Progress Toward Measles Elimination — European Region, 2009–2018

Immunization Activities

Since 2002, all 53 countries in EUR have included 2 MCV doses in routine childhood vaccination schedules. WHO and the United Nations Children’s Fund (UNICEF) estimate vaccination coverage for all countries in the region using annual, government-reported administrative coverage data (calculated as the number of doses administered divided by the estimated target population) and vaccination coverage surveys (5). During 2009–2017, annual estimates of MCV1 coverage were available for all 53 countries, and the number of countries with annual MCV2 coverage estimates increased from 47 (89%) to 52 (98%). During 2009–2017, regional coverage estimates for MCV1 and MCV2 ranged from 93% to 95% and 73% to 90%, respectively (Figure). In 2017, 30 (57%) countries achieved ≥95% MCV1 coverage, and 15 (28%) had ≥95% estimated coverage with both doses (Table 1). During 2009–2017, >16 million persons were vaccinated in 21 SIAs conducted in 13 countries (Supplementary Table, https://stacks.cdc.gov/view/cdc/77666). Reported administrative vaccination coverage was ≥95% in nine (43%) SIAs, and the weighted average SIA coverage was 88%; no post-SIA coverage surveys were reported.

Surveillance Activities

Measles surveillance data are reported monthly to WHO from all EUR countries either directly or via the European Centre for Disease Prevention and Control.^† As of 2018, 47 (89%) countries report case-based measles surveillance data; six (11%)^§ report aggregate data. Suspected measles cases are investigated and classified as laboratory-confirmed, epidemiologically linked (to a laboratory-confirmed case), clinically compatible, or discarded (a suspected case that does not meet the clinical or laboratory definition) (6). The WHO European Measles and Rubella Laboratory Network provides laboratory confirmation and genotyping of measles virus isolates from patients with reported cases (7). Key measles case-based surveillance performance indicators include 1) the number of suspected cases discarded as nonmeasles or nonrubella (target: ≥2 per 100,000 population); 2) the percentage of case investigations conducted within 48 hours of report (target: ≥80%); 3) the percentage of suspected cases (excluding those that are epidemiologically linked) with an adequate specimen collected within 28 days of rash onset and tested in a WHO-accredited or proficient laboratory (target: ≥80%); and 4) the percentage of cases for which the origin of infection (i.e., the source of the virus) is determined (target: ≥80%). During 2009–2018, the number of EUR countries that met the target for suspected cases discarded as nonmeasles at the national level increased from one (3%) in 2009 to 10 (21%) in 2018 (Table 2). From 2009 to 2018, the number of countries achieving the targets for timely investigations of suspected cases and adequate specimen collection increased from one (3%) to 24 (51%) and from 13 (36%) to 38 (81%), respectively.

Measles Incidence and Genotypes

During 2009–2018, annual regional measles incidence varied from 8.8 per 1 million population (7,884 cases) in 2009 to an average of 30.1 (average 28,021 cases) during 2010–2015. Incidence declined to a low of 5.8 (5,273 cases) in 2016, before increasing approximately fourteenfold to a high of 89.5 (82,596 cases) in 2018 (Table 1) (Figure). These 82,596 cases were reported from 47 (89%) EUR countries; 73,295 (89%) were reported by eight countries: Ukraine (53,218 cases; 64% of total); Serbia (5,076; 6%); France (2,913; 4%); Israel (2,919; 4%); Georgia (2,203; 3%); Greece (2,193; 3%); Italy (2,517; 3%); and Russia (2,256; 3%). The highest measles incidences in 2018 were in Ukraine (1,209.2 per 1 million) and Serbia (579.3). Among all measles cases reported in 2018, adults aged ≥20 years accounted for 30,561 (37%). The countries with the highest proportions of adult measles cases were Italy (68%), Serbia (67%), and Russia (42%). Among 179 measles deaths reported in EUR countries during 2009–2018, 114 (64%) occurred during 2017–2018, including 93 (82%) from four countries: Romania (46), Ukraine (20), Serbia (15), and Italy (12). EUR reported 17,587 measles virus sequences to the WHO global measles nucleotide surveillance database. The most predominant measles virus genotypes detected were D4 (21% overall, 66% during 2009–2012), D8 (45% overall, 76% during 2013–2016), and B3 (33% overall, 58% during 2017–2018) (8) (Supplementary Figure, https://stacks.cdc.gov/view/cdc/77667).

Regional Verification of Measles Elimination

The European Regional Verification Commission for Measles and Rubella Elimination was established in 2011 to evaluate the status of measles and rubella elimination^¶ in EUR countries based on documentation submitted annually by national verification committees (1). By the end of 2017, 43 (91%) countries had interrupted endemic measles virus transmission for ≥12 months, including 37 (70%)** that had sustained interruption for ≥36 months and were verified to have eliminated endemic measles virus transmission (8).

Discussion

After relatively stable albeit high measles incidence in EUR during 2009–2016, the number of reported measles cases tripled from 2017 to 2018, including outbreaks in eight countries reporting >2,000 measles cases each. The 2018 measles resurgence was attributable to measles virus transmission that began in 2017 and continued during 2018 in France, Greece, Romania, Russia, Serbia, and Ukraine. In addition, measles virus importations followed by widespread measles virus transmission occurred in countries that had achieved elimination, including Albania, Belarus, Czech Republic, Israel, and Montenegro. Despite high reported national coverage, factors associated with the resurgence included persistent measles virus reservoirs in EUR countries with limited resources and weak immunization systems, an accumulation of susceptible young children in marginalized communities with suboptimal coverage, and an accumulation of susceptible young adults who had escaped both natural measles infection and measles vaccination over a prolonged period of decreased measles incidence.

Outbreak response differed among countries. In some countries, large outbreaks caused substantial financial and human resource burdens, which resulted in delayed or inadequate outbreak responses and ongoing disease transmission. In other countries, outbreak response vaccination campaigns were not implemented because of insufficient political commitment, poor acceptance of mass immunization by health authorities and the public, lack of infrastructure to vaccinate specific susceptible population groups, and vaccine supply challenges. To achieve better outbreak control, countries in the region will need to adhere to their commitment to eliminate measles and rubella and ensure that dedicated financial and human resources are available for strong vaccination and surveillance programs, including outbreak preparedness and response.

The measles resurgence and the European Vaccine Action Plan midterm review in 2018 (9) highlighted ongoing challenges, including inadequate vaccine delivery infrastructure in some middle-income countries that resulted in suboptimal vaccination coverage and vaccine stock-outs; prevalent antivaccine sentiment; large populations of unvaccinated persons, including ethnic and religious minorities and adults; an increased proportion of cases in persons aged ≥20 years, who are difficult to reach with routine immunization services; and nosocomial outbreaks that affected patients and health care personnel with spread to the community.

To address these challenges and accelerate measles elimination efforts in EUR, the European Regional Office has targeted the following areas for action: 1) achieving and maintaining ≥95% vaccination coverage; 2) improving understanding of barriers to vaccination in vulnerable groups and increasing vaccine demand; 3) closing immunity gaps in the population through innovative and locally tailored approaches; 4) ensuring high-quality measles surveillance for rapid case detection and targeted outbreak response activities; and 5) strengthening infection prevention and control practices, particularly during outbreaks. The midterm review also highlighted the recent recommendation by the WHO Strategic Advisory Group of Experts on Immunization that countries institutionalize school entry checks to close immunity gaps as a key strategy for achieving measles elimination (10).

The findings in this report are subject to at least two limitations. First, surveillance data likely underestimate actual disease incidence because not all patients seek care, and it is likely that not all cases are reported. Second, measles surveillance performance and data quality vary among countries in the region, which might have led to reporting bias for some countries.

In EUR, 70% of countries have been verified as having achieved measles elimination; however, the recent resurgence highlighted challenges to achieving and maintaining elimination. All countries need to strengthen immunization programs to achieve and sustain high population immunity, maintain high-quality surveillance, and ensure outbreak preparedness and prompt response to contain outbreaks. Elimination efforts that focus on reaching vulnerable communities and adults will likely provide opportunities to improve access to vaccination services for all and help achieve European Vaccine Action Plan and future universal health goals.