Exploring the risk of Middle East Respiratory Syndrome- coronavirus among expatriate healthcare workers. A comparative epidemiological study of Saudi Arabian and South Korean healthcare workers

Background In comparison to South Korea, which was able to contain the outbreak of Middle East respiratory syndrome corona virus (MERS-CoV) in 2015, new cases are still emerging in the Kingdom of Saudi Arabia. The Saudi Arabian healthcare sector, which is dependent on the expatriate workforce to cater to its growing local healthcare demands, has been reporting multiple healthcare-associated MERS-CoV outbreaks since 2012. In this paper, we compare the epidemiology of MERS-CoV among healthcare workers (HCWs) in Saudi Arabia and South Korea and to ascertain the risks of MERS-CoV among expatriate HCWs. Methods Data were collected from publicly available resources such as World Health Organization and health department websites. A line list of all reported cases of MERS-CoV among HCWs in Saudi Arabia and South Korea was prepared and analysed. Results Among the total infected HCWs in Saudi Arabia, 84.6% (n=192/227) were expatriates. The mean age of infected HCWs in both settings was similar (Saudi Arabia 38 years, South Korea 39 years). Female HCWs were more likely to be infected, while male HCWs were more likely to die. In Saudi Arabia, 36.5% (n= 68/186) of HCWs with MERS-CoV were asymptomatic, compared to 7% (n=2/28) HCWs in South Korea. Most of the expatriate HCWs in Saudi Arabia were asymptomatic (78%, n=53/68) to MERS-CoV. Unlike South Korea, in Saudi Arabia, a diversity of HCWs other than doctors, and nurses were also infected with MERS-CoV. Conclusions A high proportion of expatriate HCWs were infected with MERS-CoV in Saudi Arabia which highlights the need for adequate training and education in this group about emerging infectious diseases and the appropriate strategies to prevent acquisition. Also, we did not find any policy statements restricting the contact of HCWs, vulnerable to MERS-CoV like pregnant HCW, HCWs over the age 60, HCWs with underlying comorbidity etc, from getting in proximity with a suspected or potential MERS-CoV infected patient. Policy development in this regard should be a priority, to contain healthcare-associated transmission of emerging and remerging infectious diseases like MERS-CoV. Further studies should be conducted to determine social, cultural and other factors contributing to high infection rate among expatriate HCWs.


INTRODUCTION
Healthcare-associated transmission of Middle East respiratory syndrome coronavirus (MERS-CoV) has been reported in several countries since 2012, including Kingdom of Saudi Arabia, Jordan, the United Arab Emirates, France, the United Kingdom (UK), and South Korea with varying caseloads per outbreak (2-180 per outbreak) [1].
Compared to South Korea, which had a one large outbreak of healthcare-associated MERS-CoV in 2015, Saudi Arabia, has had continuous but intermittent healthcareassociated outbreaks of MERS-CoV across the country since 2012 [2][3][4][5][6]. According to the WHO, out of total MERS-CoV infected cases reported between 2012-2018 from Saudi Arabia, 19.2% were healthcare workers (HCW) [7]. Globally, around 20% of the cases reported between the year 2012-2018 have been of HCWs [8], whilst a second study reported that around 10% of critically ill patients with MERS-CoV were HCWs [9].
The spread of healthcare-associated MERS-CoV amongst HCWs is now well documented [9]. In summary, it was first observed in Jordan in April 2012, but it was until 2013, that Saudi Arabia reported the first two laboratory confirmed cases of MERS-CoV infected HCWs, following exposure to laboratory confirmed MERS-CoV patients [10,11]. This was followed by seven female HCWs being affected in subsequent months in 2013 with MERS-CoV in Saudi Arabia, four of whom were expatriate HCWs (nationality of the rest three not available) [12]. While there have been numerous reports about the burden of infection and the factors contributing to the risk, what hasn't been given attention is the burden of infection amongst expatriate staff members.
Due to increasing local healthcare demand, many high income economies are more than ever reliant on expatriate HCWs, many of whom come from low and middle income countries including Asia [13,14]. For instance, a 2015 report from the Organisation for Economic Co-operation and Development points out that UK is the most dependent of all major EU countries on foreign doctors (35.4%) and nurses (21.7%) [15]. Likewise, a 2011 census found that 52.3% HCWs in Australia were born and educated in other countries. And also, out of 15,168 additional HCWs in Australia between the 2006 and 2011 censuses, 68.9% were foreign-born, which saved the Australian government US$1.7 billion in medical education costs [16,17].
In fact, the United States (US) health care system also, relies very heavily on HCWs from other countries with one in four doctors in the US being born and educated in another country [14]. Correspondingly a high-income country like Saudi Arabia is no different, expatriate HCWs constitute about two thirds of the physicians, nurses and pharmacists employed [18].
With WHO estimating a shortage of more than 2 million doctors, nurses and midwives to meet the minimum global recommended density [19] expatriate HCWs are bound to play a big role in filling this demand and supply gap. Therefore, the aim of this study was to compare the epidemiology of MERS-CoV among HCWs in  HCWs are outlined in Table 2.

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Availability of data and materials
The database which supports this study is available upon request.

Competing interests
Dr Holly Seale is a section editor for BMC Infectious Diseases. The author(s) declare(s) that there are no other competing interest.

Funding
No financial support was provided relevant to this article.

Authors' contributions
All the authors contributed equally and all authors read and approved the final manuscript.