicion for MERS in patients with severe respiratory symptoms following pilgrimage to Mecca; however, surveillance data in England and France showed that a diagnostic of influenza was most likely in such travelers [3], [6], [7].
Conflict of interest
None.
Appendix 1. References of Middle East coronavirus cases among travelers outside the Middle East.
[1] Bermingham A, Chand MA, Brown CS, Aarons E, Tong C, Langrish C, et al. Severe respiratory illness caused by a novel coronavirus, in a patient transferred to the United Kingdom from the Middle East, September 2012. Euro Surveill 2012 Oct 4;17(40):20290.
[2] Pebody RG, Chand MA, Thomas HL, Green HK, Boddington NL, Carvalho C, et al. The United Kingdom public health response to an imported laboratory confirmed case of a novel coronavirus in September 2012. Euro Surveill 2012 Oct 4;17(40):20292.
[3] Guberina H, Witzke O, Timm J, Dittmer U, Müller MA, Drosten C, et al. A patient with severe respiratory failure caused by novel human coronavirus. Infection 2014 Feb;42(1):203-6.
[4] Buchholz U, Müller MA, Nitsche A, Sanewski A, Wevering N, Bauer-Balci T, et al. Contact investigation of a case of human novel coronavirus infection treated in a German hospital, October–November 2012. Euro Surveill 2013 Feb 21;18(8). pii: 20406.
[5] Drosten C, Seilmaier M, Corman VM, Hartmann W, Scheible G, Sack S, et al. Clinical features and virological analysis of a case of Middle East respiratory syndrome coronavirus infection. Lancet Infect Dis 2013 Sep;13(9):745-51.
[6] Reuss A, Litterst A, Drosten C, Seilmaier M, Böhmer M, Graf P, et al. Contact investigation for imported case of Middle East respiratory syndrome, Germany. Emerg Infect Dis 2014 Apr;20(4):620-5.
[7] Guery B, Poissy J, el Mansouf L, Séjourné C, Ettahar N, Lemaire X, et al. Clinical features and viral diagnosis of two cases of infection with Middle East Respiratory Syndrome coronavirus: a report of nosocomial transmission. Lancet 2013 Jun 29;381(9885):2265-72.
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[9] Puzelli S1, Azzi A, Santini MG, Di Martino A, Facchini M, Castrucci MR, et al. Investigation of an imported case of Middle East Respiratory Syndrome Coronavirus (MERS-CoV) infection in Florence, Italy, May to June 2013. Euro Surveill 2013 Aug 22;18(34). pii: 20564.
[10] Abroug F, Slim A, Ouanes-Besbes L, Hadj Kacem MA, Dachraoui F, Ouanes I, et al. Family cluster of Middle East respiratory syndrome coronavirus infections, Tunisia, 2013. Emerg Infect Dis 2014 Sep;20(9):1527-30.
[11] Health Protection Agency (HPA) UK Novel Coronavirus Investigation team. Evidence of person-to-person transmission within a family cluster of novel coronavirus infections, United Kingdom, February 2013. Euro Surveill 2013 Mar 14;18(11):20427.
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[13] Fanoy EB, van der Sande MA, Kraaij-Dirkzwager M, Dirksen K, Jonges M, van der Hoek W, et al. Travel-related 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 Oct 17;11:16.
[14] ProMED-mail. MERS-CoV - Eastern Mediterranean (73): Saudi Arabia, Algeria, Jordan, WHO, RFI. Archive Number: 20140601.2512766. Published Date: 2014-06-01 19:27:25.
[15] ProMED-mail. MERS-CoV - Eastern Mediterranean (80): S Arabia, Iran, Algeria, Tunisia Archive Number: 20140612.2534478. Published Date: 2014-06-12 10:00:39.
[16] ProMED-mail. MERS-CoV (01): Bangladesh, KSA, Algeria, UAE, Iran, WHO, RFI Archive Number: 20140616.2541707. Published Date: 2014-06-16 15:12:09.
[17] Tsiodras S, Baka A, Mentis A, Iliopoulos D, Dedoukou X, Papamavrou G, et al. A case of imported Middle East Respiratory Syndrome coronavirus infection and public health response, Greece, April 2014. Euro Surveill 2014 Apr 24;19(16):20782. Erratum in: Euro Surveill. 2014;19(17):pii/20786.
[18] Spanakis N, Tsiodras S, Haagmans BL, Raj VS, Pontikis K, Koutsoukou A, 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 Sep 18. pii: S0924-8579(14)00278-7.
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