Measles Outbreak and Response Among International Students in Gyeongsangbuk-do Area (Gyeongsan-si) in 2024

Abstract

This report describes a large-scale measles outbreak that occurred in a university dormitory in Gyeongsan-si, Gyeongsangbuk-do, between April 6 and May 10, 2024. We analyzed the characteristics of confirmed patients, the outbreak pattern, and the central and local governments’ responses. The outbreak, which was originated in a dormitory housing international students, resulted in 22 measles cases from April 6 to May 10. The first case was confirmed on April 6 after arriving from abroad on March 20. The patients exhibited one or more symptoms of cough, coryza, or conjunctivitis. The key response strategies emphasized rapid containment to halt transmission, including cohort isolation within the dormitory and monitoring of symptomatic individuals. Communication challenges within the international students hindered verification of MMR (measles-mumps-rubella) vaccination history, underscoring the need for simultaneous assessment of susceptibility and vaccination to promote antibody formation and minimize transmission. Measures, such as verifying vaccination records upon entry and implementing post-arrival vaccination programs, are necessary to prevent future measles outbreaks among international students. Additionally, educating international students about infectious disease awareness and prevention measures is essential to enable swift responses to outbreaks.

Key messages

① What is known previously?

After the coronavirus disease 2019 pandemic, increased international exchanges have led to a rise in cases of foreign-imported patients, including in countries like the Republic of Korea, known for effectively controlling measles. Consequently, the likelihood of transmission within local communities has escalated.

② What new information is presented?

In this measles response, the key focus was early containment to stop rapid transmission, highlighting the importance of isolating contacts and monitoring symptomatic individuals. In cases where verifying vaccination history is linguistically challenging, promoting antibody testing alongside vaccination is crucial to facilitate antibody formation, thus minimizing transmission.

③ What are implications?

International students and others required to engage in communal living should undergo a procedure to verify their vaccination history upon entry, including for measles and other diseases. In addition, educational programs on disease awareness and preventive measures are necessary. Furthermore, preparing MMR (measles-mumps-rubella) vaccines and diagnostic testing resources on a regional basis is essential to prepare for potential outbreaks.

Introduction

Measles is an acute viral infection caused by the measles virus. It manifests as a high fever and a maculopapular rash, as well as a cough, coryza, and conjunctivitis (the 3C). Although the introduction of vaccination has significantly reduced the number of measles cases, during the coronavirus disease 2019 (COVID-19) pandemic, outbreaks developed in Southeast Asia, the Middle East, and Africa, regions with large numbers of infants and young children who remain unvaccinated or have delayed vaccination. In 2023, there were more than 320,000 measles cases worldwide (1.9 times the number in 2022), with a year-over-year increase in cases in Europe, the Americas, the Western Pacific, and the Middle East during the first 3 months of 2024 (January–March). There has also been an increase in the number of imported measles cases from measles-free countries and the potential for community transmission in unvaccinated and incompletely vaccinated individuals [1].

The number of measles cases in the Republic of Korea (ROK) has decreased sharply since the country was declared measles-free by the World Health Organization (WHO) in 2014, with the number being below 20 per year: 7 cases in 2015, 18 cases in 2016, 7 cases in 2017, and 15 cases in 2018. However, with the recent global measles epidemic, ROK, a measles-free country, has been reporting a steady stream of measles cases owing to imported cases. Nine measles outbreaks related to imported cases have been reported in the ROK, starting in Daegu in December 2018 and continuing through May 2019 [2-4].

This report aims to analyze the characteristics of the measles outbreak that occurred between April 6 and May 10, 2024, in a university dormitory in Gyeongsan-si, Gyeongsangbuk-do, ROK, the first major measles outbreak in the country since May 2019, and summarize the epidemic patterns and central and local government responses. The case incidence statistics presented in this report are preliminary and will be finalized by the National Vaccination Committee (Table 1).

Table 1. Current global measles incidences.

Region	Confirmed casea)		Rate (compared with previous year cases)	Confirmed casesa) (Jan–Mar)b)		Rate (compared with previous year cases)
	2022	2023		2023	2024
Global	171,153	321,582	1.9	99,377	94,438	1.0
Africa	64,922	73,381	1.1	26,426	11,145	0.4
America	169	42	0.2	3	120	40.0
Middle east	54,245	90,876	1.7	23,166	29,405	1.3
Europe	934	61,017	65.3	3,140	42,767	13.6
East Asia	49,492	90,968	1.8	46,131	10,040	0.2
West Pacific	1,391	5,298	3.8	511	961	1.9

Unit: personal. ^a)Based on each country reported data (coincided with experimental confirmed, or epidemiological related or clinical diagnostic criteria as measles case). ^b)There might be delayed cases, from January to March, 2024.

Investigation and Results

Even in the ROK, which is a measles-free country, there have been steady reports of measles cases owing to imported cases. There have been no large measles outbreaks in the country since May 2019, with six individual cases reported in 2020 and none in 2021 and 2022, when international travel was restricted because of the COVID-19 pandemic. In 2023, eight measles cases (imported) were reported, followed by 17 in 2024 (imported and import-associated) until this outbreak, a significant increase compared with the number in the previous years.

1. Outbreak Status

This measles outbreak was a cluster case that occurred in a dormitory for international students at a university. The affected individual in the first case developed symptoms including a fever on April 1, which was the 12th day after arriving from Uzbekistan on March 20, 2024. The individual visited a hospital on April 5, the 17th day after arrival, owing to worsening conjunctivitis and was classified as a suspected measles case because of worsening facial rash in the afternoon. Measles was confirmed on April 6, after testing. On April 15, 9 days after the index case was confirmed, four symptomatic cases were identified and confirmed positive by polymerase chain reaction (PCR) test, indicating an outbreak. From April 16 to April 30, 33 symptomatic cases were identified. The symptomatic individuals were tested through temporary vaccination screening and active surveillance, and 17 of them were confirmed to be positive for measles, bringing the total number of cases to 22 from April 6 to May 10, 2024. The dormitory was an all-international student dormitory with a total of 417 students (111, 103, 85, and 118 students resided on the first, second, third, and fourth floors, respectively). By May 10, 2024, 21 days into the surveillance period after the last case, the outbreak was confirmed to be confined to the dormitory with no community transmission. The index patient attended face-to-face classes twice (on March 25 and 28) after entrance.

However, during the infectious period (4 days before the rash developed on April 4), the index patient attended only non-contact classes and had no outside activities except moving from classroom and dormitory, because there was no social contact at that time.

Therefore, the transmission path was assumed to be within the dormitory, which was a communal living area. On April 6, the day the index case was confirmed, the mother of the index patient was also confirmed to have measles in her country. As a result of genotyping all cases including the index case, 19 cases including the index case were found to share the same genotype (B3) as the index case, except for three that were not genotyped owing to high cycle threshold (CT) values and low viral loads. Furthermore, from the infectious period of the index case, which was from March 31, 4 days before developing rash, the incubation period ranged from a minimum of 12 days to a maximum of 19 days, and from April 5, the last exposure date before isolation, the incubation period ranged from a minimum of 7 days to a maximum of 14 days, all of which were within the maximum incubation period of 21 days for measles, confirming secondary transmission from the index case (Figure 1).

Figure 1. Measles outbreak epidemic curve of international students' dormitory in the university, Gyeongsan (2024 April).

1) General characteristics

The 22 measles cases were all recorded in foreign nationals, 21 males and 1 female. The age distribution was as follows: 18 years, 5 cases; 19 years, 9 cases; 20 years, 3 cases; 21 years, 2 cases; 22 years, 2 cases; and 23 years, 1 case. All of them were international first-year students who entered the university in March and lived in the dormitory. There were 12 students from the Korean language program and 10 students from general majors (five from the A Department, four from the B Department, and one from the C Department). In terms of nationality, 16 students were from Uzbekistan, 5 from Kyrgyzstan, and 1 from Vietnam. Among the 155 contacts of the confirmed cases, 51 (32.9%) were confirmed positive in antibody testing (Immunoglobulin G [IgG]).

2) Clinical symptoms

The index patient was hospitalized and treated for fever, conjunctivitis, and rash. However, the symptoms did not improve after the isolation period (4 days after the rash) ended. Therefore, the attending physician extended the isolation treatment before discharging the patients. Subsequently, 21 secondary carriers were isolated in separate quarantine areas of the dormitory with fever and rash; however, the symptoms were mostly mild. The most common symptoms caused by measles included rash (100.0%) and fever (81.8%), and the patients also had at least one of the 3C symptoms (cough, coryza, and conjunctivitis). They also complained of other symptoms such as headaches, sore throat, muscle aches, and fatigue. Most rashes started on the face and neck (15 cases, 68.2%), followed by the trunk (6 cases, 27.3%) and the arms and legs (one case, 4.5%) (Figure 2).

Figure 2. The status of symptoms among confirmed measles patients (22 peoples).

^a)Etc: Headache 4, body ache 1. ^b)Duplicate entries are included.

Public Health Response

1. Individual Case Response for the Index Case (April 6–April 14)

Individual-case epidemiological and contact investigations were conducted as the index case was reported on April 5 and confirmed on April 6 after the patient arrived from a foreign country. According to the measles response guidelines, a contact is anyone who has had face-to-face contact and shared the same indoor space during the infectious period (4 days before developing a rash to 4 days after), regardless of the duration of contact. Moreover, contact management and postexposure prophylaxis should include symptom monitoring for susceptible individuals until 21 days after the last exposure, depending on susceptibility. Susceptible individuals (those without antibodies to the measles virus) should be vaccinated and monitored for symptoms until 21 days after their last exposure. On April 6, after the index case was confirmed, five international students classified as close contacts with no objective vaccination history confirmed underwent antibody (IgG) testing. In addition, three individuals who tested negative and one patient who was classified as an undetermined case were vaccinated 72 hours after exposure to prevent future measles [4]. There were a total of 180 contacts, including five close-contact friends and 103 dormitory residents (foreign nationals with unknown vaccination history), 16 healthcare providers (all vaccinated individuals and with a history of measles), and 56 healthcare visitors (6 fully vaccinated, 42 born before 1968, and 8 unknown status), who were advised to be isolated and monitored by passive surveillance for 21 days (until April 27) from the date of last contact.

2. Outbreak Response (April 15–May 10)

This measles outbreak was a cluster of cases in an international student dormitory at a university; the response to the outbreak is summarized below. In the context of many mild cases with mild symptoms, where initial controls such as isolation management in the dormitory were not adequately implemented and there was low compliance by foreign nationals, the 2024 Measles Response Guidelines recommended home isolation for susceptible contacts, which could lead to problems with spontaneous escapes. Therefore, the Korea Disease Control and Prevention Agency (KDCA) quickly changed the guidelines to allow for mandatory isolation of susceptible individuals based on field judgment. Second, since the cases were of foreign nationals, it was difficult to obtain objective data to verify immunization history other than verbal statements. According to the guidelines, immunity was assumed to be unknown. Since there has not been a large-scale measles outbreak in the ROK since May 2019, there was a lack of antibody (IgG) test kits for measles susceptibility in local public health centers; therefore, the test kits were provided by the KDCA. Most of the contacts of the cases were in their early 20s, and 32.9% of them tested positive in antibody (IgG) testing. This finding was consistent with that of a 2017 study of measles seroprevalence according to age in the Caribbean Netherlands, where the lowest seroprevalence was found among those aged 21 to 24 years [5]. Since it was possible to isolate the cohort in the dormitory, the decision was made to vaccinate all contacts in the dormitory at once, rather than first testing for susceptibility through antibody testing. Furthermore, at the same time, temporary vaccinations were administered to contacts outside the dormitory and in the same department. Third, through rapid consultation with the university, face-to-face classes were switched to non-face-to-face (online) classes, and isolation measures in the dormitory were strengthened (e.g., an agreement was reached with the school to provide food and other necessities). Fourth, during the monitoring of symptomatic cases who had been isolated as contacts, additional cases continued to emerge owing to the reporting of symptoms through active surveillance and identification of fever and rash during vaccination appointments (starting on April 17). On April 18, the Gyeongsangbuk-do Regional Center for Disease Control and Prevention and Gyeongsangbuk-do epidemiological investigators conducted room-by-room resident and symptom checks (for fever and rash) in the dormitory and identified 10 symptomatic cases, of which six were confirmed. No additional cases occurred in the dormitory during the surveillance period (until May 10). From April 18, self-checklists for measles symptoms translated into different languages were distributed according to the residents’ country of origin, and face-to-face monitoring of symptomatic cases by room was conducted twice a day during the surveillance period. In addition, to prevent the spread of the disease in the community, 943 foreign nationals at the university (394 in dormitories, 320 out of dormitories, and 229 non-contact international students) were temporarily vaccinated, and local residents, daycare centers, kindergartens, and healthcare workers were encouraged to receive the MMR (measles-mumps-rubella) vaccine. Monitoring of the 22 cases in this cluster, with a total of 1,490 contacts (417 in the dormitory, 494 outside the dormitory, and 579 in the community), ended on May 10 (Table 2). Finally, the guidelines recommend 21 days from the date of last exposure for terminating the contact cohort isolation. However, given the high level of site compliance among international students who were studying and working, they were released from isolation 14 days after vaccination and monitored for symptoms through active surveillance (twice daily) by health center staff for a week afterward to prevent measles transmission in the community.

Table 2. Status of university enrolled students and measles antibody testing/results .

Classification	Total	Testee	Antibody test result
			+	+/–	–
Total	1,490	156	51	19	86
Dorm-in
Sub-total	417	139	44	14	81
1st	111	8	2	-	6
2nd	103	97	27	13	58
3rd	85	24	11	-	13
4th	118	10	4	2	4
Dorm-out
Sub-total	494	16	7	4	5
Domestic	141	-	-	-	-
Foreign	353	16	7	4	5
Regional community
Sub-total	579	-	-	-	-
Domestic	165	-	-	-	-
Foreign	414	-	-	-	-

Unit: personal. Dorm=dormitory.

Discussion

In this report, the measles outbreak among international students in an international student dormitory at a university was analyzed and the response status was summarized. The outbreak occurred after the index patient, an international student, arrived in the country and lived in a dormitory, and contacts who were exposed to the said individual during the infectious period became infected with the measles virus. Since the genotype B3 is considered imported and import-associated, supporting the importation of the index patient as the source of infection, with the three undetected cases owing to an insufficient viral load having a clear source of infection, the 22 patients identified in this outbreak were categorized as imported or import-associated cases. The Gyeongsangbuk-do Regional Center for Disease Control, Gyeongsangbuk-do, Gyeongsan-si, and the KDCA have been conducting daily situation check meetings since the measles epidemic was recognized and have responded by providing rapid support for testing and vaccination; strengthening surveillance to prevent measles and block its spread; conducting thorough epidemiological investigations and implementing a rapid response; and strengthening prevention, publicity, and cooperation with the university to prevent the spread of measles in the university dormitory and transmission to the community at an early stage, among other things. While there have been cases of measles outbreaks in the ROK, this outbreak among international students was an issue that the ROK lacked experience dealing with. In addition, owing to the limitations such as those pertaining to time and language of communication to respond according to the guidelines, as outlined in the WHO Measles Outbreak Guide (requiring pragmatic decision-making on site when it is difficult to ascertain individual contact histories in an organization with large numbers of contacts) [6], there were a number of cases where pragmatic decisions were made on site through risk assessments and daily situational review meetings by professionals such as healthcare providers, specialists, and epidemiologists to improve on-site compliance rather than being bound by the guidelines. Because the measles outbreak occurred in an international dormitory at a university, the university's active cooperation in preventing the spread of measles, including active interpretation support and adjustment of the school schedule in consideration of communication difficulties, quarantine measures until antibody formation through temporary vaccination (providing basic necessities during the quarantine period because there are taboo foods (such as pork) in Islam), and the provision of an on-site response office, contributed to the early stabilization of the measles outbreak.

The problem with this measles outbreak was that international students (language school students) were not insured prior to the issuance of their Alien Registration Card and therefore had difficulty detecting the disease early by visiting a medical institution, because they often took over-the-counter medicines or medicines brought from home or ignored mild symptoms rather than visiting a hospital. Furthermore, as the symptoms of the index patient did not improve even after the end of the infectious period (+4 days from the date of onset), the attending physician extended the isolation treatment. The initial investigation identified the date of rash development. However, a further in-depth epidemiologic investigation led to the revision of the date of rash development in the index patient from April 2 to April 4, which could have resulted in the patient being not in quarantine during the contagious period. Therefore, it was critical to identify the correct date of rash development during the initial investigation.

Because of high immunization rates in the ROK, measles is usually mild in the country, and there have been no reported deaths from measles since 2001 [7]. However, measles is a global epidemic, and outbreaks can occur at any time due to increased international exchange and the cumulative increase in measles susceptibility in the ROK. It is highly contagious through airborne transmission and can easily spread among high-risk groups, mainly infants under the age of 1 year and healthcare providers, causing social unrest. In this report, a low seroprevalence was identified in the antibody testing of foreign nationals in their early 20s. Therefore, it is important to prevent the development of an individual case into an epidemic early, which requires an active and proactive response, including risk assessment and contact range identification, considering infants younger than 1 year of age, healthcare provider involvement, and the range of susceptible individuals. In addition, once an outbreak has been recognized, consideration should be given to the implementation of temporary vaccinations based on risk. ROK is a measles-free country, and measles, an infectious disease, must be managed to ensure that Korean society remains safe from it. Since a rash is the most important symptom to suspect measles, any symptomatic case with a rash or a patient with a rash who visits a healthcare provider during quarantine should be suspected of measles if they have a history of international travel. Therefore, awareness of measles monitoring in routine quarantine and in healthcare organizations will be important. While measles is a highly contagious disease, it is also a disease whose epidemic can be contained if immunization rates remain above 95% [8], suggesting that immunization is an effective way to prevent measles.

Funding Statement

Funding Source: None.