Progress Toward Measles Elimination — Eastern Mediterranean Region, 2013–2019

In 1997, during the 41st session of the Regional Committee for the Eastern Mediterranean, the 21 countries in the World Health Organization (WHO) Eastern Mediterranean Region* (EMR) passed a resolution to eliminate† measles (1). In 2015, this goal was included as a priority in the Eastern Mediterranean Vaccine Action Plan 2016-2020 (EMVAP) (2), endorsed at the 62nd session of the Regional Committee (3). To achieve this goal, the WHO Regional Office for the Eastern Mediterranean developed a four-pronged strategy: 1) achieve ≥95% vaccination coverage with the first dose of measles-containing vaccine (MCV1) among children in every district of each country through routine immunization services; 2) achieve ≥95% vaccination coverage with a second MCV dose (MCV2) in every district of each country either through implementation of a routine 2-dose vaccination schedule or through supplementary immunization activities§ (SIAs); 3) conduct high-quality, case-based surveillance in all countries; and 4) provide optimal measles clinical case management, including dietary supplementation with vitamin A (4). This report describes progress toward measles elimination in EMR during 2013-2019 and updates a previous report (5). Estimated MCV1 coverage increased from 79% in 2013 to 82% in 2018. MCV2 coverage increased from 59% in 2013 to 74% in 2018. In addition, during 2013-2019, approximately 326.4 million children received MCV during SIAs. Reported confirmed measles incidence increased from 33.5 per 1 million persons in 2013 to 91.2 in 2018, with large outbreaks occurring in Pakistan, Somalia, and Yemen; incidence decreased to 23.3 in 2019. In 2019, the rate of discarded nonmeasles cases¶ was 5.4 per 100,000 population. To achieve measles elimination in the EMR, increased visibility of efforts to achieve the measles elimination goal is critically needed, as are sustained and predictable investments to increase MCV1 and MCV2 coverage, conduct high-quality SIAs, and reach populations at risk for not accessing immunization services or living in areas with civil strife.

In 1997, during the 41st session of the Regional Committee for the Eastern Mediterranean, the 21 countries in the World Health Organization (WHO) Eastern Mediterranean Region* (EMR) passed a resolution to eliminate † measles (1). In 2015, this goal was included as a priority in the Eastern Mediterranean Vaccine Action Plan 2016-2020 (EMVAP) (2), endorsed at the 62nd session of the Regional Committee (3). To achieve this goal, the WHO Regional Office for the Eastern Mediterranean developed a four-pronged strategy: 1) achieve ≥95% vaccination coverage with the first dose of measles-containing vaccine (MCV1) among children in every district of each country through routine immunization services; 2) achieve ≥95% vaccination coverage with a second MCV dose (MCV2) in every district of each country either through implementation of a routine 2-dose vaccination schedule or through supplementary immunization activities § (SIAs); 3) conduct high-quality, case-based surveillance in all countries; and 4) provide optimal measles clinical case management, including dietary supplementation with vitamin A (4). This report describes progress toward measles elimination in EMR during 2013-2019 and updates a previous report (5). Sudan, Syria, Tunisia, United Arab Emirates, and Yemen. † Measles elimination is defined as the absence of endemic measles cases for a period of ≥12 months, in the presence of adequate surveillance. § SIAs are immunization campaigns, typically carried out using two targeted age ranges. An initial, nationwide catch-up SIA targets all children aged 9 months-14 years, with the goal of eliminating measles susceptibility in the population. Periodic follow-up SIAs then target all children born since the last SIA. Follow-up SIAs generally are conducted every 2 to 4 years and target children aged 9-59 months; the goal of a follow-up SIA is to vaccinate children who have not received a first dose and to protect children who did not respond to the first dose of measles vaccine.
in Pakistan, Somalia, and Yemen; incidence decreased to 23.3 in 2019. In 2019, the rate of discarded nonmeasles cases ¶ was 5.4 per 100,000 population. To achieve measles elimination in the EMR, increased visibility of efforts to achieve the measles elimination goal is critically needed, as are sustained and predictable investments to increase MCV1 and MCV2 coverage, conduct high-quality SIAs, and reach populations at risk for not accessing immunization services or living in areas with civil strife.

Immunization Activities
MCV1 and MCV2 administrative coverage** data are reported each year from all EMR countries and areas to WHO and the United Nations Children's Fund (UNICEF) through the Joint Reporting Form. WHO and UNICEF use reported administrative coverage and available survey results to generate annual estimates of vaccination coverage through routine immunization services (6). During 2013-2018, estimated regional MCV1 coverage increased from 79% to 82%, and estimated MCV2 coverage increased from 59% to 74% (Table 1). In 2018, 11 (52%) of 21 countries and areas achieved ≥95% coverage with both MCV1 and MCV2. As of 2018, only one (5%) EMR country (Somalia) had not yet introduced MCV2. During 2013-2019, 326.4 million persons were vaccinated during 89 SIAs, with weighted regional SIA coverage of 98% (Table 2). Reported vaccination coverage was ≥90% in 25 (68%) of 37 nationwide SIAs, including ≥95% in 11 (30%).

Surveillance Activities
Case-based measles surveillance † † data are reported monthly to WHO from all EMR countries except Somalia. In Somalia, ¶ Suspected cases that have been investigated and determined not to be measles using laboratory testing in a proficient laboratory or epidemiologic linkage to a laboratory-confirmed outbreak of another communicable disease that is not measles are discarded as nonmeasles cases. A proficient laboratory is one that is WHO accredited or has an established quality assurance program with oversight by a WHO accredited laboratory. ** Administrative vaccination coverage is the number of vaccine doses administered divided by the estimated target population. † † Case-based measles surveillance includes individual case investigation and blood specimen collection for laboratory testing. surveillance performance indicators ¶ ¶ including 1) the number of suspected measles cases ultimately discarded as nonmeasles (target = two or more per 100,000 population); 2) the proportion of second-level units (e.g., districts) with two or more discarded cases per 100,000 (target = 80%); 3) suspected cases ¶ ¶ Important surveillance performance indicators include 1) two or more discarded nonmeasles cases per 100,000 population at the national level per year; 2) two or more discarded nonmeasles cases per 100,000 per year in ≥80% of subnational administrative units; 3) adequate investigation of ≥80% of suspected measles cases conducted within 48 hours of notification; 4) adequate collection and testing in a proficient laboratory of specimens from ≥80% of suspected cases for detecting acute measles and rubella infection; 5) receipt of ≥80% of specimens at the laboratory within 5 days of collection; 6) report of ≥80% of serology results by the laboratory within 4 days of specimen receipt; and 7) on-time reporting of measles and rubella data to the national level by ≥80% of surveillance units.  Abbreviations: EMR = Eastern Mediterranean Region; M = measles vaccine; MMR = measles, mumps, and rubella vaccine; MR = measles and rubella vaccine. * SIAs generally are carried out using two approaches. An initial, nationwide catch-up SIA targets all children aged 9 months-14 years; it has the goal of eliminating susceptibility to measles in the general population. Periodic follow-up SIAs then target all children born since the last SIA. Follow-up SIAs generally are conducted nationwide every 2-4 years and generally target children aged 9-59 months; their goal is to eliminate any measles susceptibility that has developed in recent birth cohorts and to protect children who did not respond to the first measles vaccination. The exact age range for follow-up SIAs depends on the age-specific incidence of measles, coverage with measles-containing vaccine through routine services, and the time since the last SIA. † Targeted age groups varied by province. § Outbreak response immunization campaign that targeted children aged 6 months through 15 years and also young miners aged ≥15 years. ¶ Average SIA coverage, weighted by size of target population.

TABLE 2. (Continued) Characteristics of measles supplementary immunization activities (SIAs),* by year and country/area -World Health Organization Eastern Mediterranean Region, 2013-2019
with adequate investigation*** (target = 80%); 4) suspected cases with adequate blood specimens † † † (target = 80%); and 5) laboratory results available <5 days after specimen receipt (target = 80%). *** Adequate investigation is a case investigated within 48 hours of notification that includes all 10 core variables: 1) case identification; 2) date of birth/ age; 3) sex; 4) place of residence; 5) vaccination status or date of last vaccination; 6) date of rash onset; 7) date of notification; 8) date of investigation; 9) date of blood sample collection; and 10) place of infection or travel history. † † † An adequate blood specimen is a sample by venipuncture in a sterile tube with a volume of 5 ml for older children and adults and 1 ml for infants and younger children. Adequate samples for antibody detection are those collected within 28 days after onset of rash.
During 2013-2019, the number of EMR countries and areas that met the target for suspected cases discarded as nonmeasles per 100,000 population at the national level increased from 14 (67%) to 18 (86%), and from seven (33%) to 11 (52%) at the subnational level. From 2013 to 2019, the rate of discarded nonmeasles cases decreased from 6.4 per 100,000 population to 5.4; the percentage of suspected cases with adequate investigations increased from 76% to 86%; the percentage of suspected cases with adequate specimens collected for laboratory testing decreased from 85% to 70%, and the proportion of blood specimens received by the laboratory with results available in <5 days decreased from 86% to 66% (Supplementary Table,  What is added by this report?
Annual regional measles incidence increased from 33.5 per million population in 2013 to 91.2 in 2018, primarily because of large outbreaks in Pakistan, Somalia, and Yemen; then decreased to 23.3 in 2019.
What are the implications for public health practice?
To achieve measles elimination, efforts are needed to increase MCV1 and MCV2 coverage, conduct high-quality supplementary immunization activities, and reach populations at high risk for not accessing immunization services or living in areas with civil strife.
latter two performance indicators were largely because of the changes in Somalia's surveillance and a large-scale outbreak in Yemen during 2018-2019.

Measles Incidence and Genotypes
In EMR, reported measles cases decreased 74% from 2013 to 2014, from 16,531 to a record low of 9,499; however, in 2015, 2017, and 2018, reported measles cases increased to 21,734, 34,286 and 64,198, respectively, and then decreased to 16,703 in 2019 (Figure). Annual regional measles incidence per million population approximately tripled from 33.5 in 2013 to 91.2 in 2018, then decreased to 23.3 in 2019 ( Table 1). The increase in measles cases during 2015-2018 occurred primarily because of large outbreaks in Somalia during 2015-2017, Pakistan during 2017-2018, and Yemen in 2018. The number of detected circulating measles virus genotypes in EMR decreased from four in 2013 (B3 in 13 countries, D4 in three countries, D8 in three countries, and H1 in one country) to two in 2019 (B3 in 15 countries and D8 in five countries).

Regional Verification of Measles Elimination
The EMR Verification Commission for Measles Elimination was established in February 2018 to evaluate the status of measles elimination in EMR countries based on documentation submitted annually by national verification committees. By the end of 2019, three (14%) EMR countries (Bahrain, Iran, and Oman) were verified as having achieved measles elimination (9).

Discussion
During 2013-2018, both MCV1 and MCV2 coverage in EMR increased but remained 14 percentage points and 22 percentage points below the WHO-recommended level of ≥95%. Although a few EMR countries have achieved and maintained measles elimination, large-scale measles outbreaks in others have revealed persistent suboptimal coverage with 2 doses of MCV through routine immunization services. In several EMR countries, major challenges to implementing measles elimination activities include civil unrest, armed conflict, and unpredictable mass population displacements and resettlements that can disrupt all aspects of planning and implementation of immunization services delivery, including SIAs. Conducting SIAs in areas with no local government requires building strong partnerships and close links with local communities. Implementing periodic SIAs according to WHO SIA guidelines (https://www.who.int/immunization/diseases/measles/SIA-Field-Guide.pdf ) and using the WHO SIA readiness assessment tool (http://www9.who. int/immunization/diseases/measles/en/) to ensure a highquality activity that achieves ≥95% coverage, particularly in areas with complex humanitarian emergencies, requires the availability of adequate funds for vaccines and supplies, operational costs, and experienced personnel who can implement a complex activity in a culturally appropriate manner under challenging circumstances.
Measles elimination efforts can leverage assets, experience, and capacity from the Global Polio Eradication Initiative (GPEI). The Eastern Mediterranean Regional Technical Advisory Group on Immunization recommended forming a multipartner taskforce to apply lessons learned from the GPEI and address gaps in measles vaccination coverage. These include mapping areas where children who are missed by routine immunization services live, identifying reasons for being missed, and developing a strategic plan that includes allocation of necessary resources for implementation (10).
The findings in this report are subject to at least two limitations. First, administrative coverage might overestimate vaccination coverage through erroneous inclusion of SIA doses or doses administered to children outside target age groups, inaccurate estimates of the target population size, and inaccurate reports of the number of doses delivered. Second, surveillance data likely underestimate measles incidence because not all patients seek care, and not all measles cases in patients who seek care are reported.
To accelerate progress toward measles elimination in EMR, the visibility of efforts to achieve the measles elimination goal must be raised, including the benefits of achieving measles elimination. The new global guidance document to