We reviewed measles surveillance data from the Georgia national surveillance system. National guidelines for measles surveillance, revised in 2017 (10; Appendix), follow WHO regional recommendations. Healthcare providers report suspected measles cases to district public health centers, which report the cases to the national Electronic Infectious Disease Surveillance System and conduct case investigation and response. The National Center for Disease Control and Public Health (NCDC) is responsible for the national level analysis and provides overall guidance. Case-based data on suspected measles cases are reported electronically each month to EUR. Laboratory testing is conducted by the National Measles and Rubella Laboratory at NCDC or, in rare cases, by private laboratories. Virus characterization is performed at the Regional Reference Laboratory in Luxemburg Institute of Health and at the National Measles and Rubella Laboratory. Measles virus sequences are reported to WHO through the Measles Nucleotide Surveillance (MeaNS) database (11,12).

We reviewed basic epidemiologic data for cases reported during 2013–2018 and conducted a detailed analysis of cases reported during 2013–2014, including descriptive epidemiology, occupational status, patterns of transmission, and costs to the public health system. An analysis of measles transmission across age groups was performed for a subset of cases for which the age group of the source (adult vs. child) could be determined from the Electronic Infectious Disease Surveillance System. We obtained information on expenses associated with outbreak response (costs of vaccine and personnel) from NCDC and population data from Georgia’s National Statistics Agency.

We obtained information on administrative MMR vaccine coverage from NCDC, supplemented by independent estimates from a coverage survey that we conducted in 2015–2016 (13; Appendix). In this survey, we estimated immunization coverage (nationwide and in 3 largest cities [Tbilisi, Batumi, and Kutaisi]) for the first MMR vaccine dose (MMR1) and the second MMR vaccine dose (MMR2) among children age-eligible to receive routine vaccinations in 2014 (2009 and 2013 birth cohorts). We estimated both coverage at the time of the survey and timely coverage by standard ages (MMR1 by age 24 months and MMR2 by age 72 months). We obtained additional information on the state of the immunization program in Georgia from WHO and GAVI (https://www.gavi.org) assessment reports. Additional details on epidemiologic methods are given in the Appendix.

The activities described in this report were determined by CDC to represent nonresearch. Therefore, institutional review board review was not applicable.

Measles epidemiology in Georgia during 2013–2018 shows widespread circulation and genetic diversity of measles viruses and points to persistent gaps in population immunity across a wide age range that have not been sufficiently addressed by interventions undertaken so far (5,9). Measles in Georgia is associated with substantial economic costs, disease, and deaths; its effects extend beyond the acute illness, as suggested by the recently demonstrated high risk for subacute sclerosing panencephalitis after measles outbreaks in Georgia (17).

Cases among children highlight challenges with routine immunization services. Previous suboptimal MMR1 coverage and vaccination delays, primarily because of unwarranted contraindications (13), likely contributed to the high incidence of measles among children. Although most children receive MMR vaccine, vaccination often happens years after the recommended ages, widening the window of susceptibility, particularly among those age-eligible to MMR1 only.

High incidence among adults and <1-year-old infants results from continued susceptibility among persons born in the 1980s and 1990s (Figure 4) and is consistent with the results of a serosurvey conducted in Georgia immediately after the 2013–2015 outbreak (18), which demonstrated residual seronegativity to measles above the 7% susceptibility threshold needed for preventing outbreaks (19) among young adults. Seronegativity was 10.1% among persons 18–24 years of age, including 14.5% among college students and 8.0% among those 24–29 years of age (18). Analysis of measles transmission patterns demonstrated the important role of adults in virus circulation, suggesting that the adult population could potentially maintain measles transmission in Georgia. Along with widespread susceptibility among adults, small birth cohorts and the generally small number of children in households in Georgia (20) could have contributed to this finding.

Our findings highlight the urgent need to address population susceptibility across all age groups in Georgia. To improve immunity among children, ongoing catch-up immunization of unvaccinated and undervaccinated children should be accelerated, along with further strengthening routine immunization services. Educational efforts promoting awareness among parents and healthcare providers should be intensified to address needless delays attributable to unwarranted contraindications. Effective communication and stakeholder coordination will be needed to ensure the successful implementation of legislation endorsing mandatory childhood vaccinations in Georgia (15). Implementing mandatory MMR vaccination of certain occupational groups (16) and expanding this policy to include all college students could considerably reduce measles transmission among adults in high-risk settings, including HCFs, which have been a substantial contributor to outbreaks. However, reaching susceptible persons in the general adult population who account for a large proportion of cases, remains extremely challenging. The unsuccessful measles-rubella SIA conducted in 2008 (9) was a missed opportunity to close historic immunity gaps in Georgia. Conducting large-scale SIAs in Georgia’s present healthcare environment is not feasible because of the lack of defined catchment areas or populations, the voluntary nature of patient registration with HCFs, the lack of mechanisms or motivation for providers to identify and offer vaccinations to unregistered persons, and difficulties in locating historic records to ascertain vaccination status of adults. In addition, acceptance of mass immunizations among healthcare providers and public health professionals has been low since the SIA in 2008 (9). Under these circumstances, more selective and targeted efforts to control measles outbreaks are being implemented. The result of these efforts will depend primarily on the level of public acceptance. The suboptimal uptake of MMR vaccine among adults indicates the need for interventions to generate vaccine demand.

Information provided by the measles surveillance system is critical for guiding outbreak responses and documenting virus transmission. Measles surveillance in Georgia currently meets most performance indicators. Further improving the quality of case and outbreak investigations will help ensure that all chains of transmission are promptly identified and followed up.

Improved molecular surveillance, notwithstanding certain temporal and geographic gaps, helped demonstrate that virus introductions and local evolution likely contributed to continued transmission. At least 2 variants of measles virus (the main outbreak strain [cluster 1] and the strain in cluster 8) have likely established long-term (>12 months) transmission in Georgia during the 2013–2015 outbreak, but their circulation has been interrupted since then. Cluster 9, detected during April 2017–February 2018, possibly represents a new introduction. Given the slow rate of measles virus evolution (21) and a very low level of measles activity in 2016, the 2-nucleotide difference from the Frankfurt-Main strain probably would not have emerged over the 9-month period since its last detection in Georgia. Cluster 9 strains also might have circulated for >12 months, but no virus specimens were collected during March–November 2018 (the peak of the outbreak), preventing definitive conclusion.

Controlling measles outbreaks throughout EUR is crucial for achieving the regional elimination goal. The experience in Georgia demonstrates that without adequate and timely response, substantial susceptibility to measles can persist in settings with historically suboptimal coverage even after large-scale outbreaks, thus leaving room for future outbreaks. A similar pattern was observed in Ukraine and in Bosnia and Herzegovina, where, in the absence of appropriate response, the historically underimmunized birth cohorts were affected by repeated outbreaks of measles (22–27). In contrast, those countries in the former Soviet Union and Eastern Europe that successfully implemented wide-age SIAs, achieved elimination or substantial reduction of measles incidence for prolonged periods (4,28,29). However, implementing traditional SIAs is not feasible in many middle- and high-income countries of EUR. Lessons learned from Georgia could be useful for other countries with immunization systems facing similar challenges related to health-system transitions and the presence of age cohorts or population groups with historically low coverage.