Progress Toward Regional Measles Elimination — Worldwide, 2000–2018

In 2010, the World Health Assembly (WHA) set the following three milestones for measles control 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 1 million population, and 3) reduce global measles mortality by 95% from the 2000 estimate* (1). In 2012, WHA endorsed the Global Vaccine Action Plan,† with the objective of eliminating measles§ in five of the six World Health Organization (WHO) regions by 2020. This report updates a previous report (2) and describes progress toward WHA milestones and regional measles elimination during 2000-2018. During 2000-2018, estimated MCV1 coverage increased globally from 72% to 86%; annual reported measles incidence decreased 66%, from 145 to 49 cases per 1 million population; and annual estimated measles deaths decreased 73%, from 535,600 to 142,300. During 2000-2018, measles vaccination averted an estimated 23.2 million deaths. However, the number of measles cases in 2018 increased 167% globally compared with 2016, and estimated global measles mortality has increased since 2017. To continue progress toward the regional measles elimination targets, resource commitments are needed to strengthen routine immunization systems, close historical immunity gaps, and improve surveillance. To achieve measles elimination, all communities and countries need coordinated efforts aiming to reach ≥95% coverage with 2 doses of measles vaccine (3).

In 2010, the World Health Assembly (WHA) set the following three milestones for measles control 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 1 million population, and 3) reduce global measles mortality by 95% from the 2000 estimate* (1). In 2012, WHA endorsed the Global Vaccine Action Plan, † with the objective of eliminating measles § in five of the six World Health Organization (WHO) regions by 2020. This report updates a previous report (2) and describes progress toward WHA milestones and regional measles elimination during 2000-2018. During 2000-2018, estimated MCV1 coverage increased globally from 72% to 86%; annual reported measles incidence decreased 66%, from 145 to 49 cases per 1 million population; and annual estimated measles deaths decreased 73%, from 535,600 to 142,300. During 2000-2018, measles vaccination averted an estimated 23.2 million deaths. However, the number of measles cases in 2018 increased 167% globally compared with 2016, and estimated global measles mortality has increased since 2017. To continue progress toward the regional measles elimination targets, resource commitments * 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. https://www.who.int/immunization/ global_vaccine_action_plan/en; https://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. are needed to strengthen routine immunization systems, close historical immunity gaps, and improve surveillance. To achieve measles elimination, all communities and countries need coordinated efforts aiming to reach ≥95% coverage with 2 doses of measles vaccine (3).

Immunization Activities
WHO and the United Nations Children's Fund (UNICEF) use data from administrative records and vaccination coverage surveys reported annually to estimate MCV1 and second dose (MCV2) coverage through routine immunization services. ¶ During 2000-2018, estimated MCV1 coverage increased globally from 72% to 86% (Table), although coverage has remained at 84%-86% since 2010, with considerable regional variation. Since 2016, MCV1 coverage has remained relatively constant in the African Region (AFR) (74%-75%), the Eastern Mediterranean Region (EMR) (82%-83%), and the South-East Asia Region (SEAR) (88%-89%); and it ¶ For MCV1, among children aged 1 year or, if MCV1 is given at age ≥1 year, among children aged 24 months. For MCV2, among children at the recommended age for administration of MCV2, per the national immunization schedule. WHO/ UNICEF estimates of national immunization coverage are available at https:// www.who.int/immunization/monitoring_surveillance/data/en.

Reported Measles Incidence
In 2018, all 194 WHO member countries conducted measles surveillance, and 191 (98%) had access to standardized quality-controlled laboratory testing through the WHO Global Measles and Rubella Laboratory Network. However, surveillance remains weak in many countries, and only 84 (55%) of 152 countries that reported surveillance indicators achieved the sensitivity indicator target of ≥2 discarded measles and rubella § § cases per 100,000 population. † † Supplementary 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 due to low MCV coverage and to protect children who did not respond to MCV1. Data on SIAs by country are available at https://www.who.int/ immunization/monitoring_surveillance/data/Summary_Measles_SIAs.xls?ua. § § A discarded case is defined as a suspected case that has been investigated and determined not to be measles or rubella 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.

Measles Case and Mortality Estimates
A previously described model for estimating measles cases and deaths was updated with new measles vaccination coverage data, case data, and United Nations population estimates for all countries during 2000-2018, enabling derivation of a new series of disease and mortality estimates (5). For countries with anomalous estimates in previous iterations, the model was modified slightly to generate mortality estimates consistent with observed case data. Based on the updated data, the estimated number of measles cases decreased 65%, from 28,219,100 (95% confidence interval [CI] = 20,141,900-65,455,000) in 2000 to 9,769,400 (95% CI = 6,446,900-40,538,500) in 2018. During this period, estimated measles deaths decreased 73%, from 535,600 (95% CI = 363,400-901,700) to 142,300 (95% CI = 93,600-387,900) (Table) (Figure 2). During 2000-2018, compared with no measles vaccination, measles vaccination prevented an estimated 23.2 million deaths globally.
Korea, Oman, Singapore, Switzerland, and Timor-Leste were verified as having achieved elimination during 2018. No AFR country had yet been verified as having eliminated measles. In the AMR, a region that had achieved verification of measles elimination in 2016, endemic measles transmission was reestablished in Venezuela in 2018 and in Brazil in 2019. In EUR, endemic measles transmission was reestablished during 2018 in Albania, Czechia, Greece, and the United Kingdom.

Discussion
During 2000-2018, increased coverage with MCV1 and MCV2, widespread SIAs, and other elimination efforts contributed to a 66% decrease in reported measles incidence, a 73% reduction in estimated measles mortality, and a reduction in the number of circulating measles virus genotypes worldwide. Despite this progress, the 2015 global milestones were not met: MCV1 coverage has stagnated for nearly a decade, MCV2 coverage is only 69%, and suboptimal surveillance limits data-driven actions. Reported measles incidence has increased in five regions since 2016 and estimated global measles mortality has increased since 2017. Increased measles cases and outbreaks occurred mostly among unvaccinated persons, including school-aged children and young adults.
The causes of the measles resurgence during 2017-2018 are multifactorial and vary by country. Large sustained outbreaks in a few countries with weak immunization systems accounted for most reported measles cases during this time. In addition, unidentified or unaddressed immunity gaps in older children and adults, because of historically weak routine immunization programs and inadequate SIA coverage, led to sustained transmission in some countries that previously had low incidence or had eliminated measles (6). As well, international travel by infected persons, including both unimmunized foreign visitors and unimmunized residents traveling abroad and returning home, facilitated international spread of measles. For example, in 2018, Israel experienced nearly 100 measles importations from multiple countries including Philippines, Ukraine, and the United Kingdom; and importations from Israel and Ukraine led to outbreaks in the United States (7). Sustaining elimination in the face of frequent importations and gaps in vaccination coverage presents challenges. For example, after having experienced >100 importations in 2018 as a consequence of inadequate vaccination coverage, endemic measles virus transmission has been reestablished in the United Kingdom. Countries such as Cambodia, which, through sustained efforts, identified and closed immunity gaps to achieve elimination, but which border countries with ongoing endemic transmission, must remain vigilant to identify and stop measles outbreaks rapidly. Before international travel, travelers from all countries should ensure they have No. of measles deaths (millions) Year

FIGURE 2. Estimated annual number of measles deaths, with and without vaccination programs -worldwide, 2000-2018*
been appropriately vaccinated against measles. Progress toward measles elimination will regress without a unified effort by all communities and countries. Evaluations of routine immunization programs to identify barriers to vaccination indicate that children miss MCV1 and MCV2 doses for many reasons, including families' limited awareness of the need for vaccination, limited access to or financial barriers to receiving vaccination; vaccine stock-outs; political instability; and vaccine hesitancy and misinformation. WHO's Global Routine Immunization Strategies and Practices and The Guide to Tailoring Immunization Programmes provides guidance on identifying demand and supply barriers to routine vaccination and strengthening immunization programs (8,9). Outbreaks should serve as opportunities to investigate underlying causes of undervaccination and to design specific routine immunization strengthening activities to prevent future outbreaks. In addition, population immunity gaps should be identified through triangulation of data, including surveillance and vaccination coverage data, and should be targeted by vaccination activities.
The findings in this report are subject to at least two limitations. First, large differences between estimated and reported incidence indicate overall low surveillance sensitivity, making comparisons between regions difficult to interpret. Second, the measles mortality model estimates might be affected by biases in model inputs, including vaccination coverage and surveillance data.
The trends of increasing measles incidence and mortality are reversible; however, further progress toward achieving elimination goals will require 1) resource commitments to strengthen routine immunization systems, close historical immunity gaps, and improve surveillance to rapidly detect and respond to cases, and 2) a new perspective to use measles as a stimulus and guide to improving immunization programs. To achieve measles elimination, all communities and countries need coordinated efforts aiming to reach ≥95% coverage with 2 doses of measles vaccine.
As the period covered by the Global Vaccine Action Plan 2012-2020 approaches its end, a new vision and strategy for accelerated progress on immunization for 2021-2030 is being

Summary
What is already known about this topic?
In 2012, the World Health Assembly endorsed the Global Vaccine Action Plan; countries in all six World Health Organization regions have adopted goals to eliminate measles by 2020.
What is added by this report?
What are the implications for public health practice? To achieve regional measles elimination goals, resource commitments are needed to strengthen routine immunization systems, close immunity gaps, and improve case-based surveillance.
developed by countries and stakeholders (10). Pillars of this evolving strategy include commitment and demand, research and innovation, life course and integration, and supply and sustainability; all of these are vital to achieving and maintaining measles elimination. This new agenda should be used to secure the necessary resource commitments to improve coverage and equity substantially and, in so doing, further progress toward achieving the measles elimination goals.