SARS, MERS and COVID-19 among healthcare workers: A narrative review.

In the recent two decades, three global viral infectious diseases, severe acute respiratory syndrome (SARS), middle east respiratory syndrome (MERS), and coronavirus disease (COVID-19), have occurred worldwide. SARS occurred in November 2002, causing 8096 infected cases, as well as 774 deaths. MERS occurred in June, 2012, causing 2519 confirmed cases, along with 866 associated deaths. COVID-19 occurred in December 2019, as of 30 April 2020, a total of 3,024,059 clinical cases have been reported, including 208,112 deaths. Healthcare workers (HCWs) need to be in close contact with these virus-infected patients and their contaminated environments at work, thus leading to be infected in some of them, even a few of them are died in line of duty. In this review, we summarized the infection status of HCWs during the outbreak of SARS, MERS and COVID-19, with in-depth discussion, hoping to provoke sufficient attention to the HCWs infection status by more people.

Introduction

Viral infectious diseases have always been a threat to human survival. In the recent two decades, three global viral infectious diseases, severe acute respiratory syndrome (SARS), middle east respiratory syndrome (MERS), and the current coronavirus disease (COVID-19) [1], [2], [3], have occurred worldwide, and all the pathogens are the types of coronavirus [4].

The pathogen of SARS is named as severe acute respiratory syndrome coronavirus (SARS-CoV) [5]. It first occurred in November 2002, and originated from Guangdong province, southern China [6]. According to the aggregate data of WHO, a total of 8096 cases were reported, resulting in 774 deaths (the case-fatality ratio is 9.56%) in 26 countries on 5 continents during the SARS epidemic [7].

The pathogen of MERS is named as middle east respiratory syndrome coronavirus (MERS-CoV) by the Coronavirus Study Group (CSG) [8]. The virus was first isolated from a patient that died of the disease in June, 2012, in Jeddah, Saudi Arabia [9]. According to the summary of WHO, at the end of January 2020, a total of 2519 confirmed MERS cases, including 866 associated deaths (the case-fatality rate is 34.38%), have been reported globally [10].

COVID-19 was initially identified in December 2019, in Hubei province, central China [11]. Soon afterwards, based on phylogeny, taxonomy and established practice, the CSG named the pathogen of COVID-19 as SARS-CoV-2 [12]. As of 30 April 2020, a total of 3,024,059 confirmed cases have been reported globally, including 208,112 deaths (the case-fatality ratio is about 6.88%) [13].

Healthcare workers (HCWs) are defined as personnel responsible for direct treatment, care, service or help of patients, mainly consisting of doctors and nurses, as well as physiotherapists, laboratory technicians, respiratory therapists, housekeepers, or even medical waste handlers [14], [15], [16]. HCWs need to be in close contact with these virus-infected patients and their contaminated environments at work, so they are at great risk of job exposure. In this study, we aim to review the infection status of HCWs in the past battles of SARS and MERS, and to summarize the infection status of HCWs during the outbreak of COVID-19, expecting to provoke sufficient attention to the HCWs infection status in patients, hospital managers, public, government administrators and HCWs themselves.

SARS among HCWs

WHO had reported 1706 HCW infected cases during the SARS outbreak [7]. As is shown in Table 1 , eight countries (China, Canada, France, Germany, Philippines, Singapore, Thailand, and Vietnam) have reported SARS-infected cases among HCWs, which account for 21.27% (1706/8020) of the total infections in these countries. However, the total number of HCW infections accounts for 21.07% (1706/8096) of all SARS confirmed cases in the worldwide [7]. In addition, to a certain extent, it can be seen that countries with more SARS cases have more absolute numbers of corresponding HCWs infections (Table 1).

Table 1

SARS infection status among HCWs in different countries.

Country	Number of total cases	Number of HCW affected	Percent
China	7429	1456	19.60
Canada	251	109	43.43
France	7	2	28.57
Germany	9	1	11.11
Philippines	14	4	28.57
Singapore	238	97	40.76
Thailand	9	1	11.11
Vietnam	63	36	57.14
Total	8020	1706	21.27

In China (included the mainland, Hong Kong, Macao, and Taiwan), 1456 HCWs have been infected with SARS, accounting for 19.60% (1456/7429) of total infection cases and 85.35% (1456/1706) of all HCW infections (Table 1). Of all the above countries, Vietnam has the highest percent of HCW infection on total SARS cases, reaching 57.14% (36/63) (Table 1). There are also many SARS infections among HCWs in Canada and Singapore, and their proportions of infections to total are also high, accounting for 43.43% (109/251) and 40.76% (97/238) respectively (Table 1).

Because Beijing has the highest number of SARS cases in China, its corresponding HCW also has the largest number of infections. SARS occurred in HCWs in more than 70 hospitals in Beijing [17], including there have four hospitals, each of them, with more than 20 cases of SARS infection among HCWs, and for which one large hospital has 41 probable HCW cases [17]. In total, 395 probable SARS cases occurred in HCWs, and the attack rate of SARS among HCWs in Beijing was estimated as 465 per 100,000 [17]. Hong Kong and Guangdong are the other two regions in China where more than one thousand SARS cases occurred. Based on the report of WHO, 386 HCWs were infected with SARS in Hong Kong, accounting for 21.99% (386/1755) of its total infection cases [7]. In Guangdong, 343 HCWs were reported to have been infected with SARS, 75.1% of whom were women [18].

Most of the probable SARS cases (57.14%, 36/63) identified in the Vietnam outbreak were HCWs, all of which occurred in a private hospital in Hanoi [19], and lack of SARS transmission among the public HCWs [20]. L Clifford McDonald and colleagues [21] reported that 164 HCWs in the greater Toronto area were infected with SARS, which is more than the total number of infected HCW in Canada as summarized by WHO (Table 1). However, the reason for the inconsistency in the total number of these reports may be that the former involved suspected cases [21]. In Singapore, the most severe nosocomial outbreak of SARS among HCWs occurred in Tan Tock Seng Hospital, with a total of 44 HCWs infected [22].

It is widely known that SARS caused 774 deaths [7], but what is unknown is the exact number of HCWs that died of SARS infection worldwide. However, by analyzing the SARS mortality rate reported by the WHO [7], it can be concluded that approximately 164 (multiplying 1706 by 0.096) HCWs might die of SARS. But we speculate that the actual number of deaths of HCWs should be far lower because the HCWs fighting against SARS in front line were basically young people with good autoimmunity. However, according to statistics (maybe incomplete) from Wikipedia, about 39 HCWs died worldwide in the battle against SARS [23].

MERS among HCWs

Unlike SARS, of which no new cases have been reported worldwide since 2004, new cases of MERS have always been arising since 2012. The WHO regularly summarizes and reports on new cases of MERS, and the latest MRES summary report currently released by WHO summarizes all cases that before February 2020 [24]. WHO's statistics on new cases of MERS in different time periods reveal that the number of infections among HCWs between different months or seasons has a large fluctuation in their corresponding total number of MERS cases, which accounts for 0–32% from 2013 to 2020 [24].

More than 84.2% (2121/2519) of MERS cases worldwide occur in Saudi Arabia. According to the latest WHO report (MERS situation update, January 2020), in Saudi Arabia, 19.1% of these 2121 MERS cases are HCWs, which means 405 HCW MERS-infected cases [24] (Table 2 ). Based on epidemiological data of confirmed MERS cases reported to the WHO from September 2012 to 2 June 2018, Amgad A Elkholy and colleagues [25] found there were 415 HCW MERS cases globally by conducting a retrospective analysis. Therefore, it can be speculated that the current number of HCW cases infected with MERS may be more than 450 (Table 2).

Table 2

MERS infection status among HCWs in Saudi Arabia and South Korea.

Country	Number of total cases	Number of HCW affected	Percent
Saudi Arabia	2121	405	19.1%
South Korea	186	25	13.44%
Global Total	2519	450a	17.86%a

Speculative data.

South Korea has the largest number of MERS infections outside Saudi Arabia in the world, with 186 confirmed cases [26]. Among them, 25 cases were occupationally acquired by HCWs, accounting for 13.44% (25/186) of total infection cases in South Korea [27] (Table 2). The super-spreader of MERS-CoV is the main cause of MERS outbreak and infection of HCW in South Korea. Having followed a single patient exposure in a hospital in South Korea, Sun Young Cho and colleagues [28] found 82 individuals were infected with MERS-CoV from a super-spreader, and 8 of them were HCWs.

The case fatality rate of MERS is 34.38% (866/2519) according to the latest WHO MERS situation update report as of January 2020 [24]. By conducting a retrospective analysis based on the epidemiological data of confirmed MERS cases reported to the WHO from September 2012 to 2 June 2018, Elkholy and colleagues [25] reported the fatality rate of HCW MERS cases is 5.78% (24/415), which is far lower than that of the non-HCWs. That is because the death of secondary case of MERS is the highest in the age group 70–79, while most of the HCWs are not in this range for younger age [24], [25].

COVID-19 among HCWs

China has 84,369 COVID-19 cases with of 4643 deaths as of 30 April 2020 [13]. Since the outbreak of COVID-19, the infection among HCWs has been reported gradually in China. By extracting data regarding 1099 patients with laboratory-confirmed COVID-19, Guan and colleagues found a total of 3.5% (about 38 of 1099) confirmed cases are HCWs [29]. Wang and colleagues reported that 40 HCW infected cases among 138 hospitalized patients [30]. In early February, the China CDC reported 1716 confirmed cases of COVID-19 among HCWs [31]. On February 24, 2020, members of the China-WHO coronavirus team announced that 3387 HCWs of 476 medical institutions in China were infected with COVID-19 (2055 confirmed cases, 1070 clinically diagnosed cases and 157 suspected cases), and more than 90% of them (3062 cases) came from Hubei Province [32].

According to the WHO COVID-19 situation report-82, as of 8 April 2020, 22,073 HCW infected cases from 52 countries had been reported globally [33]. Meanwhile, the COVID-19 cases among HCWs are still on the increase. In the United States, it has almost 10,000 HCWs have been infected with COVID-19 according to the Centers for Disease Control and Prevention in early April [34]. More recently, according to the COVID-19 situation update for the WHO European Region-Data for the week of 13–19 April 2020 (Epi week 16) [35], among the 339,657 COVID-19 cases with available characteristic records data, 54,749 of them were HCWs. Because the current reported data are incomplete and dynamic, it is difficult to estimate how many HCWs worldwide have been infected with COVID-19.

As of 30 April 2020, COVID-19 has caused 208,112 deaths worldwide [13]. Despite relatively lower case fatality rate, COVID-19 has killed far more people than SARS and MERS combined [36]. These deaths caused by COVID-19 include some HCWs. China CDC analysis of epidemiological characteristics of COVID-19 cases as of February 11, 2020, found that 5 HCWs died of COVID-19 [31]. According to relevant news reports collected and summarized by Wikipedia, as of March 27, 2020, at least a total of 88 HCWs have died of COVID-19, of which 36 are in China, 31 in Italy, 13 in Iran, 5 in France and 3 in United States [37]. However, some of them died of COVID-19 epidemic prevention and control work rather than COVID-19 infection [37].

Although the COVID-19 epidemic in China has now been basically under control, it is still spreading in many other countries outside China. It is unclear how many HCWs have been infected with COVID-19 due to work, and how many HCWs have died in line of duty. It is foreseeable that despite the best protection, there also will be more HCWs infections. To know the specific situation of HCWs infection with COVID-19, further statistics and analysis are needed for subsequent studies after the epidemic is under control.

Discussion

Hospital is the important place for secondary transmission of SARS, MERS and COVID-19 [14], [38], [39]. Densely staffed, and packed with public facilities and people with compromised immunity, hospitals provide objective conditions for the secondary transmission of these infectious diseases. Generally, emergency department, infectious disease department, fever clinic, intensive care unit and respiratory medicine department are the main departments that cause the spread of these diseases. Therefore, HCWs in these departments may well be infected with SARS, MERS and COVID-19 at work.

As is known, 3 ophthalmologists in the Central Hospital of Wuhan, Hubei died of COVID-19 [40], which is a wake-up call that ophthalmology is also a high-risk department that can cause HCWs infection of COVID-19. It has been found that SARS-CoV-2 can be detected in tears and conjunctival secretions of patients with COVID-19 [41]. Studies suggest that when no eye protection was worn, SARS-CoV-2 could also possibly be spread by aerosol contact with conjunctiva and cause infection of HCWs [42], [43], [44]. Close proximity between patients and ophthalmologists during slit lamp examination, intraocular pressure measurement, direct ophthalmoscopy, pupillary dilatation and others may pose an infectious risk to ophthalmologists [44]. Hence these factors may increase the risk of cross-infection between HCWs and patients in the department of ophthalmology.

Nosocomial transmission of SARS, MERS and COVID-19 can be categorized as patient-to-patient, patient-to-HCW, HCW-to-patient, and HCW-to-HCW. Confirmed or suspected cases of these infectious diseases can be physically separated by setting up isolation wards or establishing isolation hospitals to avoid patient-to-patient transmission [38], [45], [46]. Therefore, the subsequent key issue that needs to be persistently considered, solved and prevented is how to prevent the transmission of patient-to-HCW.

Reasons for patient-to-HCW transmission involve poor institutional infection control measures, lack of awareness and preparedness in the early stage of disease outbreak, lack of training on infection control procedures, and poor compliance with personal protection equipment (PPE) use. To be specific, the recognized risk factors are close contact in physical examination and therapy, direct physical contact with body fluid and excreta from patients, airway suctioning, endotracheal intubation and cardiopulmonary resuscitation. However, the most dangerous situation is when they are facing the super-spreader, whose transmission ability is simply overwhelming [47], [48], [49]. Therefore, how to identify the super-spreaders as early as possible is of vital importance as to reducing the chance of patient-to-patient and patient-to-HCW transmission.

Hand hygiene is recognized as an easy and effective way to prevent the spread of respiratory infections that include SARS, MERS and COVID-19 [38], [50], [51], [52]. Correspondingly, wearing masks is the simplest and most important PPE to prevent infection of these infectious diseases. Both surgical and N95 masks can effectively prevent HCWs from being infected with SARS, MERS and COVID-19. However, if conditions permit, wearing N95 masks maybe relatively better [53], [54], [55], [56], [57]. Other PPE such as gloves, hats, protective clothing, isolation clothing and others are also important for HCWs to prevent infection, depending on the working environment. Improving the compliance of using PPE and standardizing the putting on and taking off process of these PPEs can better protect HCWs.

By investigating the frontline of HCWs combating SARS, Cindy W C Tam and colleagues reported that the stress and psychological distress among HCWs were high, accounting for 68% and 57% respectively [58]. Robert Maunder also reported that a high level of distress was experienced by 29–35% of HCWs, and the relevant contextual factors were having contact with SARS patients, being a nurse and having children [59]. Similarly, study conducted by Namhee Oh and colleagues reported that high stress had also shown in HCWs engaged in patient nursing during the MERS outbreak [60]. Um and colleagues found that 26.6% doctors involved in MERS care showed symptoms of depression [61].

Recently, Li and colleagues [62] reported the prevalence of depression and anxiety was 21.3%, 19.0%, respectively among public HCWs in the frontline during the COVID-19 epidemic. Lai and colleagues [63] analyzed 1257 mental health status among HCWs exposed to COVID-19, finding 50.4%, 44.6%, 34.0% and 71.5% of them reported depression, anxiety, insomnia and distress, respectively. And frontline HCWs engaged in direct diagnosis, treatment, and care of COVID-19 patients were associated with a higher risk of depression, anxiety, insomnia and distress. HCWs were anxious regarding their safety and reported psychological effects from mortality reports from COVID-19 infection [64]. Therefore, hospital administrators need to pay sufficient attention to and ease the stress and psychological distress on frontline HCWs fighting the COVID-19 epidemic.

Previous studies have found that some HCWs developed post-traumatic stress syndrome after coping with SARS or MERS outbreaks [65], [66], [67], [68]. Because of perceived risk of fatality from SARS, increased work stress, and affected social relationships, some HCWs were even considered switching or resigning from their job [69]. These previous evidences remind hospital managers, that during the outbreak of COVID-19, they must pay attention to the post-traumatic stress syndrome and occupational concerns of HCWs, and should temporarily invite psychologist or psychological counselor to participate in the management of the hospital if necessary.

In addition to providing as much psychological support and counseling as possible for the HCWs fighting the COVID-19 epidemic, hospital managers should also provide strong logistical support for these front-line HCWs, such as ensuring the supply of protective equipment, giving appropriate additional financial assistance, and taking care of their family difficulties. And in the future, hospitals and health administration departments may also consider giving these HCWs preferential promotion opportunities under the same conditions.

In less than two decades, humans have experienced SARS and MERS outbreaks and are currently experiencing the outbreak of COVID-19. It can be said that COVID-19 is the most severe blow to human health among the three infectious diseases, and it is not yet known how long it will last. After experiencing SARS and MERS, HCWs appeared to be more vigilant against similar infectious diseases [70], [71], [72]. However, in the battle against COVID-19, the vigilance does not seem to have played a due role in HCWs on the grounds that a large number of HCWs have been infected at work, indicating SARS-CoV-2 is more troublesome than SARS-CoV and MERS-CoV.

It has been five months since the outbreak of the COVID-19 epidemic in December 2019. The duration of this epidemic cannot be predicted, nor can the possibility be ruled out that it will cause seasonal epidemics like influenza in the future [73], [74]. As for the impact of COVID-19 on HCWs, many subsequent studies can and need to be performed, such as collecting the detailed statistics of the infection status of HCWs in each country, subdividing the infection status according to their different job positions, comprehensively investigating their psychological and mental problems, and researching their possible post-traumatic stress syndrome.

The pandemic of COVID-19 gave medical students a big practical lesson. The Chinese Ministry of Education has postponed the spring start of colleges and universities and discourages medical students from returning to hospitals for internships before the outbreak is under control [75]. Italy government has announced a plan to add 20,000 new HCWs to meet the demand to fight against COVID-19, and called on students who have completed their medical degrees and are in the final year of specialist training to participate [76]. The England chief medical officer has announced that the final year medical students may have their duty rights extended [77]. Anyway, governments have made appropriate arrangements for medical students in their countries according to their own epidemic situation.

However, on the other hand, we also need to consider whether the COVID-19 epidemic has affected the future career planning of medical students, and whether it has caused a psychological burden and discouraged them from engaging in the medical industry in the future. In the face of the current global epidemic disaster, and alike major outbreaks that may also occur in the future, we should encourage medical students in a suitable way to strengthen their confidence in the medical industry, and encourage young people to choose to study medicine.

Authors’ contribution

Jian Xiao and Min Fang contributed equally to this work.

Conception and design: Jian Xiao, Min Fang

Analysis and interpretation of the data: Jian Xiao, Min Fang, Bixiu He.

Drafting of the article: Jian Xiao, Min Fang, Bixiu He.

Critical revision of the article for important intellectual content: Qiong Chen, Jian Xiao.

Final approval of the article: Bixiu He, Qiong Chen.

Administrative, technical, or logistic support: Bixiu He, Qiong Chen.

Collection and assembly of data: Min Fang, Jian Xiao, Bixiu He.

Conflicts of interest

The authors disclosed no conflicts of interest.