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      A lesson learned from the MERS outbreak in South Korea in 2015

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      The Journal of Hospital Infection
      The Healthcare Infection Society. Published by Elsevier Ltd.

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          Abstract

          Introduction Middle East respiratory syndrome (MERS) viruses can spread rapidly to many people, and thus pose a global pandemic threat. MERS viruses broke out in one hospital in Pyeongtaek, South Korea (hereinafter Korea), on May 2015, 2015. Thirty-six patients died and 186 people were infected. 1 The Koreans experienced a national crisis, contributed to by the poor initial response of the affected hospitals, an inadequate response from the government, the economic depression that followed the outbreak, and the psychological impact of the outbreak on the Korean population. To date, the Korean government has not taken systematic actions to deal with global pandemics in the future. This article comments on how Korea can learn from its response to a MERS outbreak to be better prepared to control other epidemic and pandemic infectious diseases. We define the Korean reaction (which includes four major stakeholders) as a hospital infection control issue (Figure 1 ). The four stakeholders were either directly or indirectly involved in the outbreak of MERS in Korea. We argue that the nation has to transform its current reaction into an emergency management issue involving all stakeholders. Figure 1 The necessity of a paradigm change in the Korean response. MERS, Middle East respiratory syndrome. MERS outbreak as a hospital infection control issue Hospitals Mainly because of poor ventilation and ineffective disinfection in one hospital, MERS viruses began to spread rapidly to patients, visitors, and even to healthcare workers. A few neighbouring hospitals also showed a similar pattern of nosocomial transmission. 2 Consequently, healthcare workers made all efforts to improve infection control or hygiene; however, this took time. Therefore, hospitals became major stakeholders in preventing the loss of human lives. Government agencies The Korea Centers for Disease Control and Prevention (KCDC) under the Ministry of Health and Welfare (MW) insisted on not sharing MERS information from the hospitals with the public at the initial stage of the outbreak under the pretext of hospital protection, although in reality this decision may have been based on nepotism. Further, the Ministry of Public Safety and Security (MPSS), which is a single, comprehensive emergency management agency, did not implement any specific action to prevent the loss of human lives. Thus far, only the KCDC has tried to improve preparedness against similar pandemics. Residents Some Koreans were involved in manipulating the facts on the MERS outbreak and then spreading rumours through the Internet or mobile phones. Further, given the Korean culture, many people did not realize that it was not advisable for them to visit the infected patients in hospitals and share their drinks or foods. Also, a few infected residents attempted to go to public places without permission from the government. However, the majority of residents considered the MERS outbreak to be a national emergency and thus paid attention to its progress by exchanging relevant information. Others Other stakeholders took steps to efficiently respond to the outbreak of MERS. For instance, business establishments continued to operate but measured the body temperature of their customers and distributed hand sanitizers to them, which nonetheless constituted an incomplete preventive measure. Mass media also attempted to trace and reveal the sources of rumours, in the process causing political conflicts. Many schools temporarily cancelled classes, although unnecessarily, so that their students could stay at home. The military isolated infected soldiers in remote facilities, but this move came rather late. MERS outbreak as an emergency management issue for all stakeholders Korea did not give all four stakeholders equal involvement in dealing with the MERS outbreak. Rather, one stakeholder – healthcare workers in hospitals – played multiple roles in controlling MERS viruses. Thus, the situation was perceived as almost entirely a hospital infection control issue. Considering that the MERS outbreak was not only a health issue but also an emergency management issue, the model for controlling similar epidemics or pandemics in the future-oriented model should involve all stakeholders in an early and co-ordinated response. Emergency management consists of four phases: emergency prevention/mitigation (legalization, inspection, disease prediction, etc.), emergency preparedness (emergency operation planning, training, etc.), emergency response (infection control, health treatment, etc.), and emergency recovery (insurance, medical evaluation, etc.). 3 Appropriate roles and responsibilities in all the phases have to be assigned to each of the four stakeholders in advance. Although many stakeholders tried to play their own roles during the MERS outbreak in Korea, their responses were somewhat late and unco-ordinated, and thus contributed to the national crisis. In fact, their specific roles and responsibilities should have been assigned before the MERS outbreak. In this context, nations should implement regular training in and exercise of emergency management measures. Pandemics, as a type of emergency, pose three kinds of risk: loss of human lives, economic damages, and psychological impact. In the case of the MERS outbreak in Korea, local government and hospitals were oriented toward decreasing the number of deaths, mainly because they regarded the outbreak as an infection control issue. They did not realize the need to address the economic damage or the psychological impact on the general population, especially at the initial response stage. Without a co-ordinated response, the MERS outbreak caused considerable economic damage in Korea. Almost nobody dared to visit shopping malls for fear of infection. Further, because MERS scared away foreign tourists, including many Chinese and some Japanese visitors, the tourism industry suffered considerably. Thus, the national economy was significantly depressed, and the economic growth projection fell to about 2%. 4 Regarding the psychological impact, most people worried about catching MERS and thus wore masks whenever they went out. Similarly, many primary and middle schools throughout the peninsula cancelled classes to protect their students from MERS, contrary to the recommendation of the World Health Organization. Hospitals Hospitals played a major role in reducing the loss of human lives during the MERS outbreak; however, this does not mean that they have done extraordinary work. After Pyeongtaek St Mary's Hospital failed to screen the first infected patient, MERS viruses spread to many parts of Korea. Further, the Samsung Medical Center in Seoul refused to share MERS information with the public, which made the situation worse. Hence, hospitals need to be more professional in dealing with infection control, in particular by educating quarantine doctors and in following the Hippocratic Oath. 5 Government agencies The KCDC and MW will certainly remain the major government institutions that should take charge when a pandemic occurs in Korea. However, the MPSS must also become proactively involved during such an outbreak. Thus far, the MPSS officially considers only three types of hazard under its management scope: fires, floods that accompany typhoons, and maritime accidents. As a co-operative or co-ordinating institution in relation to all hazards, the MPSS must therefore extend its activities to the KCDC, other departments, and local government, and apply countermeasures against new diseases. Residents Contrary to the expectation of the government, the level of emergency awareness of Korean residents increased considerably during the MERS outbreak, particularly as the death toll rose. These residents should now directly demand that the government and the whole nation take more systematic actions against new pandemics toward achieving efficient emergency management. The public must also be willing to challenge cultural practices, and in particular to co-operate with restrictions on visiting hospitals. Others Other stakeholders, including business establishments, mass media, schools, and the military played their own roles in responding to the outbreak of MERS within their areas. However, they should have approached the issue more seriously from the beginning of the emergency response instead of merely acting as outsiders in a national crisis. Considering that a pandemic may spread quickly to anyone, these entities should join the major stakeholders from the initial response stage. Conclusion The MERS outbreak in Korea in May to July 2015 caused the biggest loss of human lives due to the disease outside the Middle East. Thus far, however, the Korean government has yet to comprehensively improve its national response against pandemics. The key tenet is that Korea must not consider the MERS outbreak to be a hospital infection control issue. Rather, the nation must regard such an outbreak as an emergency management issue involving all stakeholders, particularly in fighting against new pandemics in the international community. Conflict of interest statement None declared. Funding sources None.

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          MERS in South Korea and China: a potential outbreak threat?

          First reported in September, 2012, human infections with Middle East respiratory syndrome coronavirus (MERS-CoV) can result in severe respiratory disease, characterised by life-threatening pneumonia and renal failure. 1 Countries with primary infections of MERS-CoV are located in the Middle East, but cases have been occasionally exported in other countries (figure ). Human-to-human infections of MERS-CoV are rare 2 and confirmed cases are usually traced back to contact with camels, an intermediate host species for MERS-CoV. 3 Figure Imported MERS-CoV human cases and affected countries Countries affected by MERS-CoV are shown in red, including the recent cases in South Korea and China. Arrows show MERS-CoV importations. Red arrows show the recent importation of MERS-CoV in South Korea and China. Countries involved in the importation of MERS-CoV in South Korea and China are shown in dark red. As of May 24, 2015, worldwide, a total of 1134 cases and 427 deaths (case fatality rate 37·7%) have been reported, according to WHO. 4 There is no approved vaccine or treatment. On May 11, 2015, a 68-year-old male in South Korea developed symptoms and sought medical care at a clinic between May 12–15, before admittance into hospital on May 15. 4 The patient had been travelling between April 18–May 3 through Bahrain, the United Arab Emirates, Saudi Arabia, and Qatar. He was asymptomatic upon return to South Korea on May 4, but tested positive for MERS-CoV on May 20, along with two additional cases: his 64-year-old wife, and a 76-year-old male who was a fellow patient. 4 Concerns of further MERS-CoV spread were confirmed when a 71-year-old male fellow patient, the daughter of the 76-year-old case, and two medical staff developed symptoms and were diagnosed with MERS-CoV infection (appendix). As of May 29, 2015, South Korea has 12 laboratory-confirmed cases of MERS-CoV, and more than 120 additional contacts under surveillance. 5 On May 28, a 44-year-old male traveller from South Korea to Huizhou, China was admitted into hospital. MERS-CoV infection was confirmed on May 29, marking the first laboratory-confirmed case in China (appendix), and the patient was immediately put in isolation. This patient was the son of the 76-year-old South Korean patient. He had visited his father in the hospital on May 16, developed symptoms on May 21, 6 and travelled to Hong Kong by plane on May 26 before arriving by road into mainland China via Shenzhen. 6 In response, the Chinese health authorities promptly placed 38 high-risk contacts under surveillance, but it is not known whether additional contacts exist and further MERS-CoV infections in China remains a possibility. This series of events highlighted issues with the current surveillance system put in place to prevent the importation of infectious diseases. The diagnosis for MERS-CoV infection was made on May 20 for the 76-year-old patient. His 44-year-old son should have been monitored as a close contact of the laboratory-confirmed case, with provisional quarantine and testing upon development of symptoms and isolation upon a positive diagnosis. Such a high-risk case should not be travelling until after the incubation period, which is between 2–15 days for MERS-CoV. 2 Non-compliance by the patient regarding travel advice likely contributed to this scenario. 5 These events serve as a timely reminder that natural geographical barriers against pathogens can now be easily overcome through trade and travel, and marks the first MERS-CoV import case that did not come directly from the Middle East. These developments are worrisome given that Hong Kong airport is a major international transport hub, and thus any potential infections can travel worldwide in a short time. After dealing with several pandemic threats over the past 15 years, notably severe acute respiratory syndrome coronavirus (SARS-CoV) in 2003, H1N1 influenza in 2009, and Ebola virus in 2014–15, authorities now have ample experience in outbreak response compared with past years. In addition to the need for increased vigilance from health authorities, compliance by the public is crucial for the effective implementation of outbreak responses. Everyone is responsible for upholding the principles of public health, and must play their part to minimise the chances of disease transmission across borders.
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            Middle East Respiratory Syndrome– advancing the public health and research agenda on MERS- lessons from the South Korea outbreak

            The weekly epidemiological record of the World Health Organisation 15th May 2015 1 states that ‘the cases of Middle East Respiratory Syndrome (MERS) recently exported to other countries have not resulted in sustained onward transmission to persons in close contact with these cases on aircraft or in the respective countries outside the Middle East.’ This situation has changed rapidly and remarkably. Five days after the publication of this report, the first case of a MERS-coronavirus (MERS-CoV) infection in Seoul, South Korea was reported on 20 May 2015 2 . This patient had a history of recent travel to the Middle East. Over the ensuing three weeks, the number of secondary, tertiary and perhaps quaternary cases of MERS from this single patient rose rapidly and has become the largest case cluster of MERS occurring outside the Middle East. The Korean outbreak appears from the available data to be attributable to poor infection control measures, although the hospital air-conditioning system's lack of ventilators may have resulted in the rapid extensive spread of MERS among patients and staff 3 . Furthermore, MERS-CoV was detected in bathrooms and on doorknobs indicating ineffective disinfection procedures. As of June 9th 2015, there have been 95 cases (with 7 deaths) of MERS-CoV infection associated with the South Korean outbreak 3 . Over two thirds of all confirmed cases have been reported from St. Mary's Hospital, a 400 bed facility in Gyeonggi Province, Seoul and at least 14 facilities have reported MERS cases during the outbreak. This unusually large number of secondary (80 cases) and tertiary (14 cases) associated with an imported case of MERS by a traveller is a significant development (as per 11th June 2015). Furthermore, whilst the Korea outbreak has focussed global attention, a nosocomial outbreak of MERS in Hufoof, Saudi Arabia has been on going since 20 Apr 2015 and resulted in 26 cases over the past 3 weeks 4 . There continue to be MERS cases reported from Jeddah and Riyadh, which are “sporadic” community cases. To date Saudi Arabia has reported 1026 MERS cases including 450 deaths (44 percent) since the first MERS case was reported in September, 2012. The South Korean and Hufoof outbreaks raise several important concerns: First the Korean outbreak emphasizes that MERS-CoV remains a major threat to global health security and could have epidemic potential with time, even in the absence of virus mutation. Second the nature of the virus and its evolution into a more virulent form continues to need close monitoring. Genomic sequencing studies of MERS-CoV obtained from the first Korean case published by the Chinese Center for Disease Control and Prevention 5 has shown homology with MERS-CoV strains originating from Saudi Arabia. Whilst no significant variation has been identified it remains crucial that genomic studies for as many MERS cases as possible are performed. Third, up to a million pilgrims from over 182 countries will travel to Mecca, Saudi Arabia for the Ramadan period which begins on June 18th 2015 and the threat of further global spread remains. Fourth, for the past 18 months, MERS and other global infectious diseases threats were totally overshadowed by the Ebola virus disease epidemic 6 , highlighting the inadequacies of global surveillance systems to focus concurrently on several emerging and re-emerging infectious diseases simultaneously. Fifth, many basic questions about the epidemiology, pathogenesis and management of MERS-CoV remain to be answered 8 . Sixth, it's been 3 years since MERS was identified as a lethal new viral respiratory infection of humans 9 and primary cases of MERS-CoV infection continue to occur throughout the year 7 in the Middle East. The South Korean outbreak now illustrates the need to enhance MERS-CoV surveillance systems, and heightens global awareness of MERS and the importance of infection control measures. Finally, the Korean outbreak emphasizes the importance of individuals, especially healthcare workers, recognizing that they may have been exposed to MERS patients and seeking medical care and self-quarantining at an early time during the disease course. Moving forward, it is critical that global efforts are focussed urgently on the basic science and on clinical and public health research so that the exact mode of transmission to and between humans, and new drugs and other therapeutic interventions and vaccines can be developed6, 7. Two coronaviruses, SARS-CoV and now MERS-CoV, which cause severe respiratory disease with high mortality rates emerged within the past two decades 10 , reinforcing the need for clinically efficacious antivirals targeting coronaviruses. Lessons learnt from the recent Ebola Virus Disease could also be applied to MERS 11 . Whilst MERS does not yet constitute an International Public Health Emergency the Korean outbreak is an extraordinary event. Previous estimates of the epidemic potential of MERS-CoV have not found that it had pandemic potential 12 , suggesting that airborne, human-to-human transmission is rare, but the present outbreak indicates that simple hygiene is important, especially in health care facilities. The index patient arrived at a health care system that was able to identify MERS as a risk given his travel itinerary and had the laboratory resources to rapidly identify the virus. With continuing spread of MERS-CoV to countries outside the Middle East and to all continents, MERS remains a public health risk and possible consequences of further international spread could be serious in view of the patterns of nosocomial transmission within healthcare facilities. Further spread to countries with weak health systems and laboratory facilities unable to rapidly identify an unexpected virus may result in a widespread outbreak or an epidemic in many of the 182 countries from which Ramadan, Hajj and Umrah pilgrims originate. Declaration: Authors declare no conflicts of interest.
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              What can we learn from MERS outbreak in South Korea?

              Since 20th May 2015, the world has been paying significant attention to the emerging outbreak of Middle East Respiratory Syndrome (MERS), rather than in the Middle East but in South Korea. According to the report of the Ministry of Health and Welfare's Central MERS Response Team, as of 11 Jun 2015, the number of South Koreans diagnosed with the Middle East Respiratory Syndrome (MERS) increased to 122 since the first case was reported, including 9 deaths [1]. More than 2800 persons have been quarantined and hundreds of schools have been closed. The number of MERS cases in South Korea has been the second all around the world, only less than that of Saudi Arabia. As reported, one case occurred in a Korean man who traveled to China and had been confirmed to have close contact with two relatives with MERS-CoV infection, and this patient became the first reported case in China. 1 The earliest MERS patients The index case was a 60-year-old man who presented with acute pneumonia and subsequent renal failure with a fatal outcome in Saudi Arabia in June, 2012 [1]. A novel coronavirus was isolated from the sputum of the patient in Erasmus Medical Center (EMC) in Rotterdam, Holland, therefore, initially it was called the EMC coronavirus. According to a retrospective survey, the earliest MERS cases from Jordan were found at April 2012, which were the first cases of cluster. Both the 2 cases were found in medical staffs and they both died later. Since the sources of all the MERS patients were associated with the Middle East, the WHO in May 2013 named it as Middle East Respiratory Syndrome [2], [3]. 2 The clusters During the past three years, the clusters of MERS have been reported for many times (more than ten), with only a few clusters were found with hundreds of cases. The known data showed that nosocomial infections accounts for most of the cluster cases, mainly occurred in medical staffs, and secondary in the family members of the MERS patients or other people who had close contacts with the MERS-CoV infected patients. However, there is still not very clear about how the medical staff became infected, what the Personal Protective Equipment (PPE) they used and how the standard precautions in these hospitals were implemented. The following is the cluster outbreaks in hospital. A cluster occurred from October to November 2012 in four men of a family in Riyadh, Saudi Arabia, two of whom died. None of the 24 other family members who lived with the infected patients or 124 healthcare workers who had contact with them became infected [4], [5]. In April 2013, another cluster of 23 confirmed cases of MERS-CoV was detected in Al-Hasa in the Eastern Province of Saudi Arabia. Almost all cases were directly linked to person-to-person exposure. Most of them are in the hemodialysis (9 cases) or intensive care (4 cases) units of a same hospital. Two cases are healthcare workers. Three family members of over 200 household contacts (all of whom had visited the hospital) were proven infected [1], [5]. More than 500 cases was reported in Saudi Arabia and the United Arab Emirates in March and April 2014, the majority represented hospital-based outbreaks in the Saudi Arabian cities of Jeddah (255 cases), Riyadh, Tabuk, and Madinah and in Al Ain City, Abu Dhabi, United Arab Emirates, and included cases in healthcare workers, patients admitted for other medical problems, visitors, and ambulance staff. 75% of those cases had known sources of exposure. However, there has been no clear evidence of sustained community transmission of MERS-CoV. Of the family members, 7 of 554 were infected (1.3%) [4], [5], [6]. 3 The importance of hospital infection control From the current reported cases in the South Korean, the epidemic is primary caused by hospital infection. After9 days of onset, the first case was diagnosed and isolated, which suggested the importance of early detection and hospital infection control. The reported cases in South Korea were distributed at least 9 hospitals, but the involved hospitals are as many as 26 or even more. Because of the numerous contacts, there will be more new cases reported in the future. The exact source and mode of transmission of MERS-CoV to human beings is unknown. Initial investigations suggested that MERS-CoV originate in bats, however, MERS-CoV has never been isolated from bats. Recent studies suggested that dromedary camels may be the intermediate host of MERS-CoV, and human can be infected through contact with infected dromedary, for example, exposure to secretion, excreta (urine and stool), undercooked dairy or meat products. The virus appeared to be able to spread from human to human through respiratory droplets, and it can also spread through close contact with secretions or excretions of the patients infected by MERS-CoV. The early symptoms of MERS include fever, chills, fatigue, headache, muscle pain, etc., followed by cough, chest pain, dyspnea [5], [6]. About 30% of the cases may suffer from vomiting, abdominal pain, diarrhea and other symptoms. The severe cases can develop severe pneumonia within 1 week, which may lead to acute respiratory distress syndrome (ARDS), acute renal failure, and even multiple organ failure (MODF). It is worth noting that a considerable portion of the patients develop diarrhea firstly in the early onset. The chest radiography abnormalities could be from 90% to 100% in MERS Patients. But the image findings on chest radiography can range from minimal to extensive abnormalities, it presented with viral pneumonitis and acute respiratory distress syndrome, with bilateral hilar infiltration, unilateral or bilateral patchy densities or infiltrates, segmented or lobar opacities, ground-glass opacities [7], [8], [9], [10]. The clinical manifestations of MERS are diverse and complex, short of specificity, so it is difficult to make early diagnosis. The medical staff should pay attention to the epidemiological history and should strengthen the hospital infection control measures and perform standard precautions.
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                Author and article information

                Contributors
                Journal
                J Hosp Infect
                J. Hosp. Infect
                The Journal of Hospital Infection
                The Healthcare Infection Society. Published by Elsevier Ltd.
                0195-6701
                1532-2939
                24 October 2015
                March 2016
                24 October 2015
                : 92
                : 3
                : 232-234
                Affiliations
                [1]Department of Emergency Management, Inje University, Gimhae, South Korea
                Author notes
                []Address: Department of Emergency Management, Inje University, 197, Inje-ro, Gimhae, 50834, South Korea. Tel.: +82 (0)10 2511 2593. ha1999@ 123456hotmail.com
                Article
                S0195-6701(15)00397-7
                10.1016/j.jhin.2015.10.004
                7124385
                26601605
                cc212420-8d64-4a47-aace-db4258e6f344
                Copyright © 2015 The Healthcare Infection Society. Published by Elsevier Ltd. All rights reserved.

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                History
                : 29 September 2015
                : 8 October 2015
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                Infectious disease & Microbiology
                Infectious disease & Microbiology

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