The Middle East respiratory syndrome coronavirus (MERS-CoV) outbreak in 2015 was an
unprecedented challenge to academic medical centers in the Republic of Korea. It involved
186 confirmed cases and 38 fatalities all across the country, and notably, nearly
half of the cases were nosocomial infections (1). This tragic outbreak led to a call
for fundamental changes in the Korean healthcare system to prepare for potential infectious
disease outbreaks in the future (2,3). Academic medical centers set out to transform
their environment with two major goals of 1) preparedness for emerging infectious
diseases, and 2) reduction of nosocomial infections (4). Here we describe an example
of a major academic institution, Seoul National University Bundang Hospital (SNUBH),
focusing on three key aspects of preparedness: renovating infrastructure, training
healthcare professionals, and constructing a community-based response system to infectious
disease outbreaks.
Renovating infrastructure
On September 1, 2016, the national health insurance in Korea introduced a new policy
providing reimbursements for hospitals equipped with infection control and prevention
measures meeting new standards. Eligible hospitals could be reimbursed at a per diem
rate for every inpatient. The rate was determined by the number of infection control
nurses per inpatient beds (one per 150 beds for tier 1, one per 200 beds for tier
2) (5). To meet the tier 1 reimbursement policy, SNUBH newly hired qualified personnel
to increase the number from three full-time and two part-time staff to nine full-time
staff. They developed hospital protocols for responding to emerging infectious diseases,
conducted surveillance of nosocomial infections, and educated hospital staff. An enhanced
workforce improved the hospital’s capacity for nosocomial infection control and pandemic
preparedness.
Another important change was the installation of high-level isolation units (HLIUs)
(6). Because of the ever-increasing trend of international travel and immigration,
there was an urgent need to renovate the hospital infrastructure in order to prepare
for novel infectious diseases without compromising the health and safety of the health
care workers. SNUBH leadership formed a new task force in February 2016 to develop
HLIUs. A total of nine single-patient rooms were installed by August 2017. All rooms
were designed to generate a negative pressure environment to minimize nosocomial transmissions
amidst a highly transmissible disease outbreak. Five of those were also equipped to
provide critical care including mechanical ventilation, renal replacement therapy,
and extracorporeal membrane oxygenation. The costs of installing HLIUs were partly
funded by the government through the Korea Centers for Disease Control (KCDC)’s initiative
for nationally designated isolation units. As of 2019, there were a total of 535 beds
within nationally designated isolation units in 29 hospitals nationwide, established
through this initiative. Among them, 198 beds were in negative pressure isolation
units, including nine at SNUBH (7).
To guide the clinical management of patients with highly contagious diseases in HLIUs,
the infection control office of the hospital developed an in-house protocol with the
aim of preventing secondary transmissions of pathogens. To develop this, infection
control officers reviewed relevant KCDC protocols and adapted them through discussions
with a multidisciplinary group of hospital staff. Additionally, they defined an organizational
structure in which members of the Infectious Control Task Force would be activated
in times of active infectious disease threats with predefined roles in order to enable
organized decision-making and to facilitate effective communication. Furthermore,
the infection control office stratified the hospital’s responses according to the
level of the national alert system for infectious diseases (Table 1
). Detailed practice manuals - for example, environment and waste management and close
contact management - were also developed to be readily applicable in epidemic situations.
For intra- and inter-hospital HLIU patient transfers, patient flows were specified
in order to minimize the transmission risks to other patients and hospital staff.
An entrance was also designated for exclusive use for transporting patients requiring
HLIUs or contaminated materials. The first version of the protocol was approved by
the Medical Executive Committee at SNUBH, enacted in August 2017, and updated on a
yearly basis (see web-only Supplementary Table S1).
Table 1
Hospital response protocols by the national alert level for infectious diseases
Table 1
National alert levels
Hospital response
Departments in charge of infectious disease control
Infectious diseases control task force
Management of patient with EIDs
Control of the hospital entrances
Education and training of all hospital staff
Promotion of infection control measures
Mobilization of healthcare workers and resources
Attention (Blue)
EIDs overseas with no immediate threat of importation
■
Review relevant KCDC protocols
■
Notify and educate on general infection control measures
Caution (Yellow)
Domestic importation of EIDs from abroad
■
Monitor the national outbreak status
■
Hold simulation exercises
■
Activate an infectious diseases control task force for key decision making
■
Prepare to operate high-level isolation units (HLIUs)
■
Prepare to operate screening clinics outside of hospital entrance
■
Distribute guidelines for infectious disease response
■
Educate the staff on the specifics of infection control measures
■
Post public health information leaflets and banners around the hospital
Alert (Orange)
Confined spread of EIDs within the country
■
Operate a 24-hour emergency response system
■
Strengthen infection control measures
■
Admit and treat patients with EIDs in HLIUs
■
Operate screening stations at hospital entrances and screening clinicsa
■
Strengthen the education and training for all hospital staff (e.g. PPE training)
■
Strengthen the promotions of public health information within the hospital
Serious (Red)
Spread of EIDs in communities across the country
■
Strengthen the operations of infectious diseases control task force (e.g., daily hospital-wide
updates)
■
Strengthen infection control measures
■
Admit and treat patients with EIDs in HLIUs
■
Install temporary isolation wards using negative pressure devices
■
Strengthen the entrance control
■
Strengthen the education and training
■
Establish occupational health program (e.g., daily self-report)
■
Devise public health promotional plans through media to reach the surrounding communities
■
Mobilize the reserve hospital staff and resources
■
Devise a regional and national plan for infection control
EIDs: Emerging infectious diseases.
a
The screening stations at the hospital entrances are aimed to screen patients and
visitors for symptoms related to EIDs (e.g., fever, respiratory symptoms) or epidemiologic
risk factors (e.g., recent travel history to an endemic region) to prevent any unprepared
entry into the hospital. Suspected people are triaged to the screening clinic, a temporary
facility located outside of the main hospital building, for further evaluation for
EID.
Lastly, to protect the healthcare workers caring for patients in the HLIUs, SNUBH
procured a large supply of personal protective equipment (PPE) through coordination
with the Korean government. This step was prompted by the hospital’s experiences of
admitting suspected patients with Ebola and MERS, prior cardiopulmonary resuscitations
in HLIUs, and PPE training for hospital staff.
Training healthcare workers
SNUBH introduced multiple new education programs to enhance healthcare workers’ understanding
and preparedness for emerging infectious diseases. A new session entitled “Responding
to emerging infectious diseases” was added to the mandatory education program for
all hospital employees. In addition, PPE training programs were conducted regularly.
Every PPE training session included a demonstration of PPE donning and doffing and
hands-on exercises. Participants practiced as a pair, using a fluorescent solution
to evaluate the degree of contamination during the PPE doffing procedure. Basic supplies
of this training included an N95 respirator and a set of level D PPE (defined by the
KCDC), which was comprised of a waterproof coverall with an attached hood, goggles,
inner and outer gloves, and shoe covers. An advanced training session was performed
with powered air-purifying respirators (PAPRs) or level C PPE, composed of chemically-resistant
clothing and eye protection. Since the first regular PPE training held on January
18, 2017, SNUBH provided 1,191 days of staff training between 2017 to 2019, and nearly
40% of the training included the use of PAPRs (see web-only Supplementary Table S2).
The PPE training was particularly emphasized for clinical staff taking care of patients
in HLIUs. Physicians and nurses were required to have completed the PPE training in
the prior 6 months in order to work at HLIUs. Staff involved in critical care at HLIUs
were also required to participate in annual trainings with PAPRs.
Furthermore, simulation exercises were developed to prepare for complex clinical situations
and first conducted in August 2017, including a clinical scenario of an admission
of a patient with MERS-CoV to the HLIU. Participants practiced wearing full sets of
PPE, entering a negative pressure room, managing clinical problems, and safely taking
off PPEs upon exiting the room. Three months later, the hospital started a biannual
multidisciplinary workshop with simulation exercises and subsequent evaluations. Based
on feedback, the hospital improved its clinical protocols and equipment, and simulated
multiple clinical situations, including an inpatient outbreak from secondary transmission,
patient triage and management in the emergency department, cardiopulmonary resuscitation
on infected patients, and managing the remains of infected patients who died in the
hospital. In 2019, the workshop was expanded into a joint workshop with other neighboring
hospitals in the province that had nationally designated isolation units.
The clinical workforce harnessed experience accumulated from treating patients suspected
of MERS-CoV and viral hemorrhagic fevers (137 and 6 patients from 2017 to 2019, respectively).
Before the COVID-19 pandemic, patients suspected of emerging infectious diseases were
treated in HLIUs, regardless of disease severity. The hospital continuously improved
training and preparedness protocols to reflect the lessons learned.
Community-based response network in collaboration with the provincial government
Finally, SNUBH helped establish a network among other hospitals and governmental agencies
to cope with the massive outbreak (8). SNUBH took on the responsibility of leading
the infection control initiatives in Gyeonggi-do, a densely populated province with
13 million residents surrounding metropolitan Seoul. SNUBH initiated the first provincial
Gyeonggi-do Infectious Disease Control Center (GIDCC) in April 2014, accredited by
the Gyeonggi provincial government and the KCDC. During the Ebola virus epidemic in
West Africa, GIDCC held simulation exercises with multiple stakeholders, based on
a clinical scenario of an Ebola outbreak. These preemptive preparations and drills
helped Gyeonggi-do to respond to MERS-CoV cases during the outbreak in 2015. For example,
the province rapidly created a bed allocation system by disease severity, which was
a new strategy developed during the outbreak to isolate all patients through risk
stratification. In Gyeonggi-do, two hospitals were designated for the treatment of
MERS patients. While coordinating the GIDCC, SNUBH focused on treating patients with
severe clinical presentations of MERS. Meanwhile, a public community hospital took
charge of patients with less severe disease. Through local collaboration, the Gyeonggi
province was able to contain the MERS-CoV cases efficiently in its area.
Since then, SNUBH continued to provide support for infection control in the community.
Infection control education programs were held for staff at long-term care facilities,
school nurses, and infection control nurses at local hospitals. SNUBH worked with
public health authorities and other hospitals in order to reassess and promote provincial
preparedness for infectious disease threats following the MERS outbreak. This long-term
collaboration paved the way for better communication and collaboration among key parties
(hospitals, local governments, and communities) that ultimately allowed a rapid activation
of the regional response system when the current COVID-19 pandemic began (9,10).
COVID-19 Response and Conclusion
Five years after the MERS-CoV outbreak, Korea was hit by the COVID-19 pandemic in
January 2020. Both Korean government and hospitals were better prepared than in 2015
(Figure 1
). Since SNUBH admitted Korea’s first suspected COVID-19 patient on January 7, 2020,
more than a hundred confirmed or suspected COVID-19 cases have been treated in the
hospital. Through the regional triage system, SNUBH primarily provided advanced care
for critically-ill COVID-19 patient while moderately-ill patients were admitted to
the dedicated community hospital. SNUBH also took care of mildly-ill patients who
were admitted at the Gyeonggi Community Treatment Center, a repurposed non-medical
facility, from March 19 to April 29, 2020. By enacting strict isolation and triage
protocols, SNUBH has had no reported cases of nosocomial SARS-CoV-2 transmission and
has not had to halt the care of non-COVID-19 patients. (The timeline of pandemic preparations
and the COVID-19 response in South Korea and SNUBH, along with the distribution of
admitted patients across different levels of service are summarized in the web-only
Supplementary Figure S1 and Table 2
, respectively.)
Figure 1
Pandemic preparedness of Seoul National University Bundang Hospital. * Infectious
diseases control task force consists of an executive board, a clinical management
team (department of infectious diseases, respiratory diseases, emergency medicine,
and pediatrics), an infection control team (infection control physicians and nurses,
and the occupational health office), a clinical support team (department of laboratory,
radiology, pharmacology, and nutrition), a nursing team, and an administrative team.
* HLIU: high-level isolation units.
Figure 1
Table 2
COVID-19 Response of Seoul National University Bundang Hospital: goals, actions, and
outcomes
Table 2
Goals
Actions
Outcomes
Identify, isolate and report early cases
Identification and report
●
SARS-CoV-2 testing at hospital laboratory and commercial laboratories
●
A COVID-19 screening clinic outside of the hospital building and pre-triage zone at
the emergency department entrance
Isolation
●
Activation of high-level isolation units with extensive triage protocol
●
Installation of temporary isolation wards using negative pressure devices
●
Triage to a pre-emptive isolation ward for patients with risk factors
●
2,572 patients visited the COVID-19 screening clinic with 596 (23.2%) tested (as of
June 16)
●
2,698 patients were triaged at the emergency department, with 506 (18.8%) tested and
453 (16.8%) admitted in isolation wards (as of June 16)
●
782 patients were isolated pre-emptively (as of July 10)
Keep the health-care system functioning for pandemic and non-pandemic patients
●
In-hospital triage protocols for hospital entrance, the emergency department, and
COVID-19 screening clinic
●
Policies for patient flow to separate the area for COVID-19 patients and non-COVID-19
patients
●
Establishment of regional triage system for bed allocation based on patients’ medical
needs, including utilization of non-medical facilities (community treatment center,
CTC)
●
133 COVID-19 confirmed or suspected patients treated at the hospital (58 and 75, respectively,
as of July 10)
●
A total of 17 patients required critical care (≥high -flow oxygen therapy) and 7 patients
received mechanical ventilation
●
201 mildly-ill COVID-19 patients managed at the Gyeonggi CTC
●
Most of the elective surgeries and outpatient clinics continued as scheduled
Reduce the risk of pandemic acute respiratory infection transmission associated with
health care
●
Treating COVID-19 patients in negative pressure isolation units
●
Training healthcare workers: (1) regularly scheduled personal protective equipment
training, (2) bi-annual workshops for development of epidemic scenarios and simulation
exercises
●
Establishment of occupational health programmes, including surveillance of healthcare
workers through electronic questionnaire
●
Risk communication: (1) sharing information by emails and intranet on the daily basis,
(2) text messaging when an immediate survey of epidemiological risk factors of hospital
workers was needed, (3) communication with health authorities and other hospitals
coordinated by the infection control office
●
No nosocomial infections, including no healthcare worker infections
Note. Goals at the left column were adapted from “Infection prevention and control
of epidemic-and pandemic-prone acute respiratory infections in health care”, by WHO,
2014.
Since the MERS-CoV outbreak, many academic medical centers in Korea have taken an
active role in not only preparing their facilities and staff, but also their communities
and regional governments, allowing the country as a whole to effectively tackle the
current wave of COVID-19. Although the level of community spread in Korea has been
relatively moderate due to widespread testing, rigorous contact tracing, and mandatory
quarantine, current efforts will be maintained to prepare for potential future outbreaks
of COVID-19. As countries overcome surges and likely face future waves, academic medical
centers around the world can continue to take up a similar mantle of preparation,
innovation, training, critical care, and community leadership.
Transparency declaration
All authors have stated that there are no conflicts of interest to declare. No funding
was received for this study.
Authors’ contributions
JA-RA and K-HS contributed equally to this work. JA-RA, K-HS, ESK, J-HK, AB, and HBK
conceived the study. K-HS, ESK, JJ, JYP, JSP, HL, MJS, HYL, SL, KUP, and HBK collected
data. JA-RA, K-HS, ESK, RK, and J-HK wrote the manuscript. All authors reviewed and
approved the final version for submission.