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      Imported cases of Middle East respiratory syndrome: An update

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          Abstract

          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] a 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.

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          Most cited references6

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          Travel implications of emerging coronaviruses: SARS and MERS-CoV

          Summary The emergence of Severe Acute Respiratory Syndrome Coronavirus (SARS-CoV) and of the Middle East Syndrome Cornavirus (MERS-CoV) caused widespread fear and concern for their potential threat to global health security. There are similarities and differences in the epidemiology and clinical features between these two diseases. The origin of SARS-COV and MERS-CoV is thought to be an animal source with subsequent transmission to humans. The identification of both the intermediate host and the exact route of transmission of MERS-CoV is crucial for the subsequent prevention of the introduction of the virus into the human population. So far MERS-CoV had resulted in a limited travel-associated human cases with no major events related to the Hajj.
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            Lack of nasal carriage of novel corona virus (HCoV-EMC) in French Hajj pilgrims returning from the Hajj 2012, despite a high rate of respiratory symptoms

            A cohort of 154 French Hajj pilgrims participating in the 2012 Hajj were systematically sampled with nasal swabs prior to returning to France, and screened for the novel HCoV-EMC coronavirus by two real-time RT-PCR assays. Despite a high rate of respiratory symptoms (83.4%), including 41.0% influenza-like illness, no case of HCoV-EMC infection was detected. Despite the fact that zoonotic transmission was suspected in the first few cases, a recent family cluster in the Kingdom of Saudi Arabia suggests that the virus might show at least limited spread from person to person, which justifies continuing epidemiological surveillance.
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              Is Open Access

              Lack of MERS Coronavirus but Prevalence of Influenza Virus in French Pilgrims after 2013 Hajj

              To the Editor: Saudi Arabia has reported the highest number of Middle East respiratory syndrome coronavirus (MERS-CoV) cases since the virus first emerged in 2012, with >127 confirmed cases and a case-fatality rate of 42%, as of November 2013 ( 1 ). Global attention has focused on the potential for spread of MERS-CoV after the Hajj pilgrimage during which Muslims from 180 countries converge in Mecca, Saudi Arabia. Such pilgrims have a high risk for respiratory tract infections because of severe overcrowding. The International Health Regulations Emergency Committee advised all countries (particularly those with returning pilgrims) to strengthen their surveillance capacities and ensure robust reporting of any identified cases ( 2 ). We report the results of a prospective cohort study conducted in Saudi Arabia in October 2013. Participants in the survey were adult Hajj pilgrims who traveled together in a group (through 1 travel agency in Marseille, France) from October 3 through October 24, 2013. Pilgrims were included in the study on a voluntary basis and were asked to sign a written consent form. All pilgrims received advice about individual prevention measures against respiratory tract infection before departing, and follow-up was conducted during the journey by a medical doctor who systematically documented travel-associated diseases. Nasal swab specimens were obtained just before the pilgrims left Saudi Arabia, frozen <48 hours after sampling, and processed ( 3 , 4 ). Each sample was tested for MERS-CoV (upE and ORF1a genes) ( 5 , 6 ) and influenza A, B ( 7 ), and A/2009/H1N1 viruses ( 8 ) by real-time reverse transcription PCR. The protocol was approved by our Institutional Review Board (July 23, 2013; reference no. 2013-A00961–44) and by the Saudi Ministry of Health ethics committee. On departure from France, the study comprised 129 pilgrims. Their mean age was 61.7 years (range 34–85 years), and the male/female ratio was 0.7:1. Sixty-eight (52.7%) pilgrims reported having a chronic disease, including hypertension (43 [33.3%]), diabetes (34 [26.4%]), chronic cardiac disease (11 [8.5%]), and chronic respiratory disease (5 [3.9%]). Forty-six (35.7%) pilgrims reported receiving influenza vaccination in 2012; none had been vaccinated in 2013 before the Hajj because the vaccine was not yet available in France. Clinical data were available for 129 persons: 117 (90.7%) had respiratory symptoms while in Saudi Arabia, including cough (112 [86.8%]) and sore throat (107 [82.9%]); 64 (49.6%) reported fever, and 61 (47.3%) had conditions that met the criteria for influenza-like illness (ILI; i.e., the association of cough, sore throat, and subjective fever) (Figure) ( 4 ). One patient was hospitalized during travel (undocumented pneumonia). Nasal swab specimens were obtained from 129 pilgrims on October 23, 2013 (week 43), 1 day before pilgrims left Saudi Arabia for France; 90 (69.8%) pilgrims were still symptomatic. All PCRs were negative for MERS-CoV. Figure Onset of respiratory symptoms by week, reported by 129 Hajj pilgrims from France during their stay in Saudi Arabia, October 2013. Eight pilgrims tested positive for influenza A(H3N2), 1 for influenza A(H1N1), and 1 for influenza B virus. No dual infections were reported. 70 (54.3%) pilgrims were seen 3–5 weeks after they returned to France, and the remaining were lost to follow-up. Fifty-five (78.6%) had experienced respiratory symptoms since their return, including cough (50 [71.4%]) and sore throat (14 [20.0%]); 12 (17.1%) reported fever, and illness in 5 (7.1%) pilgrims met the criteria for ILI. The 10 pilgrims who had positive test results for influenza virus on return had cleared their infection; only 1 additional sample was positive (for influenza A[H1N1]). Our results support data obtained from a similar cohort in 2012 that showed a lack of nasal carriage of MERS-CoV among Hajj pilgrims from France ( 3 ). However, a higher prevalence of influenza virus (7.8%) was observed in nasal swab specimens in 2013 than in 2012 when 2 (3.2%) cases of influenza B virus infection were detected and no case of influenza A virus infection was detected among 162 pilgrims returning from the Hajj ( 4 ). The estimated incidence of ILI in France during week 43 was 27 per 100,000 inhabitants, far below the epidemic threshold (126/100,000) with few sporadic cases of influenza A virus infection reported in some regions in France (www.grog.org/bullhebdo_pdf/bull_grog_43-2013.pdf). No case was reported in the Marseille area (http://websenti.u707.jussieu.fr/sentiweb). The high prevalence of respiratory symptoms in our cohort probably reflects the close surveillance performed and is consistent with 2012 results ( 3 , 4 ). In Marseille, all patients with suspected MERS-CoV infection are referred to the Institut Hospitalo-Universitaire Méditerranée Infection. As of November 8, 2013, of the 14 first returning patients hospitalized for respiratory symptoms and screened for MERS-CoV and other pathogens, including influenza, 4 were infected with influenza A(H3N2), 4 with influenza A(H1N1), and 1 with influenza B virus. All samples tested negative for MERS-CoV. Our preliminary results indicate that pilgrims from France returning from the 2013 Hajj were free of MERS-CoV but that a proportion were infected with influenza viruses and may represent a potential for early introduction of influenza in southern France. This proportion may have been underestimated because screening was performed at the end of the study period when some infections had cleared. Influenza vaccination should be a priority for pilgrims attending the Hajj ( 9 , 10 ).
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                Author and article information

                Contributors
                Journal
                Travel Med Infect Dis
                Travel Med Infect Dis
                Travel Medicine and Infectious Disease
                Elsevier Ltd.
                1477-8939
                1873-0442
                21 November 2014
                January-February 2015
                21 November 2014
                : 13
                : 1
                : 106-109
                Affiliations
                [1]Assistance Publique Hôpitaux de Marseille, CHU Nord, Pôle Infectieux, Institut Hospitalo-Universitaire Méditerranée Infection, 13015 Marseille, France
                [2]Aix Marseille Université, Unité de Recherche en Maladies Infectieuses et Tropicales Emergentes (URMITE), UM63, CNRS 7278, IRD 198, Inserm 1095, Faculté de Médecine, 27 bd Jean Moulin, 13005 Marseille, France
                Author notes
                []Corresponding author. Tel.: +33 0 4 91 96 35 35, +33 0 4 91 96 35 36; fax: +33 0 4 91 96 89 38. philippe.gautret@ 123456club-internet.fr
                Article
                S1477-8939(14)00220-8
                10.1016/j.tmaid.2014.11.006
                7128971
                25477148
                19e59e2f-ebfb-4af6-b010-9fb52bb20336
                Copyright © 2014 Elsevier Ltd. All rights reserved.

                Since January 2020 Elsevier has created a COVID-19 resource centre with free information in English and Mandarin on the novel coronavirus COVID-19. The COVID-19 resource centre is hosted on Elsevier Connect, the company's public news and information website. Elsevier hereby grants permission to make all its COVID-19-related research that is available on the COVID-19 resource centre - including this research content - immediately available in PubMed Central and other publicly funded repositories, such as the WHO COVID database with rights for unrestricted research re-use and analyses in any form or by any means with acknowledgement of the original source. These permissions are granted for free by Elsevier for as long as the COVID-19 resource centre remains active.

                History
                : 12 November 2014
                Categories
                Article

                Infectious disease & Microbiology
                middle east respiratory syndrome,travelers,umrah,hajj
                Infectious disease & Microbiology
                middle east respiratory syndrome, travelers, umrah, hajj

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