Progress Toward Measles Elimination — Pakistan, 2000–2018

In 1997, the 21 countries in the World Health Organization (WHO) Eastern Mediterranean Region* (EMR) passed a resolution during the 41st session of the Regional Committee for the Eastern Mediterranean to eliminate measles† (1). In 2015, this goal was included as a priority in the Eastern Mediterranean Vaccine Action Plan 2016-2020 (2), approved at the 62nd session of the Regional Committee (3). To achieve measles elimination, the WHO Regional Office for the Eastern Mediterranean developed the following four-pronged strategy: 1) achieve ≥95% vaccination coverage with the first dose of measles-containing vaccine (MCV) among children in every district of each country through routine immunization services; 2) achieve ≥95% vaccination coverage with a second MCV dose 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 measles surveillance in all countries; and 4) provide optimal measles clinical case management, including dietary supplementation with vitamin A (4). Pakistan, an EMR country with a population of approximately 200 million, accounts for nearly one third of the overall EMR population. This report describes progress and challenges toward measles elimination in Pakistan during 2000-2018. During the study period, estimated coverage with the first MCV dose (MCV1) increased from 57% in 2000 to 76% in 2017. The second MCV dose (MCV2) was introduced nationwide in 2009, and MCV2 coverage increased from 30% in 2009 to 45% in 2017. During 2000-2018, approximately 232.5 million children received doses of MCV during SIAs. Reported confirmed measles incidence increased from an average of 24.6 per 1 million persons during 2000-2009 to an average of 80.4 during 2010-2018, with peaks in 2013 (230.3) and 2018 (153.6). In 2017 and 2018, the rates of suspected cases discarded as nonmeasles after investigation were 2.1 and 1.5 per 100,000 population, reflecting underreporting of cases. To achieve measles elimination, additional efforts are needed to increase MCV1 and MCV2 coverage, develop strategies to identify and reach communities not accessing immunization services, and increase sensitivity of case-based measles surveillance in all districts.

In 1997, the 21 countries in the World Health Organization (WHO) Eastern Mediterranean Region* (EMR) passed a resolution during the 41st session of the Regional Committee for the Eastern Mediterranean to eliminate measles † (1). In 2015, this goal was included as a priority in the Eastern Mediterranean Vaccine Action Plan 2016-2020 (2), approved at the 62nd session of the Regional Committee (3). To achieve measles elimination, the WHO Regional Office for the Eastern Mediterranean developed the following four-pronged strategy: 1) achieve ≥95% vaccination coverage with the first dose of measles-containing vaccine (MCV) among children in every district of each country through routine immunization services; 2) achieve ≥95% vaccination coverage with a second MCV dose 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 measles surveillance in all countries; and 4) provide optimal measles clinical case management, including dietary supplementation with vitamin A (4). Pakistan, an EMR country with a population of approximately 200 million, accounts for nearly one third of the overall EMR population. This report describes progress and challenges toward measles elimination in Pakistan during 2000-2018. During the study period, estimated coverage with the first MCV dose (MCV1) increased from 57% in 2000 to 76% in 2017. The second MCV dose (MCV2) was introduced nationwide in 2009, and MCV2 coverage increased from 30% in 2009 to 45% in 2017. During 2000-2018, approximately 232.5 million children received doses of MCV during SIAs. Reported confirmed measles incidence increased from an * The Eastern Mediterranean Region, one of six regions of the World Health Organization, consists of 21 member states and Palestine (West Bank and Gaza Strip), with a population of nearly 583 million persons. The member states are as follows: Afghanistan, Bahrain, Djibouti, Egypt, Iran, Iraq, Jordan, Kuwait, Lebanon, Libya, Morocco, Oman, Pakistan, Qatar, Saudi Arabia, Somalia, 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 eliminate any measles susceptibility that has accumulated in recent birth cohorts and to protect children who did not respond to the first dose of measles vaccine. and 2018 (153.6). In 2017 and 2018, the rates of suspected cases discarded as nonmeasles after investigation were 2.1 and 1.5 per 100,000 population, reflecting underreporting of cases. To achieve measles elimination, additional efforts are needed to increase MCV1 and MCV2 coverage, develop strategies to identify and reach communities not accessing immunization services, and increase sensitivity of case-based measles surveillance in all districts.

Immunization Activities
MCV1 was introduced in the routine childhood immunization schedule nationwide in Pakistan in 1974 (4), and MCV2 was added to the schedule in 2009. The doses are administered to children at ages 9 and 15 months. Administrative vaccination coverage ¶ data are reported each year from all districts** in Pakistan to the National Immunization Programme, where they are aggregated and reported 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 (5). Estimated MCV1 coverage in Pakistan increased from 57% in 2000 to 76% in 2017, and estimated MCV2 coverage increased from 30% in 2009 to 45% in 2017 ( Figure). A Demographic and Health Survey implemented nationwide during 2017-2018 estimated MCV1 and MCV2 coverage at 73% and 67%, respectively. Among the eight provinces and federal areas, survey estimates of MCV1 and MCV2 coverage were highest in Punjab (85% and 82%, respectively), Islamabad (83%, 77%), and Azad Jammu and Kashmir (83%, 75%); intermediate in Gilgit-Baltistan (66%, 62%), Khyber Pakhtunkhwa (63%, 50%) and Sindh (61%, 60%); and lowest in the Federally Administered Tribal Areas (35%, 21%) and Balochistan (33%, 34%) (6).

Surveillance Activities and Measles Incidence
Aggregated measles cases † † are reported by all health facilities in Pakistan through the National Health Management Information System and reported annually through the Joint Reporting Form. In 2009, case-based measles surveillance § § was initiated in Pakistan following WHO Regional Office for the Eastern Mediterranean guidelines and using the existing vaccine-preventable diseases surveillance system with some modification (7). During 2013-2018, the case-based surveillance system was expanded to include additional health facilities; as of 2018, there were 7,555 reporting units. WHO technical officers were appointed in every province and area † † Aggregate measles surveillance involves a report of a summary of suspected measles cases, by age group and location (district), but does not include a line-listing of individual cases. § § Case-based measles surveillance includes individual case investigation and blood specimen collection for laboratory testing. Essential data elements to be obtained during the investigation include name or identifier, date of birth or age, sex, place of residence, vaccination status or date of last vaccination, date of rash onset, date of notification, date of investigation, date of specimen collection, and place of infection or travel history. * 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 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 vaccine dose. The exact age range for follow-up SIAs depends on the age-specific incidence of measles, measles vaccination coverage through routine services, and the time since the last SIA. Monovalent measles vaccine was used in all SIAs. † 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. ¶ Average SIA coverage, weighted by size of target population.
in the country during 2017-2018 to monitor key surveillance performance indicators. ¶ ¶ Reporting of measles virus genotyping to the WHO global measles nucleotide surveillance database was begun in 2007 (8). ¶ ¶ Key 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. During 2017 and 2018, the rates of suspected cases discarded after investigation were 2.1 and 1.5 per 100,000 population, respectively (Table 2)   Abbreviation: MCV = measles-containing vaccine. * An illness in any person a clinician suspects of having a measles infection, or in any person with fever and rash, and cough, coryza or conjunctivitis. † Epidemiologically linked measles cases are those that occurred in geographic and temporal proximity to a laboratory-confirmed case or to another epidemiologically linked case. § Clinically compatible measles cases are suspected cases for which there is no laboratory confirmation or epidemiologic link. ¶ Discarded nonmeasles cases include those suspected measles cases with an adequate specimen for laboratory testing that were found to be measles immunoglobulin M (IgM) antibody negative or rubella IgM antibody positive. ** Includes collection of all the following data elements regarding each suspected case of measles: patient name or identifiers, place of residence, place of infection (at least to district level), age (or date of birth), sex, date of rash onset, date of specimen collection, measles vaccination status, date of last measles vaccination, date of notification, date of investigation, and travel history. † † Blood specimen collected within 28 days of rash onset. § § A World Health Organization-accredited laboratory that has an established quality assurance program or one with oversight by a World Health Organizationaccredited laboratory.
[DTP] vaccine, 3 doses of polio vaccine, and 1 dose of measles vaccine) ranged from 80% among children in the highest wealth quintile to 38% among children in the poorest wealth quintile and from 71% among children residing in urban areas to 63% among those in rural areas (6). To reduce disparities, increase vaccination coverage, and achieve measles elimination, enhanced efforts are needed to reach all children, particularly those in rural areas and poor communities. Periodic highquality SIAs conducted according to WHO SIA guidelines, using the WHO SIA readiness assessment tool to ensure ≥95% 2-dose coverage, will require availability of adequate resources for success. For the 2018 SIA, Gavi, the Vaccine Alliance, provided funding support, and WHO, UNICEF and other international partners contributed to SIA planning, implementation, and monitoring. A postcampaign survey documented 93.3% coverage nationally, demonstrating the potential impact that appropriately funded and well-executed activities can have on improving SIA quality. Case-based measles surveillance was introduced in 2009 and strengthened during 2017-2018. Some of the apparent increase in measles cases, especially during 2013-2018, reflects improved surveillance sensitivity. Nonetheless, WHO standard surveillance indicators reflected underreporting and low sensitivity of case detection overall. To increase case-based surveillance sensitivity to achieve measles elimination, case-based surveillance reporting sites need to be expanded to all health facilities in the country. High-quality nationwide case-based surveillance data are essential for identifying subpopulations with measles susceptibility in need of SIAs.
Pakistan remains one of only three countries worldwide that has never interrupted wild poliovirus type 1 transmission (9); therefore, polio eradication activities remain intense in the country. Measles elimination efforts can leverage the polio assets, experience, and capacity to identify and reach communities not accessing routine immunization services; engage local leaders and community members to ensure that all children in the target age groups participate in SIAs; use epidemiologic investigations to identify areas that need additional SIAs; and improve outbreak preparedness and response to rapidly contain outbreaks.
The Eastern Mediterranean Regional Technical Advisory Group on Immunization (RTAG) recommended forming a multipartner taskforce to apply lessons learned from the polio eradication initiative to address gaps in measles vaccination coverage. These include mapping areas where children missed by routine immunization services reside, identifying reasons for being missed, and developing a strategic plan that includes allocation of necessary resources for implementation (10). RTAG also recommended introduction of rubella-containing vaccine into the national infant immunization schedule by 2020. Introduction of combined measles-rubella vaccine would provide an opportunity to build population measles immunity to achieve measles and rubella elimination through a measlesrubella vaccine SIA targeting children aged <15 years.
The findings in this report are subject to at least three limitations. First, administrative coverage might overestimate vaccination coverage through erroneous inclusion of SIA doses or doses administered to children outside of 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 patients who seek care are reported. Finally, efforts to strengthen surveillance over time likely led to reporting bias through increased reporting efficiency annually.
To advance progress toward measles elimination in Pakistan, there is a need to raise the visibility of measles elimination efforts, including the benefits of achieving measles elimination. Without jeopardizing the focused efforts to interrupt poliovirus transmission, transitioning the substantial polio infrastructure and resources should be carefully managed to support measles elimination and broader EMR vaccination goals.
Corresponding author: James P. Alexander, Jr., axj1@cdc.gov. 1 Communicable Diseases Cluster, Pakistan Country Office, World Health Organization; 2 Global Immunization Division, Center for Global Health, CDC; 3 National Immunization Program, Federal Ministry of Health, Islamabad, Pakistan; 4 National Institutes for Health, Islamabad, Pakistan; 5 Vaccine Preventable Diseases and Immunization, World Health Organization Eastern Mediterranean Regional Office, Cairo, Egypt.

Summary
What is already known about this topic?
In the 2 decades before 2000, estimated coverage with the first measles-containing vaccine dose (MCV1) in Pakistan was ≤57%. The number of reported measles cases per year averaged approximately 29,000 during 1980-1989 and 3,900 during 1990-1999.
What is added by this report? Estimated MCV1 coverage increased from 57% to 76% during 2000-2017, and second-dose coverage increased from 30% to 45% during 2009-2017. Approximately 232.5 million children were vaccinated with MCV during 2005-2018 vaccination campaigns. Despite these efforts, MCV coverage remained well below the recommended level of 95%, and measles incidence increased during 2010-2018.
What are the implications for public health practice?
To achieve measles elimination, efforts are needed to increase 2-dose vaccine coverage, reach communities not accessing immunization services, and increase measles surveillance sensitivity.