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Measles Outbreaks and Progress Toward Measles Preelimination --- African Region, 2009--2010
In 2008, the World Health Organization (WHO) African Region (AFR) measles technical advisory group (TAG) recommended establishing a measles preelimination goal, to be achieved by the end of 2012. The goal sets the following targets for the 46 AFR countries: ≥98% reduction in estimated regional measles mortality compared with 2000; measles incidence of <5 cases per 1 million population per year nationally; >90% national measles-containing vaccine (MCV) first dose (MCV1) coverage and >80% MCV1 coverage in all districts; and ≥95% MCV coverage by supplementary immunization activities (SIAs) in all districts (1). The goal also sets surveillance performance targets of ≥2 cases of nonmeasles febrile rash illness per 100,000 population, ≥1 suspected measles cases investigated with blood specimens in ≥80% of districts, and routine reporting from all districts (1). In addition, introduction of a routine second MCV dose (MCV2) was recommended for countries meeting specific criteria for MCV1 coverage and measles surveillance (1,2). This report updates progress toward the preelimination goal during 2009--2010 and summarizes measles outbreaks occurring in AFR countries since 2008. Of the 46 AFR countries, 12 (26%) reported measles incidence of <5 cases per 1 million population during 2010, compared with 28 (61%) in 2008. Furthermore, 28 (61%) countries reported a laboratory-confirmed measles outbreak during 2009--2010 (3). The recent measles outbreaks highlight the need for renewed dedication by donors and governments to ensure that national multiyear vaccination plans, national budgetary line items, and financial commitments exist for routine immunization services and measles control activities.
Measles Vaccination Coverage
The 46 AFR countries* report routine vaccination coverage to the WHO Regional Office for Africa (AFRO) using the WHO and United Nations Children's Fund (UNICEF) Joint Reporting Form (JRF) (4). In addition, WHO and UNICEF publish MCV1 coverage estimates based on multiple data sources, including JRF reports and demographic surveys (5). As of 2010, MCV1 was administered routinely at age 9 months† in 43 countries, and MCV2 was included in the routine immunization program in seven countries (Algeria, Cape Verde, Lesotho, Mauritius, Seychelles, South Africa, and Swaziland).
During 2001--2008, reported MCV1 coverage increased from 55% to 79% in the region (6). In 2009, AFR MCV1 administrative coverage§ was 83%, based on the most recent JRF data; the WHO and UNICEF regional MCV1 coverage estimate was 69% (Figure 1). In 2009, four (9%) countries (Burkina Faso, Gambia, Mauritius, and Sao Tome and Principe) reported >80% MCV1 coverage in all districts. To interrupt endemic transmission of measles, mathematical models indicate that 93%--95% population immunity is needed (7). Since 1997, 41 (89%) countries (all except Algeria, Cape Verde, Mauritius, Sao Tome and Principe, and Seychelles) have conducted an SIA targeting children aged 9 months--14 years, and 43 (93%) countries (all except Algeria, Mauritius, and Seychelles) have conducted at least one SIA targeting children aged 9--59 months. A nationwide SIA was conducted in 31 (67%) countries during 2009--2010 (Table); of these countries, five (16%) (Ethiopia, Ghana, Malawi, Zambia, and Zimbabwe) conducted post-SIA vaccination coverage surveys.
Data on suspected measles cases are tallied monthly at local health facilities, reported to the district level, aggregated at the national level, and annually reported to AFRO using the JRF (8). JRF data on 2010 suspected measles cases were not yet available; thus, 2010 measles case-based surveillance data reported to AFRO by 40 (87%) countries, in accordance with WHO AFRO measles surveillance guidelines, are cited instead (8). During 2001--2008, reported measles cases in AFR decreased by 93%, and estimated measles-related mortality declined 91% (2). The number of reported measles cases decreased from 520,102 in 2000 to 37,162 in 2008, then increased to 83,464 in 2009 and to 172,824 in 2010 (Figure 1). Of 172,824 reported cases, 23,842 (14%) were laboratory confirmed and 109,570 (63%) were confirmed through epidemiologic link¶ (3). During 2010, 25 (63%) countries met the nonmeasles febrile rash illness reporting target of ≥2 cases per 100,000 population and 29 (73%) had ≥80% of districts reporting ≥1 suspected cases with blood specimen. The overall confirmed measles incidence for the region in 2010 was 17.2 per 100,000 population and 12 (30%) countries reported measles incidence of <5 cases per 1 million population (Figure 2).
During 2009 and 2010, B3 measles virus was detected in all 25 countries with genotype information and was the predominant genotype in the region. In addition to the B3 outbreak strain, Angola and Namibia reported transmission of the B2 genotype, and South Africa reported two additional genotypes: a D4 from a single case imported during the World Cup games in June 2010 and a D8 from a single case in 2009.
Major Outbreaks and Response Activities
During 2009--2010, a total of 28 (61%) of the 46 AFR countries had laboratory-confirmed measles outbreaks** with >100 reported measles cases, including 13 countries in 2009 and 15 additional countries in 2010 (Table), compared with nine (20%) countries in 2008. Of these 28 countries, 10 reported ≥90% MCV1 coverage in 2009, 15 had a follow-up SIA within 24 months before the outbreak, and all reported ≥90% SIA administrative coverage in the most recent measles SIA (Table). Of the 28 countries with reported outbreaks, 20 conducted an outbreak investigation and 14 implemented an outbreak response immunization (ORI) campaign or a nationwide SIA following the start of the outbreak.
In some AFRO countries, frequent outbreaks continued, suggesting that children were missed by routine vaccinations and by SIAs in recent years. Measles outbreaks in which the majority of cases involved children aged <5 years occurred in Angola, Democratic Republic of Congo, Ethiopia, Nigeria, and Sierra Leone. Ethiopia, for example, reported that MCV1 coverage increased from 59% in 2005 to 75% in 2009. The last nationwide measles SIA, conducted in three phases during 2007--2009, targeted children aged 9--59 months, with reported coverage of 98%, 92%, and 93%, respectively. The 2009 nonmeasles febrile rash illness rate was 2.4 per 100,000 population, and 87% of districts reported ≥1 suspected cases with blood specimen. In 2009, 1,176 suspected cases were reported, compared with 8,261 cases in 2010 in 93 of 96 administrative zones. Of the cases reported in 2010, a total of 4,182 (51%) were confirmed by either laboratory testing or epidemiologic link. Of the confirmed cases, 3,142 (75%) were among children aged <5 years, and 3,877 (93%) were among unvaccinated persons. In 2010, an ORI campaign was conducted in 54 districts of five zones, targeting children aged 6--59 months, with reported coverage >100%.
In AFRO countries with higher, but still suboptimal, MCV1 coverage and SIA implementation, the age distribution of measles cases shifted to include older children and young adults. A measles outbreak pattern in which the age distribution of measles cases included older children and young adults occurred in Burkina Faso, Malawi, Namibia, South Africa, and Zambia. In Malawi, for example, reported MCV1 coverage increased from 82% in 2005 to 92% in 2009; a nationwide SIA targeting children aged 9--59 months was implemented in both 2005 and 2008, each with >95% reported coverage. In 2009, the nonmeasles febrile rash illness rate was 3.8 per 100,000 and 96% of districts reported ≥1 suspected case with blood specimen. In 2010, 73,727 suspected measles cases were reported from 24 of 28 districts in Malawi. Among 35,366 patients reported during October 24, 2009--July 17, 2010, a total of 14,627 (41%) were aged <5 years, 11,391 (32%) were aged 5--14 years, and 9,348 (26%) were aged ≥15 years. An initial ORI campaign was conducted 3 months after the start of the outbreak in three districts targeting children aged 9--59 months. A second ORI campaign was conducted 5--6 months after the outbreak started in eight districts targeting children aged 6 months--14 years in affected schools and prisons with clusters of patients. In 2010, a nationwide SIA was implemented targeting children aged 6 months--14 years with >95% administrative coverage in 26 of 28 districts.
Reasons for nonvaccination identified through outbreak investigations during 2009--2010 included vaccine unavailability; strict adherence to the WHO open vial policy,†† leading to batching of children into infrequent vaccination sessions; and exclusion of children aged >12 months, who were considered ineligible for MCV1. In addition, unwillingness to receive vaccination was identified among certain religious groups in Zimbabwe, Botswana, Malawi, and South Africa.
Countries in the WHO African Region; Immunization and Vaccine Development Program, WHO Regional Office for Africa. Dept of Immunization, Vaccines, and Biologicals, WHO, Geneva, Switzerland. Global Immunization Div, National Center for Immunization and Respiratory Diseases, CDC.
During 2001--2008, AFR countries made remarkable progress in reducing measles mortality and morbidity by increasing MCV1 coverage and periodic SIAs (2). However, since reaching an historic low of 32,278 reported cases in 2008, a resurgence of measles led to multiple large outbreaks during 2009--2010, despite increases in reported MCV1 coverage, indicating the fragility of the progress (Figure 1). Suboptimal routine and SIA vaccination coverage led to an increasing number of susceptible persons over a prolonged period of low incidence, allowing some children to remain susceptible as they grew older. Outbreak cases occurring among older children and young adults suggest some progress in reducing measles incidence together with long-standing gaps in vaccination activities. In countries with large outbreaks occurring primarily among children aged <5 years, substantial numbers of children were missed by both routine vaccination and SIAs in recent years. In these countries, estimated MCV1 coverage remains suboptimal and reviews of vaccination services are needed to identify programmatic reasons for nonvaccination (9). Detailed outbreak investigations are recommended to describe the epidemiology of an outbreak, guide rapid ORI, and determine the likely cause of the outbreak (e.g., failure to vaccinate) (1).
The findings in this report are subject to at least two limitations. First, underreporting of measles cases and low sensitivity of measles case-based surveillance in some countries likely led to underestimates of measles incidence. Second, SIA administrative coverage >100% suggests inaccurate and inflated reported coverage (9).
Although post-SIA coverage surveys are recommended, only five of 31 countries implemented a post-SIA coverage survey during 2009--2010. Estimates of vaccination coverage from population-based coverage surveys are key inputs to determine the susceptibility profile of a population. In addition, reliable coverage estimates can help identify areas of low coverage so that program managers can better prioritize and more efficiently use resources. Even though AFR reported MCV coverage has increased continuously and the quality of measles surveillance has improved, subsequent measles outbreaks raise doubts concerning the accuracy and reliability of reported coverage and surveillance data. WHO-recommended methods for improving the accuracy of monitoring measles vaccination programs and post-SIA surveys to estimate coverage should be implemented routinely (1).
The 2009--2010 outbreaks highlight the need for full implementation of regional strategies, with an emphasis on improving vaccination coverage through routine immunization services and SIAs in every district, and introduction of MCV2 into routine immunization services in eligible countries (1). National immunization program policies and delivery systems should be reviewed to ensure access to the recommended 2 doses of MCV by all eligible children. Communication strategies should be identified to ensure vaccination acceptance and demand among all segments of the population. Renewed dedication by donors and governments is needed to ensure that national multiyear plans, budgetary line items, and financial commitments exist for routine immunization services and measles control activities.
- World Health Organization. Report of the second meeting of the African regional measles technical advisory group (TAG), recommendations. Addis Ababa, Ethiopia: World Health Organization, Regional Office for Africa; 2008. Available at http://www.afro.who.int/index.php?option=com_docman&task=doc_download&gid=3616. Accessed March 23, 2011.
- CDC. Progress toward measles control---African Region, 2001--2008. MMWR 2009;58:1036--41.
- World Health Organization. Case-based surveillance performance with lab confirmation: measles. Geneva, Switzerland: World Health Organization, Regional Office for Africa; 2009. Available at http://www.afro.who.int/index.php?option=com_content&view=article&id=1938:case-based-measles-surveillance-with-lab-confirmation-&catid=1974&Itemid=2734. Accessed March 24, 2011.
- World Health Organization. WHO/UNICEF joint reporting process. Geneva, Switzerland: World Health Organization; 2011. Available at http://www.who.int/immunization_monitoring/routine/joint_reporting/en/index.html. Accessed March 24, 2011.
- World Health Organization. Immunization surveillance, assessment and monitoring. Data, statistics and graphics by subject. Geneva, Switzerland: World Health Organization; 2011. Available at http://www.who.int/immunization_monitoring/data/data_subject/en/index.html. Accessed March 24, 2011.
- World Health Organization. WHO vaccine-preventable diseases: monitoring system---2010 global summary. Geneva, Switzerland: World Health Organization; 2010. Available at http://www.who.int/immunization/documents/who_ivb_2010/en/index.html. Accessed March 24, 2011.
- World Health Organization. Measles vaccines: WHO position paper. Wkly Epidemiol Rec 2009;84:349--60.
- World Health Organization. Guidelines for measles surveillance. Geneva, Switzerland: World Health Organization, Regional Office for Africa; 2004. Available at http://www.afro.who.int/index.php?option=com_docman&task=doc_download&gid=3675. Accessed March 24, 2011.
- CDC. Global routine vaccination coverage, 2009. MMWR 2010;59:1367--71.
* AFR countries: Algeria, Angola, Benin, Botswana, Burkina Faso, Burundi, Cameroon, Cape Verde, Central African Republic, Chad, Comoros, Congo, Côte d'Ivoire, Democratic Republic of Congo, Equatorial Guinea, Eritrea, Ethiopia, Gabon, Gambia, Ghana, Guinea, Guinea-Bissau, Kenya, Lesotho, Liberia, Madagascar, Malawi, Mali, Mauritania, Mauritius, Mozambique, Namibia, Niger, Nigeria, Rwanda, Sao Tome and Principe, Senegal, Seychelles, Sierra Leone, South Africa, Swaziland, Togo, Uganda, United Republic of Tanzania, Zambia, and Zimbabwe.
† MCV1 is administered in Cape Verde, Mauritius, and Seychelles at ages 12--15 months.
§ Administrative coverage is the total number of doses given to the target population, divided by the estimated target population.
¶ A laboratory-confirmed case is confirmed by serology for measles-specific immunoglobulin M (IgM) antibody in a person who was not vaccinated in the previous 30 days. A case of measles is confirmed by epidemiologic linkage when linked in time and place to a laboratory-confirmed measles case in a district but lacks serologic confirmation (8).
** A measles outbreak is laboratory confirmed when 3 or more laboratory-confirmed measles IgM-positive cases occur in a health facility or district in a month (8).
†† The WHO policy requires that opened vials of MCV be discarded at the end of each immunization session or immediately if potentially contaminated. The policy is available at http://www.who.int/vaccines-documents/docspdf/www9403.pdf.
What is already known on this topic?
During 2001--2008, reported measles-containing vaccine first dose (MCV1) coverage increased from 55% to 79% in 46 African countries, reported measles cases decreased by 93%, and estimated measles-related mortality decreased 91%. By 2008, 40 of the 46 countries had established case-based surveillance in accordance with the World Health Organization guidelines, and 28 reported measles incidence <5 cases per 1 million population per year.
What is added by this report?
In 2009, reported MCV1 coverage among the 46 African countries was 83%; 12 (26%) countries had measles incidence of <5 cases per 1 million population in 2010, and 28 (61%) reported laboratory-confirmed measles outbreaks.
What are the implications for public health practice?
Despite substantial progress toward reducing measles mortality and morbidity, multiple outbreaks during 2009--2010 showed the gains were fragile, and epidemiologic investigations of some outbreaks showed a failure to vaccinate. The reasons for nonvaccination and corrective solutions need to be determined, the quality of reported data should be verified, and measles surveillance should be strengthened.
FIGURE 1. Number of reported measles cases* and coverage with the first dose of measles-containing vaccine (MCV1) in children aged <1 year† --- World Health Organization (WHO) African Region (AFR), 2000--2010§
* Confirmed cases of measles for 2000--2009 were reported by member states to WHO and the United Nations Children's Fund (UNICEF) through the Joint Reporting Form (JRF).
† Data are from WHO/UNICEF measles vaccination coverage estimates based on reviews of surveys and national reports of administrative coverage and adjusted for biases. Administrative coverage is calculated by dividing the number of doses administered by the total estimated number in the <1 year target population.
§ 2010 data are from monthly measles case-based surveillance reported to the WHO AFR Office; JRF data are not included.
Alternate Text: The figure above shows the number of reported measles cases and coverage with the first dose of measles-containing vaccine (MCV1) in children aged <1 year during 2000-2010, in the World Health Organization (WHO) African Region (AFR). In 2009, AFR MCV1 administrative coverage was 83%, based on the most recent WHO Joint Reporting Form data; the WHO and UNICEF regional MCV1 coverage estimate was 69%
* Confirmed measles incidence per 100,000 population; measles cases confirmed by laboratory testing or epidemiologic linkage.
Alternate Text: The figure above shows confirmed measles incidence in 2009 and 2010, for the World Health Organization (WHO) African Region. The overall confirmed measles incidence for the region in 2010 was 17.2 per 100,000 population and 12 (30%) countries reported measles incidence of <5 cases per 1 million population.
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