Abstract
In 2023, as public health and social measures due to coronavirus disease 2019 (COVID-19) eased and overseas travel resumed, measles cases increased rapidly worldwide. According to the World Health Organization (WHO), approximately 320,000 measles cases were reported worldwide in 2023, 1.8 times higher than approximately 170,000 cases in 2022. Even in countries verified as measles-eradication countries, community epidemics have been observed mainly among unvaccinated and incompletely vaccinated people. The WHO indicated that low vaccination rates and increased international travel are the main causes of the rapid increase in measles outbreaks. During the COVID-19 pandemic, vaccination services were suspended or delayed in many countries, significantly decreasing vaccination rates. Simultaneously, as travel restrictions eased, population movement increased worldwide, creating an environment that made it easy for the measles virus to spread to various regions. The WHO has set the goal of eradicating measles by 2030, and important strategies include maintaining and strengthening vaccination rates, strengthening quarantine, patient surveillance, public health education, and information sharing through international cooperation. As of 2022, the Republic of Korea has maintained a relatively high vaccination rate by meeting the standards for maintaining herd immunity of over 95% recommended by the WHO, with a secondary vaccination rate of 95%. However, there is a risk of transmission through certain age groups and overseas inflows where vaccination rates are relatively low. Therefore, in areas with an active measles outbreak, it is essential to be vaccinated before traveling to areas where outbreaks are increasing, and careful monitoring is necessary to prevent domestic inflow.
Keywords: Measles, Overseas importation, Vaccination, World Health Organization
Key messages
① What is known previously?
Measles is a highly contagious disease. In particular, when children and pregnant women with low immunity are infected with measles, there is a high risk of severe illness, and even death.
② What new information is presented?
Measles outbreaks are increasing worldwide due to decreased vaccination rates during the COVID-19 pandemic and increased imports from overseas.
③ What are implications?
Even in countries that have previously been verified to eradicate measles, low vaccination rates and increased population movement can lead to community transmission. Therefore, it is important to be vaccinated before traveling to areas where outbreaks are increasing, and careful monitoring is necessary to prevent domestic inflow.
Introduction
The history of the measles elimination strategy began with the development of the measles vaccine in 1963. In the 1980s and 1990s, the World Health Organization (WHO) identified measles as an important global health issue and intensified vaccination campaigns worldwide. In the 2000s, WHO and the United Nations Children's Fund (UNICEF) set a goal of reducing measles mortality by 50% by 2005 and recommended that each country increase vaccination rates and strengthen surveillance systems through the announcement of the Measles: Mortality Reduction and Regional Elimination: Strategic Plan 2001–2005, further systematizing the strategy for measles eradication [1]. Owing to these efforts, the number of global measles cases decreased significantly from approximately 850,000 cases in 2000 to 350,000 cases in 2018 [2]. However, despite WHO’s efforts to eradicate measles, misinformation about vaccinations continued to spread in 2019, leading many to not vaccinate their children, with the WHO reporting nearly 870,000 cases in the year, the highest number since 1996. This surge led to the declaration of a global measles epidemic [3]. During the subsequent coronavirus disease 2019 (COVID-19) pandemic that began in 2020, various measures such as travel restrictions and social distancing were implemented, resulting in a sharp decrease in the incidence of measles worldwide (Figure 1). As social distancing and quarantine measures were relaxed and international travel resumed in 2023 [4,5], the overall incidence of infectious diseases including influenza, tuberculosis, and whooping cough increased, with an especially sharp increase in measles cases. Recently, the Republic of Korea (ROK) experienced a mass outbreak of measles, with most cases attributed to foreign students in university dormitories (22 cases as of April 15, 2024) [6].
Figure 1. Measles case distribution by month and WHO region (2016–2024).
WHO=World Health Organization. Reused from the report of World Health Organization, 2024 [4].
Measles is a highly contagious disease that can infect more than 90% of immunocompromised individuals who are exposed to the virus. Particularly, when individuals with low immunity, such as children and pregnant women, become infected with measles, the infection severity can worsen, causing pneumonia, encephalitis, and even death. Therefore, it is important to prevent measles effectively by administering two doses of the measles, mumps, and rubella (MMR) vaccine [7]. Additionally, we must be prepared for a global measles epidemic by strengthening the domestic and international surveillance systems and preemptively managing imported cases from other countries.
Therefore, this report examined the status of the recent measles outbreaks outside ROK and the factors associated with the increased incidence. The report also examined the measures and recommendations issued by major organizations as a reference for preparing prevention and management measures for future measles outbreaks in ROK.
Methods
The status of the global measles cases was identified from the “Provisional monthly measles and rubella data,” which is regularly updated every month by the WHO. The aforementioned data include the number of suspected and confirmed cases of measles and rubella worldwide and the vaccination rate in each country [4]. To assess the response measures and recommendations for measles outbreaks and factors associated with the increased incidence of measles, major reports and data published by key organizations, including the WHO, US Centers for Disease Control & Prevention (CDC), and European Centre for Disease Prevention and Control (ECDC), were referenced along with data published by the health ministries of the affected countries.
Results
1. Global Measles Status
According to the WHO, the number of measles cases worldwide in 2023 was 1.8 times higher than that in 2022 (approximately 320,000 vs. 170,000 cases) [4]. The incidence of measles tends to be high in Africa, the Middle East, and Asia, where implementing vaccination drives is difficult due to the vulnerable public health infrastructure [7]. However, even Europe and Western Pacific regions reported an increased incidence in 2023 compared to previous years (Table 1, Figure 1) [4]. In ROK, the number of cases has increased due to imported cases, mostly from Uzbekistan, Thailand, and Kazakhstan.
Table 1. Number of reported measles cases by WHO region (2022–2023) .
| Region | Member states | No. of reported measles casesa) | Year-on-year increase (times) | |
|---|---|---|---|---|
| 2022 | 2023 | |||
| Global | 194 | 171,153 | 321,582 | 1.9 |
| Africa | 47 | 64,922 | 73,381 | 1.1 |
| Americas | 35 | 169 | 42 | 0.2 |
| Middle East | 21 | 54,245 | 90,876 | 1.7 |
| Europe | 53 | 934 | 61,017 | 65.3 |
| Southeast Asia | 11 | 49,492 | 90,968 | 1.8 |
| Western Pacific | 27 | 1,392 | 5,298 | 3.8 |
WHO=World Health Organization. a)Cases reported by each country (if laboratory confirmed, epidemiologically related, or meet clinical criteria). Reused from the report of World Health Organization, 2024 [4].
In Europe, approximately 42,000 cases of measles were reported in 2023, representing a 45-fold increase from 941 cases reported in 2022 [4]. According to the “Measles, Annual Epidemiological Report for 2023” published by the ECDC, measles outbreaks began to increase from July 2023 at a much higher level than that in the previous 3 years and showed a pattern that differed from the typical seasonal pattern of increased incidence reported between late winter and spring [8]. Factors such as changes in vaccination rates and increased population mobility may have contributed to these results [8]. In December 2023, the WHO and European authorities issued a warning regarding the risk of measles transmission via unvaccinated individuals and urged timely vaccinations to protect children and mitigate additional transmission [9]. In the Western Pacific region, approximately 5,000 cases were reported in 2023, mostly in the Philippines and Malaysia, which represented an almost 2.5-fold increase from the combined total of approximately 2,500 cases in the previous 2 years [10]. In Kazakhstan, one of the countries with a high prevalence of measles, 13,677 cases were reported in 2023, with most of the cases involving unvaccinated children. This was the highest number of cases reported in the past decade [11,12].
Even in countries that have been verified to be measles-free, a continued community-acquired epidemic, mostly among unvaccinated and incompletely vaccinated individuals, has been observed. The United Kingdom, which was declared measles-free in 2017, reported 216 cases of measles in the West Midlands region between October 2023 and January 2024 [13], mostly involving community transmission through unvaccinated children. In January 2024, the United Kingdom Health Security Agency declared the situation a national incident, emphasizing the seriousness of measles outbreaks and implementing community- and school-based vaccination drives [14]. The United States, which was declared measles-free in 2000, reported 338 cases of measles between January 2020 and March 2024. Particularly, 97 cases occurred in the first quarter of 2024 alone, representing a more than 17-fold increase from the average number of cases reported during the same period in previous years [15]. It was confirmed that the measles cases that occurred in Chicago in the past 5 years spread from unvaccinated migrants from South America, including Venezuela [16]. In March 2024, the CDC mentioned that the number of measles cases is increasing globally, including in the United States, and they provided guidelines on measles prevention for healthcare workers, state health authorities, parents, and travelers. Moreover, the CDC suggested that countries that have been verified to be measles-free may face the risk of a measles outbreak due to the increase in measles cases worldwide and reduced vaccination rates. They emphasized the need for early detection of cases, timely management and care, and increasing the measles vaccination rate [17].
2. Measles-free Verification Procedures and Status
The measles-free status of each country is assessed by the WHO Regional Verification Commission (RVC). Each country must regularly report information to the WHO RVC, including measles status data and information regarding surveillance systems. The commission reviews the reports submitted by each country to assess not only the measles status comprehensively but also the public health infrastructure, including the availability of an effective surveillance system, laboratory testing capacity, and measles vaccination rate (≥59% second-dose vaccination rate) to determine the measles-free status [18]. As of April 2024, 78 out of 194 WHO member nations (40.2%) have been verified to be measles-free; the region-wise order is as follows: Europe (17.0%), the Americas (15.5%), Western Pacific (3.1%), Southeast Asia (2.6%), the Middle East (2.1%), and Africa (0.0%) (Table 2, Figure 2) [4]. Some countries received verifications as measles-free countries but could not maintain the verification status due to the re-emergence of community transmission. For instance, although Mongolia was verified to be measles-free in 2014, the economic recession in 2016 led to an increased poverty rate, resulting in a lapse in vaccinations and a decreased vaccination rate. Consequently, Mongolia was unable to maintain its measles-free status because transmission continued among unvaccinated individuals aged 8–35 years and children [19]. To manage this situation, the WHO and United Nations Children’s Fund collaborated with the Mongolian government to implement a large-scale additional vaccination campaign, especially targeting young adults aged 18–30 years [20].
Table 2. WHO measles verification of elimination .
| Region | Member states | Measles verification of elimination | |||
|---|---|---|---|---|---|
| Verified | Eliminated | Endemic | Not classified | ||
| Global | 194 | 78 (40.2) | 21 (10.8) | 89 (45.9) | 6 (3.1) |
| Africa | 47 | 0 (0.0) | 0 (0.0) | 47 (24.2) | 0 (0.0) |
| Americas | 35 | 30 (15.5) | 0 (0.0) | 0 (0.0) | 5 (2.6) |
| Middle East | 21 | 4 (2.1) | 0 (0.0) | 17 (8.8) | 0 (0.0) |
| Europe | 53 | 33 (17.0) | 8 (4.1) | 11 (5.7) | 1 (0.5) |
| Southeast Asia | 11 | 5 (2.6) | 0 (0.0) | 6 (3.1) | 0 (0.0) |
| Western Pacific | 27 | 6 (3.1) | 13 (6.7) | 8 (4.1) | 0 (0.0) |
Values are presented as number only or number (%). WHO=World Health Organization. Reused from the report of World Health Organization, 2024 [4].
Figure 2. Measles verification of elimination by country.
Reused from the report of World Health Organization, 2024 [4].
3. Causes of Increased Measles Outbreaks
In its announcement in November 2023, the WHO proclaimed low vaccination rates and increased international travel as the major causes of the sudden increase in measles outbreaks. Particularly, vaccination services were discontinued or delayed in many countries during the COVID-19 pandemic, which significantly decreased the measles vaccination rate. Simultaneously, the relaxation of travel restrictions led to increased population mobility worldwide, which was conducive to the spread of the measles virus to various regions [5].
1) Low vaccination rate
According to the “Progress toward Regional Measles Elimination-Worldwide, 2000–2022” report published by the WHO, the global measles vaccination rate increased from 72% to 86% between 2000 and 2019 but decreased to 81% in 2021 during the COVID-19 pandemic, which was the lowest vaccination rate recorded since 2008. During 2021–2022, suspected measles cases increased by 18%, while the number of countries that experienced mass outbreaks increased from 22 to 37 countries. During 2021–2022, the number of measles-related deaths increased by 94% [21].
Additionally, according to the “threat assessment brief: measles on the rise in the EU/EEA” published by the ECDC in March 2024, 75.5% of the cases reported in 2023 involved unvaccinated individuals. Moreover, the first-dose vaccination rate for measles decreased from 95% in 2018 to 92% in 2022, while the second-dose vaccination rate decreased from 91% in 2018 to 89% in 2022 [8].
The Ministry of Healthcare of Kazakhstan reported that the inability to conduct regular vaccination programs during the COVID-19 pandemic led to a decline in the MMR vaccination rate, resulting in measles outbreaks mostly among unvaccinated children [12]. In response, a vaccination campaign was launched in late 2023 to vaccinate individuals who had not received MMR vaccination. The campaign provided additional vaccinations to over 930,000 unvaccinated individuals between November 2023 and early January 2024. In 2023, the incidence of measles showed an increasing trend in all regions but changed to a downward trend in 2024 [22].
2) Increased international travel and mobility
Since travel restrictions were relaxed despite MMR vaccinations not being implemented during the COVID-19 pandemic, the likelihood of measles being imported increased with increasing international travel worldwide. Measles outbreaks that occurred in countries with high MMR vaccination rates were often identified to involve imported cases from regions with low vaccination rates [15]. Such imported cases can cause additional outbreaks in communities or groups with low vaccination rates [16]. According to the CDC, 96% of all measles cases that occurred in the United States since 2020 were imported cases or related to imported cases, mainly from the Middle East and Africa [15]. In the first quarter of 2024, 6 cases imported from Europe and Southeast Asia were reported, which represented an increase of approximately 50% compared to the average number of cases imported from the same regions during 2020–2023 [15].
4. Recommendations for Strengthening the Measles Response
To strengthen the management of and response to such a global measles epidemic, major organizations, including the WHO, CDC, and ECDC, are emphasizing on certain measures. The first is the early detection of cases by strengthening the surveillance system [17]. It is important to minimize additional transmission by immediately reporting and rapidly responding to cases confirmed in healthcare institutions. Importantly, genotyping using reverse transcriptase polymerase chain reaction can provide important information for tracing the route of viral transmission and infection source, which is important in preparing measures for preventing the onset and spread of measles [17]. The second is maintaining a high vaccination rate. The WHO recommends that a vaccination rate of at least 95% should be maintained to assure herd immunity against measles [18]. Various public health campaigns and educational programs may be implemented to resolve regional immunization disparities and increase vaccination rates. Furthermore, the overall awareness about measles and other vaccine-preventable diseases can be raised through such efforts [21,23]. The third is an emphasis on providing continued education and training regarding the clinical features and transmission methods of measles to enable healthcare providers to diagnose measles accurately, which can exhibit symptoms similar to the common cold in the early stage. Lastly, there is an emphasis on strengthening crisis communications to enhance public awareness [17]. This can minimize public confusion by providing accurate and reliable information regarding infectious diseases. Moreover, public trust can be built by the government demonstrating the transparency, which is important for gaining cooperation from the public when implementing recommendations or policies.
Conclusions
The number of measles cases has increased worldwide. An increasing risk of measles being introduced into and spreading through communities has been observed due to increased international travel and decreased vaccination rates, even in countries that have been verified to be measles-free. The WHO has set goals to eliminate measles by 2030 and has identified maintaining and strengthening vaccination rates, strengthening quarantine measures, patient surveillance, public health education, and information sharing through international collaboration as the key strategies [23]. In ROK, the second-dose vaccination rate for measles was 95% in 2022, maintaining a relatively high vaccination rate that fulfilled the WHO recommendation (maintaining ≥95% vaccination rate for herd immunity) [24]. Starting in December 2023, measles was designated as a quarantinable infectious disease; consequently, the fever surveillance criteria for arrivals from countries with major outbreaks have been strengthened. Furthermore, plans are underway for measles response education and simulation training, and the Ministry of Education and Ministry of Health and Welfare are encouraging measles vaccinations in schools and childcare centers [25].
Overall, ROK has a relatively high vaccination rate and a public health system capable of responding to measles outbreaks. However, based on the domestic and international cases examined, even countries verified to be measles-free are facing the possibility of transmission among specific age groups with relatively low vaccination rates or through imported cases. Therefore, continued promotion of the importance of vaccination through public health campaigns and education programs and increasing accessibility is crucial. Additionally, close monitoring of arrivals from countries with major outbreaks is important to prevent imported cases. Travelers should check in advance for any information about major infectious disease outbreaks and infectious diseases, exert caution in areas that they plan to visit, and get vaccinated to protect themselves. Information regarding infectious disease prevention for each country can be checked on “Imported Infectious Diseases NOW.” Lastly, gaining public cooperation for policies and precautions through effective crisis communication can help minimize public health risks.
Acknowledgments
We thanks Division of Infectious Disease Control, Division of Quarantine Policy, Division of Immunization Planning, Korea Disease Control and Prevention Agency.
Declarations
Ethics Statement: Not applicable.
Funding Source: None.
Conflict of Interest: The authors have no conflicts of interest to declare.
Author Contributions: Conceptualization: JYS, JAL, YWJ, HSY. Data curation: JYS, JHC, JYO, JEY, SWC, YHL. Formal analysis: JYS, JHC, JYO, JEY, SWC, YHL. Methodology: JYS, JAL. Visualization: JYS. Writing – original draft: JYS, JHC. Writing – review & editing: JYS, JAL, YWJ, HSY.
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