Progress Toward Measles Elimination — Bangladesh, 2000–2016

In 2013, at the 66th session of the Regional Committee of the World Health Organization (WHO) South-East Asia Region (SEAR), a regional goal was established to eliminate measles and control rubella and congenital rubella syndrome* by 2020 (1). WHO-recommended measles elimination strategies in SEAR countries include 1) achieving and maintaining ≥95% coverage with 2 doses of measles-containing vaccine (MCV) in every district, delivered through the routine immunization program or through supplementary immunization activities (SIAs)†; 2) developing and sustaining a sensitive and timely measles case-based surveillance system that meets targets for recommended performance indicators; and 3) developing and maintaining an accredited measles laboratory network (2). In 2014, Bangladesh, one of 11 countries in SEAR, adopted a national goal for measles elimination by 2018 (2,3). This report describes progress and challenges toward measles elimination in Bangladesh during 2000-2016. Estimated coverage with the first MCV dose (MCV1) increased from 74% in 2000 to 94% in 2016. The second MCV dose (MCV2) was introduced in 2012, and MCV2 coverage increased from 35% in 2013 to 93% in 2016. During 2000-2016, approximately 108.9 million children received MCV during three nationwide SIAs conducted in phases. During 2000-2016, reported confirmed measles incidence decreased 82%, from 34.2 to 6.1 per million population. However, in 2016, 56% of districts did not meet the surveillance performance target of ≥2 discarded nonmeasles, nonrubella cases§ per 100,000 population. Additional measures that include increasing MCV1 and MCV2 coverage to ≥95% in all districts with additional strategies for hard-to-reach populations, increasing sensitivity of measles case-based surveillance, and ensuring timely transport of specimens to the national laboratory will help achieve measles elimination.


Immunization Activities
In Bangladesh, MCV1, administered at age 9 months, was introduced nationwide ¶ in 1989 (4), and MCV2, administered at age 15 months, in 2012.Administrative vaccination coverage** data are reported each year from the 64 districts in Bangladesh to the National Immunization Programme, where they are aggregated and reported to WHO and UNICEF through the Joint Reporting Form (JRF).WHO and UNICEF use reported administrative coverage and available survey results to generate annual estimates of vaccination coverage through routine services (5).As noted previously, in Bangladesh estimated coverage for MCV1 and MCV2 increased significantly (Figure).A routine vaccination coverage survey † † implemented in 2015 estimated 92% national coverage for MCV1 and 81% for MCV2.

Surveillance Activities and Measles Incidence
In 2003, laboratory-supported case-based surveillance for suspected measles § § was implemented in Bangladesh by adapting the existing acute flaccid paralysis surveillance system for polio detection; data are provided from 143 active and 625 passive surveillance sites in all 64 districts.In addition, aggregated measles cases ¶ ¶ are reported by all health facilities through the National Health Management Information System and have been reported annually through the JRF since 2000.The difference in number of cases reported annually by these two parallel systems has decreased since 2013 (Table 1).Measles virus genotyping began in Bangladesh in 2014.§ § In Bangladesh, a suspected measles case is defined as an illness in any person a clinician suspects of having measles infection, or in any person with fever and maculopapular rash and cough, coryza, or conjunctivitis.¶ ¶ National measles case data are reported to WHO South-East Asia Region Office) through the World Health Organization/UNICEF Joint Reporting Form (JRF) aggregate reporting annually.Bangladesh uses administrative data reported through the national Health Management Information system (HMIS) to report in the JRF.The HMIS receives aggregated data from all the health facilities in the country, including private and public clinics and hospitals.
During 2013-2016, years for which data on key surveillance performance indicators*** (7) were available, the discarded nonmeasles, nonrubella rate increased nationally from 1.1 to 1.9 per 100,000 population; percentage of districts reporting at least two discarded nonmeasles, nonrubella cases per 100,000 population increased from 19% to 44%; percentage of suspected cases with adequate investigation initiated within 48 hours of notification increased from 87% to 94%; and the percentage of serology results reported by the laboratory within 4 days of specimen receipt increased from 82% to 94% (Table 2).
During 2000-2016, incidence of measles cases reported through the JRF decreased 84%, from 40.0 to 6.0 per million *** Key surveillance performance indicators include 1) ≥2 discarded nonmeasles, nonrubella cases per 100,000 population at the national level per year; 2) ≥2 discarded nonmeasles, nonrubella cases per 100,000 per year in ≥80% of subnational administrative units; 3) an adequate investigation conducted within 48 hours of notification for ≥80% of suspected measles cases; 4) adequate specimens for detecting acute measles and rubella infection collected and tested in a proficient laboratory from ≥80% of suspected cases; 5) receipt of ≥80% of specimens at the laboratory within 5 days of collection; 6) laboratory reporting of ≥80% of serology results 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.
* Measles incidence calculated based on reported confirmed measles cases and population by countries through WHO/UNICEF JRF.† National measles case data as reported to WHO South-East Asia Region Office (SEARO) as of December 2015 through the WHO/UNICEF JRF.Bangladesh uses administrative data reported through the national Health Management Information system (HMIS) to report in the JRF.The HMIS receives aggregated data from all the health facilities in the country, including private and public clinics and hospitals.§ Data from case-based measles surveillance through the Vaccine Preventable Diseases surveillance network reported to WHO SEARO as of December 2016.¶ An illness in any person a clinician suspects of having measles infection or in any person with fever and maculopapular rash and cough, coryza, or conjunctivitis.** Includes laboratory-confirmed and epidemiologically linked cases.An epidemiologically linked case is one that meets the clinical case definition and is linked epidemiologically to a laboratory-confirmed or another epidemiologically confirmed case.

Discussion
During 2000-2016, after increasing MCV1 and MCV2 coverage and three SIAs, confirmed measles incidence in Bangladesh decreased 84% (9).In 2016, however, an outbreak occurred, and transmission has continued into 2017, revealing gaps in both RI and SIA coverage.The national vaccination * An illness in any person a clinician suspects of having measles infection, or in any person with fever and maculopapular rash and cough, coryza, or conjunctivitis.† Includes collection of all the following data elements about each suspected case of measles or rubella: 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-rubella vaccination status, date of last measles-rubella or measles-mumps-rubella vaccination, date of notification, date of investigation, and travel history.§ A blood specimen collected within 28 days of the onset of rash.coverage survey conducted in 2015 found the following most common reasons for a child being unvaccinated or partially vaccinated: 1) caretakers were too busy with other priorities, 2) caretakers did not remember to bring the child for vaccination, and 3) lack of information about when to bring the child for vaccination.These findings indicated the need for intensified social mobilization activities to strengthen RI, and a communication campaign is planned for 2017-2018.
In 2003, laboratory-supported measles case-based surveillance was implemented in Bangladesh by adapting the existing acute flaccid paralysis surveillance system for polio detection.Measles case-based surveillance indicators reflected underreporting and low sensitivity of the suspected measles case definition.Case-based surveillance sensitivity could be increased by expanding case-based surveillance reporting sites from acute flaccid paralysis reporting units to all health facilities in the country and by using the broad definition of "fever and maculopapular rash" (10).In addition, specimens for genotyping need to be collected from more chains of transmission to better track transmission pathways and identify outbreak sources.mitigation plans, conduct an immediate nationwide follow-up measles-rubella SIA to address current immunity gap among children aged 9-59 months, and build capacity for epidemiologic investigations and outbreak preparedness and response to rapidly identify and contain outbreaks.

FIGURE.
FIGURE.Aggregated measles cases,* estimated coverage † with the first and second dose of measles-containing vaccine (MCV1 and MCV2), and supplementary immunization activities (SIAs) §, ¶, ** , † † -Vaccine Preventable Disease Surveillance Report, Bangladesh, 1980-2016 ¶ A World Health Organization (WHO)-accredited laboratory that has an established quality assurance program or one with oversight by a WHOaccredited laboratory.** Changed to 4 days from 7 day in 2015.