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Elimination of Measles --- South Korea, 2001--2006

Before the introduction of measles-containing vaccine (MCV), measles was endemic in South Korea. MCV became available in South Korea in 1965, and measles, mumps, and rubella (MMR) vaccine was added to the country's national immunization program in 1983, with 1 dose administered at age 9--15 months. In 1997, a second dose of MCV (MCV2) was added to the schedule; recommended ages for administration of MCV1 and MCV2 were 12--15 months and 4--6 years, respectively. However, with insufficient policies and programs in place to promote 2-dose coverage, this 1997 recommendation achieved limited coverage with 2 doses of MCV. In a 2000 seroepidemiologic study among children aged 7--9 years who had been eligible for vaccination since 1997, only 39% had received MCV2 (Korea Centers for Disease Control and Prevention [KCDC], unpublished data, 2001). During 2000--2001, South Korea experienced a measles epidemic that affected tens of thousands of children. In response, in 2001, South Korea announced a 5-year National Measles Elimination Plan. This report describes the activities and summarizes the results of that plan, which enabled South Korea to announce in late 2006 that interruption of indigenous measles transmission had been achieved, making South Korea the first country in the World Health Organization's (WHO) Western Pacific Region declare measles eliminated.

The January 2000--July 2001 measles epidemic in South Korea resulted in approximately 55,000 reported cases (118 cases per 100,000 population) of measles and seven deaths. Most cases occurred among children aged <2 years and 7--15 years. Among patients aged <2 years, approximately 86% had not received measles vaccination; among patients aged 7--15 years, approximately 80% had received 1 dose of MCV. Fifteen measles virus strains were isolated and identified as genotype H1 (1).

National Measles Elimination Plan

Recognizing that indigenous measles virus circulation and periodic epidemics would continue without a more intensified approach, South Korea established a goal to eliminate measles by 2005. In 2001, a National Committee for Measles Elimination was formed to determine appropriate strategies, provide recommendations, and monitor progress. The committee included representatives from the Korean Ministry of Health & Welfare, KCDC, the Korean Ministry of Education Welfare, the Korea Advisory Committee on Immunization Practice, the Korea Medical Association, the Korean Society of Pediatrics, and the Parents Association of True Education. Representatives of WHO's Western Pacific Regional Office (WPRO), and CDC served as advisors to the committee. Key elimination strategies developed by this group were 1) maintaining 2-dose measles vaccination coverage of >95% by requiring completion of MCV2 for school entry by children aged 7 years, 2) conducting a measles vaccination catch-up campaign among children aged 8--16 years, and 3) strengthening case-based surveillance with laboratory confirmation of reported cases.

School entry. A new school-entry requirement was implemented in March 2001, resulting in 99% of children aged 7 years entering primary school with documentation of MCV2. This was the first time vaccinations were required for school entry in South Korea. Children without documented history of MCV2 were not refused admission but were directed to private clinics or public health centers where they were encouraged to receive vaccination. During the next 4 years, MCV2 coverage ranged from 95.0% to 99.9% among children aged 7 years entering school (2).

Catch-up campaign. During May 21--July 14, 2001, a nationwide measles-rubella (MR) vaccination catch-up campaign was conducted, targeting youths aged 8--16 years who did not have documented evidence of receiving MCV2. The target age range was based on the epidemiology of the 2000--2001 measles epidemic (Figure 1) and on results from a 2000 population-based seroepidemiologic survey using enzyme linked immunosorbent assay (ELISA) to detect anti-measles immunoglobulin G (IgG) antibody* among 18,139 youths aged 7--18 years (Figure 2). The survey indicated that, by specific age, 5.3% (children aged 17 years) to 15.4% (children aged 10 years) of youths in the target age range lacked immunity to measles (KCDC, unpublished data, 2001). MR vaccine was selected for the campaign on the basis of results of a cost-benefit analysis (JK Lee, Seoul National University, Korea, unpublished data, 2003).

Information regarding the measles campaign and possible adverse events following immunization (AEFI) were publicized through the media and through school officials beginning 40 days before the campaign. Safe-injection and waste-management guidelines were distributed to vaccination teams before the campaign. AEFIs were monitored through passive surveillance in public health centers, private clinics, hospitals, and a toll-free telephone emergency call service. Vaccination teams, including a physician and two or three nurses, visited nearly every school in South Korea.

Among the 5.8 million youths in the target population, approximately 4.8 million (83%) were administered MR vaccine, 833,000 (14%) had immunization records with previously documented MCV2, 132,000 (2.3%) deferred vaccination to a later date, and 22,849 (0.4%) were not vaccinated because of contraindications. At the conclusion of the campaign, 97% of the target population had received MCV2, either before or during the campaign; coverage was high in all 16 provinces.

Enhanced surveillance. Before the 2000--2001 epidemic, the goal of measles surveillance in South Korea was to detect outbreaks; after the catch-up plan was implemented in 2001, the goal of surveillance became to monitor and confirm elimination of indigenous measles virus transmission in the country. To increase measles surveillance sensitivity, in July 2001, officers from the Division of Epidemic Intelligence Service of the KCDC began investigating suspected measles cases and collecting clinical specimens. A network of public- and private-sector laboratories was established at the national and provincial levels to confirm suspected cases serologically by ELISA for anti-measles immunoglobulin M (IgM) antibody and to conduct molecular diagnostics and genotyping on viral isolates (3). By 2006, among 126 reported measles cases (i.e., cases with rash and fever and either cough, coryza, or conjunctivitis), 107 (84.9%) were investigated within 48 hours of report, and adequate serologic specimens were collected from 117 (92.8%). Laboratory results from all 117 cases with adequate specimens (100%) were available within 7 days. Measles virus was isolated from one identified chain of measles transmission involving 15 cases but not from sporadic confirmed cases.

Effects of Measles Elimination Activities

Before implementation of the National Measles Elimination Plan, South Korea experienced multiple measles epidemics. Before the 2000--2001 epidemic, measles epidemics occurred during 1993--1994 and in 1990 (Table). The annual number of measles cases from 1990 to 2000 ranged from two in 1997 to 32,647 in 2000.

During 2002--2006, after implementation of the national plan, the number of annual confirmed measles cases ranged from six to 25, with corresponding annual incidence ranging from 0.13 to 0.52 cases per million (KCDC, unpublished data, 2007). One confirmed measles case in 2002 was imported, as were two cases in 2003, one in 2005, and five in 2006. The annual number of reported measles cases that were not serologically confirmed (an indicator of measles surveillance sensitivity with a target incidence of at least one case per 100,000 population in 80% of districts) ranged from 45 to 132, with corresponding annual incidence ranging from 0.09 to 0.28 cases per 100,000 population.

During 2002--2006, South Korea satisfied nearly all interim criteria for measles elimination as established by WHO/WPRO. Those criteria include 1) less than one confirmed measles case reported per million population per year (excluding imported cases); 2) case-based surveillance with comprehensive reporting and investigation of all cases and chains of transmission; 3) maintaining 95% immunity to measles in each cohort in every district, as demonstrated by at least 95% coverage with 2 doses of MCV; and 4) importations leading to only small outbreaks (4). In South Korea, reported measles incidence has been less than one confirmed case per million population since 2002. Adequate serologic specimens have been collected from >80% of reported suspected cases since 2005. National coverage with 2 doses of MCV among children aged 7 years has been >95% since 2002. Additional evidence of high levels of protection against measles includes results from a 2004 seroepidemiologic study among school children. Among 7,131 youths aged 7--16 years, 6,583 (92.3%; 95% confidence interval [CI] = 91.7--92.9) had protective anti-measles IgG antibody titers of >150 MIU/mL (5), an increase from the 2000 seroepidemiologic study, in which 8,339 (87.9%; CI = 87.2--88.6) of 9,501 youths in the same age group had protective measles IgG antibody titers. Finally, the largest measles outbreak since the 2001 campaign, reported in 2006, consisted of 15 confirmed cases among children aged 1--5 years and was caused by measles virus genotype H1 (6).

On November 7, 2006, the National Committee for Measles Elimination invited international measles authorities from WHO/WPRO, UNICEF, CDC, Japan National Institute of Infectious Diseases, and the International Vaccine Institute to meet in South Korea to review the evidence for elimination of indigenous measles transmission in accordance with WHO/WPRO guidelines. Members of the group concluded that measles elimination had been achieved in South Korea.

Reported by: J-K Lee, MD, H-W Cho, PhD, D-K Oh, MD, Korea Centers for Disease Control and Prevention, South Korea. Western Pacific Regional Office, Manila, Philippines; Vaccines and Biologicals Dept, World Health Organization, Geneva, Switzerland. Global Immunization Div, National Center for Immunization and Respiratory Diseases, CDC.

Editorial Note:

South Korea has rapidly interrupted indigenous transmission of endemic measles virus, thereby achieving measles elimination, by using WHO/WPRO's recommended strategies of appropriately targeted supplementary immunization activities (SIAs), high routine coverage with 2 doses of MCV, and case-based measles surveillance. In 2001, in the midst of an epidemic that resulted in approximately 55,000 cases of measles, South Korea established measles vaccination as a requirement for school entry for children aged 7 years, while simultaneously conducting a measles vaccination catch-up campaign among children in a wide age range. Usually, a catch-up measles elimination campaign also includes a younger population. However, implementing a school-entry requirement in a setting where school enrollment is >95% ensured high routine MCV2 vaccination coverage.

The effect of school-entry requirements on achieving measles elimination has been demonstrated previously in the United States, where several states required a single dose of measles vaccine before school entry as early as the 1960s. In the 1970s and 1980s, more states adopted and strictly enforced such school entry requirements (7). A 2-dose MCV requirement was phased in beginning in 1989. By the fall of 2001, 96% of states required 2 doses of MCV before entering primary school, and median MCV2 coverage of students entering primary school among 38 states surveyed was 97% (range: 57%--99%) (8).

Despite apparent success in interrupting indigenous measles virus transmission in South Korea, the overall number of measles cases might be underreported because many parents seek health care for their children from the private sector, which might not adhere to case definitions and reporting requirements. The finding of a measles virus genotype H1 isolate in the recent chain of measles transmission is difficult to interpret. Genotype H1 had been indigenous to South Korea before implementation of the catch-up campaign in 2001. More recently, this genotype was detected in Japan and Vietnam and in measles imported to the Americas and Europe. Multiple lineages of genotype H1 also continue to circulate in China (9). Health officials in countries where measles is considered to be eliminated must remain vigilant through sensitive and timely case-based surveillance to potential recurrences of measles virus transmission.

The experience in South Korea demonstrated that introduction of a 2-dose measles vaccination schedule in 1997 without school-entry requirements was insufficient to prevent the 2000--2001 epidemic because of low MCV2 coverage. To eliminate indigenous measles virus circulation in the presence of repeated importations, high population immunity was ensured through 1) simultaneous implementation of a catch-up vaccination campaign targeting a wide age range and requirements that students have documentation of MCV2 before school entry and 2) enhanced case-based measles surveillance. Maintaining elimination will require sustaining 2-dose measles vaccination coverage >95% and maintaining sensitive case-based surveillance to identify whether and when preventive SIAs or other interventions might be required.

Acknowledgments

This report is based, in part, on technical assistance from WA Orenstein, MD, Emory University, Atlanta, Georgia; Y Baoping, MD, Western Pacific Regional Office, World Health Organization, Manila, Philippines; J McFarland, MD, UNICEF, New York, New York; and M Papania, MD, Office of the Chief Science Officer, CDC.

References

  1. Korean Ministry of Health and Welfare and National Institute of Health. First year evaluation of the 5-year measles elimination program in Korea, and challenges and opportunities to eliminate measles in the Western Pacific Region. Seoul, South Korea: Korean Ministry of Health and Welfare and National Institute of Health; 2001.
  2. World Health Organization. WHO vaccine-preventable disease: monitoring system. 2006 global summary. Geneva, Switzerland: World Health Organization; 2006. Available at http://www.who.int/vaccines-documents/globalsummary/globalsummary.pdf.
  3. World Health Organization. Global measles and rubella laboratory network---update. Wkly Epidemiol Rec 2005;80:384--8.
  4. World Health Organization, Western Pacific Regional Office. Field guidelines for measles elimination. Manila, Philippines: World Health Organization; 2004. Available at http://www.wpro.who.int/publications.
  5. Korea Centers for Disease Control and Prevention. The 5th year evaluation of the measles elimination program: the strategy for measles elimination and hepatitis B control. Seoul, South Korea: Korea Centers for Disease Control and Prevention; 2006.
  6. Na BK, Shin JM, Lee JY, et al. Genetic and antigenic characterization of measles viruses that circulated in Korea during the 2000--2001 epidemic. J Med Virol 2003;70:649--54.
  7. Orenstein WA, Hinman AR. The immunization system in the United States---role of school immunization laws. Vaccine 1999;17(Suppl 3):S19--24.
  8. Kolasa MS, Klemperer-Johnson S, Papania MJ. Progress toward implementation of a second-dose measles immunization requirement for all schoolchildren in the United States. J Infect Dis 2004;189(Suppl 1):S98--103.
  9. Zhang Y, Zhu Z, Rota PA, et al. Molecular epidemiology of measles viruses in China, 1995--2003. Virol J 2007;4:14.

* Presence of IgG antibody might result from either vaccination or natural infection.

Figure 1

Figure 1
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Figure 2

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Table

Table 3
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