Progress Toward Regional Measles Elimination — Worldwide, 2000–2017

In 2010, the World Health Assembly set three milestones for measles prevention to be achieved by 2015: 1) increase routine coverage with the first dose of measles-containing vaccine (MCV1) among children aged 1 year to ≥90% at the national level and to ≥80% in every district; 2) reduce global annual measles incidence to less than five cases per million population; and 3) reduce global measles mortality by 95% from the 2000 estimate (1).* In 2012, the World Health Assembly endorsed the Global Vaccine Action Plan (GVAP),† with the objective of eliminating measles§ in four of the six World Health Organization (WHO) regions by 2015 and in five regions by 2020. Countries in all six WHO regions have adopted goals for measles elimination by 2020. This report describes progress toward global measles control milestones and regional measles elimination goals during 2000-2017 and updates a previous report (2). During 2000-2017, estimated MCV1 coverage increased globally from 72% to 85%; annual reported measles incidence decreased 83%, from 145 to 25 cases per million population; and annual estimated measles deaths decreased 80%, from 545,174 to 109,638. During this period, measles vaccination prevented an estimated 21.1 million deaths. However, measles elimination milestones have not been met, and three regions are experiencing a large measles resurgence. To make further progress, case-based surveillance needs to be strengthened, and coverage with MCV1 and the second dose of measles-containing vaccine (MCV2) needs to increase; in addition, it will be important to maintain political commitment and ensure substantial, sustained investments to achieve global and regional measles elimination goals.

In 2010, the World Health Assembly set three milestones for measles prevention to be achieved by 2015: 1) increase routine coverage with the first dose of measles-containing vaccine (MCV1) among children aged 1 year to ≥90% at the national level and to ≥80% in every district; 2) reduce global annual measles incidence to less than five cases per million population; and 3) reduce global measles mortality by 95% from the 2000 estimate (1).* In 2012, the World Health Assembly endorsed the Global Vaccine Action Plan (GVAP), † with the objective of eliminating measles § in four of the six World Health Organization (WHO) regions by 2015 and in five regions by 2020. Countries in all six WHO regions have adopted goals for measles elimination by 2020. This report describes progress toward global measles control milestones and regional measles elimination goals during 2000-2017 and updates a previous report (2). During 2000-2017, estimated MCV1 coverage increased globally from 72% to 85%; annual reported measles incidence decreased 83%, from 145 to 25 cases per million population; and annual estimated measles deaths decreased 80%, from 545,174 to 109,638. During this period, measles vaccination prevented an estimated 21.1 million deaths. However, measles elimination milestones have not been met, and three regions are experiencing a large measles resurgence. To make further progress, case-based surveillance needs to be strengthened, and coverage with MCV1 and the second dose of measles-containing vaccine (MCV2) needs to increase; in addition, it will be important to maintain political commitment and ensure substantial, sustained investments to achieve global and regional measles elimination goals. * The coverage milestone is to be met by every country, whereas the incidence and mortality reduction milestones are to be met globally. † The Global Vaccine Action Plan is the implementation plan of the Decade of Vaccines, a collaboration between WHO; UNICEF; the Bill and Melinda Gates Foundation; the National Institute of Allergy and Infectious Diseases; the African Leaders Malaria Alliance; Gavi, the Vaccine Alliance; and others to extend the full benefit of immunization to all persons by 2020 and beyond. In addition to 2015 targets, it also set a target for measles and rubella elimination in five of the six WHO regions by 2020. http://www.who.int/immunization/ global_vaccine_action_plan/en; http://apps.who.int/gb/ebwha/pdf_files/ wha65/a65_22-en.pdf. § Measles elimination is defined as the absence of endemic measles virus transmission in a region or other defined geographic area for ≥12 months, in the presence of a high quality surveillance system that meets targets of key performance indicators.
* Mortality estimates for 2000 might be different from previous reports. When the model used to generate estimated measles deaths is rerun each year using the new WHO/UNICEF Estimates of National Immunization Coverage data, as well as updated surveillance data, adjusted results for each year, including the baseline year, are also produced and updated. † Coverage data: WHO/UNICEF Estimates of National Immunization Coverage, July 15, 2018 update. http://www.who.int/immunization/monitoring_surveillance/ data/en. § Reported case data: measles cases (2017) from World Health Organization, as of July 15, 2018 (http://apps.who.int/immunization_monitoring/globalsummary/ timeseries/tsincidencemeasles.html). Reported cases are a sizeable underestimate of the actual number of cases, accounting for the inconsistency between reported cases and estimated deaths. ¶ Cases per 1 million population; population data from United Nations, Department of Economic and Social Affairs, Population Division, 2017. Any country not reporting data on measles cases for that year was removed from both the numerator and denominator. ** Gavi, the Vaccine Alliance (Gavi), previously known as the Global Alliance for Vaccines and Immunization (GAVI), is a public-private global health partnership committed to increasing access to immunization in poor countries. Gavi-eligible countries are those that received funding support from Gavi, the Vaccine Alliance.
Countries are eligible to apply for Gavi support when their Gross National Income (GNI) per capita is ≤US$1,580 on average over the past three years (according to World Bank data published every year on July 1

Reported Measles Incidence
In 2017, 189 (97%) countries conducted measles casebased surveillance in at least part of the country, and 191 (98%) had access to standardized quality-controlled testing through the WHO Global Measles and Rubella Laboratory Network. However, surveillance was weak in many countries, and fewer than half of the countries reporting surveillance indicators (73 of 152; 48%) achieved the sensitivity indicator target of two or more discarded measles and rubella § § cases per 100,000 population. † † Supplemental immunization activities (SIAs) generally are carried out using two target age ranges. An initial, nationwide catch-up SIA focuses on all children aged 9 months-14 years, with the goal of eliminating susceptibility to measles in the general population. Periodic follow-up SIAs then focus on all children born since the last SIA. Follow-up SIAs generally are conducted nationwide every 2-4 years and focus on 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 MCV1. § § A discarded case is defined as a suspected case that has been investigated and discarded as nonmeasles and as nonrubella using 1) laboratory testing in a proficient laboratory or 2) epidemiological linkage to a laboratory-confirmed outbreak of a communicable disease that is not measles or rubella. The discarded case rate is used to measure the sensitivity of measles surveillance.
Countries report the aggregate number of incident measles cases ¶ ¶, *** to WHO

TABLE 2. (Continued) Measles supplementary immunization activities (SIAs)* and the delivery of other child health interventions, by World Health Organization (WHO) region and country -African, Eastern Mediterranean, European, South-East Asian, and Western Pacific Regions, 2017
Abbreviations: bOPV = bivalent oral poliovirus vaccine; DPT = diphtheria and pertussis toxoids and tetanus vaccine; DT = diphtheria and tetanus toxoids; DTaP = diphtheria and tetanus toxoids and acellular pertussis vaccine; Hib = Haemophilus influenzae type b vaccine; IPV = inactivated polio vaccine; N = national; OPV = oral poliovirus vaccine; PCV = pneumococcal conjugate vaccine; Penta = pentavalent (DTP, hepatitis B, Hib) vaccine; SIA = supplementary immunization activity; SN = subnational. * SIAs generally are carried out using two approaches: 1) An initial, nationwide catch-up SIA targets all children aged 9 months to 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. 2) Follow-up SIAs are generally conducted nationwide every 2-4 years and 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 1 dose of measles-containing vaccine, and the time since the last SIA. † Values >100% indicate that the number of doses administered exceeded the estimated target population. § Rollover national campaigns started the previous year or will continue into the next year. 5,789 reported measles virus sequences,**** 2,641 (45.6%) were genotype B3 (53 countries); 15 (0.26%) were D4 (two countries); 2,542 (43.9%) were D8 (49 countries); 46 (0.80%) were D9 (six countries); and 545 (9.4%) were H1 (11 countries).

Measles Mortality Estimates
A previously described model for estimating measles disease and mortality was updated with new measles vaccination coverage data, case data, and United Nations population estimates for all countries during 2000-2017, enabling derivation of a new series of disease and mortality estimates. For countries with previously anomalous estimates, the model was modified slightly to generate mortality estimates consistent with the observed case data (4). Based on the updated data, the estimated number of measles cases declined from 28,493,539 (95% confidence interval [

Regional Verification of Measles Elimination
In 2017, AFR and EMR established regional verification commissions (RVCs); thus, all six regions now have RVCs. In September 2016, the AMR RVC declared the region free of endemic measles (5). In 2017, the EUR RVC verified measles elimination in 37 (70%) countries and the reestablishment of endemic measles virus transmission in the Russian Federation and in Germany (6). In SEAR, Maldives and Bhutan were verified as having eliminated measles in 2017 (7). In WPR, six (22%) countries (Australia, Brunei, Cambodia, Japan, New Zealand, and South Korea) and two areas, Hong Kong Special  (8).
No EMR or AFR countries had verified elimination in 2017.

Discussion
During 2000-2017, increased coverage with MCV administered through routine immunization programs and SIAs, and other global measles elimination efforts contributed to an 83% decrease in reported measles incidence and an 80% reduction in estimated measles mortality. Measles vaccination prevented an estimated 21.1 million deaths during this period; the large majority of deaths averted were in AFR and among Gavi-eligible countries. Global MCV2 coverage has steadily increased since 2000; in 2017, 167 (86%) countries provided MCV2. In 2017, MCV1 and MCV2 coverage in WPR was ≥94%, and measles incidence in this region was at an all-time low. The increasing number of countries verified as having achieved measles elimination indicates progress toward global interruption of measles virus transmission.
Despite this progress, however, the 2015 global milestones have not been achieved; global MCV1 coverage has stagnated for nearly a decade; global MCV2 coverage is only at 67% despite steady increases; and SIA quality was inadequate to achieve ≥95% coverage in several countries. Since 2016, measles incidence has increased globally and in five of the six WHO regions. Furthermore, as of July 2018, endemic measles has been reestablished in Venezuela because of the sustained transmission of measles virus for >12 months; the remaining 34 AMR countries continue to maintain their measles elimination status, but the ongoing outbreak in Venezuela has led to measles virus importations and outbreaks in bordering AMR countries. In addition, the measles resurgence in Europe has likely led to reestablished endemic measles in some EUR countries. These outbreaks highlight the fragility of gains made toward global and regional measles elimination goals. Continuing to increase MCV1 and MCV2 coverage is critical to both the achievement and sustainability of the global and regional measles elimination goals. Meanwhile, conducting high quality SIAs that reach unvaccinated and undervaccinated children will prevent future outbreaks that are costly in terms of morbidity and mortality and are disruptive to immunizations service delivery. It is important to have high-performing surveillance for early detection of outbreaks; and when outbreaks do occur, thorough outbreak investigations are needed to better understand and address the underlying causes of the outbreak and why children are being missed by immunization delivery systems.
The findings in this report are subject to at least three limitations. First, SIA administrative coverage data might be biased by inaccurate reports of the number of doses delivered, doses administered to children outside the target age group, and inaccurate estimates of the target population size. Second, large differences between the estimated and reported incidence indicate variable surveillance sensitivity, making comparisons between countries and regions difficult to interpret. Finally, the accuracy of estimates from the measles mortality model is affected by biases in all model inputs, including countryspecific measles vaccination coverage and measles case-based surveillance data.
Monitoring progress toward measles elimination goals could be improved by establishing updated indicators. For example, the WHO Strategic Advisory Group of Experts on Immunization recently approved country classifications, and updates to the framework for the verification of measles elimination will standardize monitoring of countries' progress toward verified elimination (9). Moreover, synergizing future global health efforts and capitalizing on immunization partners' investments could be enhanced by dovetailing measles and rubella elimination strategies with post-GVAP immunization targets and strategies.
Strengthening routine immunization and continuing to conduct high-quality SIAs will help achieve global and regional measles elimination goals, improve overall vaccination coverage and equity, and assist in attaining universal health coverage. It is important that countries continue to strengthen case-based surveillance and increase MCV1 and MCV2 coverage and that immunization partners continue to raise the visibility of measles elimination goals and secure political commitment to these goals and sustained investments in health systems.

Summary
What is already known about this topic?
In 2012, the World Health Assembly endorsed the Global Vaccine Action Plan; as a result, countries in all six World Health Organization regions have adopted goals for elimination of measles by 2020.
What is added by this report?
During 2000-2017, annual reported measles incidence decreased 83%, and annual estimated measles deaths decreased 80%. Since 2000, global measles elimination efforts have prevented an estimated 21.1 million deaths. However, measles elimination milestones have not been met, and three regions are experiencing a large measles resurgence.
What are the implications for public health practice?
To make further progress, case-based surveillance needs to be strengthened, and coverage with the first and second dose of measles-containing vaccine needs to increase; moreover, it is important to maintain political commitment, and secure substantial, sustained investments.