Progress Toward Measles Elimination in the Eastern Mediterranean Region

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S U P P L E M E N T A R T I C L E

Progress Toward Measles Elimination in the

Eastern Mediterranean Region

Boubker Naouri,1_{Hinda Ahmed,}1_{Raef Bekhit,}1_{Nadia Teleb,}1_{Ezzeddine Mohsni,}2_{and James P. Alexander Jr.}3 1_{Vaccine Preventable Diseases and Immunization and}2_{Disease Surveillance, Eradication and Elimination, Regional Office for the Eastern Mediterranean,}

World Health Organization, Cairo, Egypt; and3_{Global Immunization Division, National Center for Immunization and Respiratory Diseases, Centers for Disease}

Control and Prevention, Atlanta, Georgia

Since 1997, when the goal of interrupting measles transmission by 2010 was adopted, substantial progress has been made toward the elimination of measles in the Eastern Mediterranean Region (EMR). For the 22 EMR member countries, routine coverage with the first dose of a measles-containing vaccine (MCV) increased from 70% in 1997 to 82% in 2009. All 22 countries conducted measles catch-up vaccination campaigns during 1994–2009, and most conducted follow-up campaigns as needed. Of the 22 EMR countries, 19 have established case-based surveillance for measles with laboratory confirmation. Reported measles cases decreased by 86% during 1998–2008, and estimated measles mortality decreased by 93% during 2000–2008, accounting for 17% of global measles mortality reduction during that period. Despite these successes, several significant challenges remain, and the EMR will not be able to achieve measles elimination by the end of 2010. Achieving and maintaining high population immunity with 2 doses of MCV, improving sensitive case-based surveillance, identifying and vaccinating high-risk subpopulation groups, and appropriately responding to outbreaks are key steps needed to achieve the goal.

The Eastern Mediterranean Region (EMR) of the World Health Organization (WHO) includes 22 countries that stretch from Morocco in the west to Pakistan in the east and are home to.550 million people (for this report, the geographic regions West Bank and Gaza Strip are considered to constitute 1 of the 22 countries of the region). There is a wide variation in the gross national product (GNP) per capita among the countries of the region, ranging from a low of US$ 160 for Afghanistan to a high of US$ 28,270 for Qatar. Five countries (Af-ghanistan, Djibouti, Somalia, Sudan, and Yemen) are among the least developed countries in the world [1]. The geopolitical situation of the Region is complex:

several countries are in a state of crisis and conflict or have experienced natural disasters, including Afghani-stan, Iraq, PakiAfghani-stan, West Bank and Gaza Strip, Somalia, Sudan and Yemen. Providing emergency medical assis-tance and technical support to these countries has been a challenging undertaking for the WHO Regional Office for the Eastern Mediterranean (EMRO).

In 1997, the 22 EMR member countries resolved to eliminate measles from the region by 2010, defined as the absence of endemic measles cases in a defined geo-graphical area for.12 months in the presence of a well-performing surveillance system. (One measure suggest-ing measles elimination is a sustained measles incidence of,1 case per 1 million population confirmed by lab-oratory or epidemiological linkage [excluding clinically compatible and imported cases].) Key strategies for achieving measles elimination in the region included (1) achieving and maintainingR90% vaccination coverage of children with the first dose of measles-containing vaccine (MCV1) in every district of each country through routine immunization services, (2) achieving R_{90% vaccination coverage with a second dose of} a measles-containing vaccine (MCV2) in every district either through a routine 2-dose vaccination schedule or through supplemental immunization activities (SIAs),

Potential conflicts of interest: none reported.

Supplement sponsorship: This article is part of a supplement entitled "Global Progress Toward Measles Eradication and Prevention of Rubella and Congenital Rubella Syndrome," which was sponsored by the Centers for Disease Control and Prevention.

Correspondence: James P. Alexander, Jr, MD, Centers for Disease Control and Prevention, 1600 Clifton Rd, NE, Mailstop E-05, Atlanta, Georgia 30333 (axj1@cdc.gov).

The Journal of Infectious Diseases 2011;204:S289–S298

Published by Oxford University Press on behalf of the Infectious Diseases Society of America 2011.

0022-1899 (print)/1537-6613 (online)/2011/204S1-0037$14.00 DOI: 10.1093/infdis/jir140

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(3) establishing high-quality case-based surveillance with in-vestigation and laboratory testing in a proficient measles labo-ratory of all suspected cases of measles, and (4) providing optimal clinical-case management, including supplementation of diets with vitamin A [2]. In 1999, the EMRO developed a 5-year plan for measles elimination based on the joint WHO– United Nations Children’s Fund (UNICEF) strategy for measles mortality reduction. A second plan was developed for the period 2006–2010 [3].

Significant progress has been made in the EMR toward measles elimination, through increasing coverage with a routine MCV1 and implementation of catch-up and follow-up measles SIAs in EMR countries. The number of confirmed measles cases has decreased dramatically from 89,518 in 1998 to 12,186 in 2008 (86% decrease), and the EMR achieved a 93% reduction in estimated measles mortality during 2000–2008—the largest percentage reduction among all WHO regions, accounting for 17% of the global reduction in measles mortality [4]. Despite these successes, in recent years, there has been a resurgence of measles virus circulation and outbreaks in a number of coun-tries, including a nationwide epidemic in Iraq during 2008– 2009. Although several countries are near elimination, the EMR as a whole will not reach the goal of measles elimination by 2010, based on current levels of measles control. In this article, we summarize the impact of measles elimination strategies on the interruption of measles transmission in the EMR during the period 1990–2009 and the challenges that remain to reach the goal.

METHODS

Vaccination Strategy and Coverage

On the basis of WHO recommendations, MCV1 has been ad-ministered in the EMR to children at 9 months of age in countries with high measles incidence and to children 12 months of age in countries with low measles incidence and a low risk of measles infection among infants [5]. To interrupt the transmission of measles, EMRO recommended in 1997 that all countries conduct an initial SIA (catch-up campaign) against measles, targeting all children 9 months–14 years of age and to add MCV2 to the routine immunization schedule in those countries that achieved .80% MCV1 coverage for 3 years consecutively. On the basis of the experience in the Americas, EMRO recommended that countries unable to meet this crite-rion continue to increase MCV1 coverage and conduct addi-tional measles SIAs (follow-up campaigns) at appropriate intervals, usually every 2–4 years [6].

As of 2009, MCV1 is administered at age 9 months in 8 (36%) of the EMR countries and at age 12–15 months in the remaining 14 (64%) countries (Table 1). Nineteen (86%) countries have a routine 2-dose measles vaccination schedule; MCV2 is ad-ministered at 12–23 months, 15–18 months, and 4–6 years in 1

(5%), 9 (47%), and 9 (47%) of the 2-dose countries, re-spectively. Twelve (55%) countries in the region use a combined measles, mumps and rubella (MMR) vaccine for MCV1, and 14 (64%) use MMR for MCV2. Five countries have a 3-dose measles vaccine schedule, including a dose of monovalent measles vaccine at 9 months, because of either recent outbreaks affecting infants or transition from a 9-month to a 12-month MCV1 schedule. Vaccination coverage with MCV1 and MCV2 is calculated annually for each country by dividing the total number of doses administered to children in the targeted age group by the estimated population of children in that age group based on the most recent census (the administrative method). In addition, the WHO and UNICEF estimate coverage of MCV1 annually for each country using reported coverage of MCV1, survey results, and other information [7].

The 22 EMR countries conducted measles or combined measles-rubella SIAs during 1994–2009, the last of which oc-curred in Iraq in December 2009 (Table 2). All countries con-ducted catch-up SIAs, generally targeting children aged 9 months–14 years, to rapidly interrupt measles transmission. Many countries conductedR_{1 follow-up measles SIAs,} gener-ally targeting children aged 9–59 months, to prevent the build-up of susceptible children and reduce the risk of outbreaks. As needed, countries conducted smaller-scale, focused immuniza-tion campaigns in high-risk areas, often in response to measles case-clusters, or larger-scale campaigns in response to outbreaks [8]. Vaccination coverage for SIAs is calculated by dividing the total number of doses administered to children in the targeted age group by the estimated population of children in that age group. Some countries also conducted vaccination coverage surveys to independently assess the coverage of SIAs.

Disease Surveillance

After completion of initial catch-up campaigns, measles sur-veillance was intensified in all countries in the EMR. Since 2006, 19 (86%) 22 countries in the region have conducted case-based surveillance (CBS). Of the 3 countries without CBS, Morocco and Pakistan have sentinel surveillance for measles with labo-ratory confirmation of cases identified at sentinel sites, and Somalia is initiating sentinel site surveillance for measles. Standard WHO definitions are used for surveillance; confir-mation of measles is made by clinical diagnosis, epidemiologic linking, or laboratory testing [9]. In countries with CBS, a thorough investigation of each suspected measles case is done, with collection of clinical and epidemiologic data on an in-dividual case-reporting form, collection of serum for detection of measles-specific immunoglobulin M (IgM) antibodies, and collection of serum or other specimens for virus isolation [10]. By 2006, all countries were reporting measles and rubella data to EMRO on a monthly basis, and all countries have demonstrated significant improvement in management and sharing of measles surveillance and laboratory data during the past few years. In the

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absence of a routine surveillance system for measles-related deaths, the WHO uses a model to estimate measles-associated mortality based on measles case counts (corrected for a certain level of underreporting), estimated case-fatality rates, and esti-mated vaccination coverage [11].

In 2006, the WHO’s Technical Advisory Group on Immuni-zation in the EMR recommended monitoring surveillance per-formance, using standard indicators and targets. These standards include ensuring that (1) R _{2 non-measles suspected measles} cases per 100,000 persons are detected and reported (to monitor the sensitivity of the surveillance system), (2)R_{80% of suspected} cases have adequate investigation (ie, investigation conducted within 48 h after notification that includes all essential data ele-ments), (3) R80% of suspected measles cases are tested for measles IgM antibody (to monitor adequacy of testing), (4) R_{80% of specimens are received by a laboratory within 7 days} after collection (to monitor timeliness of specimen trans-portation), (5)R_{80% of specimens sent to the laboratory arrive} in good condition (to monitor adequacy of specimen collection),

and (6)R80% of laboratory test results are reported within 7 days after receipt in the laboratory (to monitor timely reporting). Rubella surveillance is integrated with measles surveillance, be-cause most countries use the febrile rash illness definition for suspect measles cases and perform laboratory testing for both measles-specific and rubella-specific IgM antibodies.

Laboratory Surveillance

The EMR Measles and Rubella Laboratory Network (LabNet) was initiated in 2002 to support measles and rubella surveillance, and it became fully functional in all EMR countries in 2006. The LabNet is composed of 22 national laboratories and 2 Regional Reference Laboratories (RRLs), one each in Oman and Tunisia. EMRO provides funding support to ensure that the LabNet has adequate supplies and equipment.

National laboratories perform confirmatory testing of serum specimens from suspected measles cases using validated enzyme-linked immunosorbent assays (ELISAs) to detect measles im-munoglobulin M (IgM) antibodies and, if negative, to test for Table 1. Recommended 2009 Routine Measles VaccineaSchedules and Percentage of Children Who Received Their First Dose of Measles Vaccineb, by Country/Area – World Health Organization (WHO) Eastern Mediterranean Region, 1997–2009

Country/Area Age at first dose Age at second dose

Coverage, %

1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009

Afghanistan 9 mosc _{18 mos}c ₄₈ ₄₀ ₄₀ ₃₅ ₄₇ ₄₄ ₅₀ ₆₁ ₆₄ ₆₈ ₇₀ ₇₅ ₇₆d

Bahrain 12 mos 5 yrs 94 99 94 98 98 99 99 99 99 99 99 99 99

Djibouti 9 mosc _None ₃₁ ₂₁ ₂₃ ₅₀ ₄₉ ₆₂ ₆₆ ₆₀ ₆₅ ₆₇ ₇₄ ₇₃ ₇₃d

Egypt 12 mos 18 mos 92 98 96 98 97 97 98 97 98 98 97 92 95

Iran 12 mos 18 mos 95 99 99 99 96 99 99 96 94 99 97 98 99

Iraqe _{15 mos}c _{4-6 yrs} ₈₅ ₈₈ ₉₀ ₈₇ ₈₃ ₈₀ ₇₆ ₇₃ ₆₉ ₆₉ ₆₉ ₆₉ ₆₉d

Jordane _{12 mos} _{18 mos} ₉₅ ₉₃ ₈₃ ₉₄ ₉₉ ₉₅ ₉₆ ₉₉ ₉₅ ₉₉ ₉₅ ₉₅ ₉₅

Kuwait 12 mos 4-6 yrs 95 99 96 99 99 97 97 97 97 97 97 97 97

Lebanone 12 mos 4-6 yrs 89 83 77 71 65 59 53 53 53 53 53 53 53d

Libya 12 mos 18 mos 91 92 92 93 93 91 96 99 97 98 98 98 98

Morocco 9 mosc 6 yrsc 92 91 90 93 96 94 90 95 97 95 95 96 98

Oman 12 mos 18 mos 98 98 99 99 99 99 98 98 98 96 97 97 97

Pakistan 9 mosc 12-23 mosc 52 54 56 59 61 63 61 67 78 80 80 85 80d

West Bank and Gaza Strip 12 mos 18 mos 96 94 91 93 98 94 100 98 99 99 100 96 97

Qatar 12 mos 4-6 yrs 87 89 87 91 92 99 93 99 99 99 92 96 99

Saudi Arabiae _{12 mos} _{4-6 yrs} ₉₂ ₉₃ ₉₂ ₉₄ ₉₄ ₉₇ ₉₆ ₉₇ ₉₇ ₉₅ ₉₆ ₉₇ ₉₈

Somalia 9 mosc _None ₂₅ ₃₂ ₃₈ ₃₅ ₃₅ ₄₅ ₄₀ ₄₀ ₃₅ ₃₅ ₃₄ ₂₄ ₂₄d

Sudanf _{9 mos}c _None ₅₈ ₄₉ ₅₁ ₅₈ ₅₈ ₅₈ ₆₅ ₆₇ ₆₉ ₇₃ ₇₉ ₇₉ ₈₂d

Syria 12 mos 18 mos 84 84 83 83 83 82 82 81 81 81 81 81 81d

Tunisia 15 mosc _{6 yrs}c ₉₂ ₉₄ ₉₀ ₉₅ ₉₂ ₉₄ ₉₀ ₉₅ ₉₆ ₉₈ ₉₈ ₉₈ ₉₈

United Arab Emiratese _{15 mos} _{6 yrs} ₉₅ ₉₅ ₉₆ ₉₄ ₉₄ ₉₄ ₉₄ ₉₄ ₉₂ ₉₂ ₉₂ ₉₂ ₉₂

Yemen 9 mosc _{18 mos}c ₄₁ ₅₈ ₆₆ ₆₂ ₆₄ ₅₄ ₅₆ ₆₅ ₆₅ ₅₇ ₆₃ ₆₂ ₅₈d

Region overall 70 72 73 73 74 75 75 77 81 82 82 83 82d

NOTE.a

A combined measles, mumps and rubella (MMR) vaccine is used except where noted.

b

By age 12 months or later if first dose was scheduled after age 12 months. Data are from WHO and United Nations Children Fund (UNICEF) estimates.

c

Single-antigen measles vaccine used, except Morocco, where 2nd dose vaccine is a combined measles-rubella vaccine.

d

Vaccination coverage was below the regional goal of 90% in 2009.

e

Country has a 3-dose measles vaccination schedule, including a dose of monovalent measles vaccine given at 9 months of age.

f

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Table 2. Measles Supplementary Immunization Activities (SIAs), by Country/Area, Target Age Group, Type of SIA, and Number and Percentage of Targeted Children Vaccinated – World Health Organization (WHO) Eastern Mediterranean Region, 1994–2009

Country/Area

No. and % of targeted children vaccinated

Year Target age group Type of SIA No. %a

Afghanistan 1999 9–23 mos High-risk area 74,588 53

2002 6 mos–14 yrs Catch-up 8,791,532 74

2003 9–59 mos Follow-up 5,338,285 96

2006 9–59 mos Follow-up phase 1 1,064,000 109

2009 9–36 mos Follow-up phase 1 702,047 118

2009 9–36 mos Follow-up phase 3 646,455 95

Bahrain 1998 6–18 yrs Catch-up phase 1 127,092 97

1999 1–7 yrs Catch-up phase 2 63,000 90

Djbouti 2002 9–59 mos Follow-up 72,854 80

2003 9–59 mos Follow-up 77,854 83

2006 9 mos–15 yrs Catch-up 186,317 85

2007 9–59 mos High-risk area 7,475 37

2008 9 mos–15 yrs Catch-up 184,638 86

Egypt 1998 9–59 mos High-risk area 1,864,549 99

2001 6–11 yrs Catch-up phase 1 5,616,000 78

Iran 1997 9 mos–14 yrs High-risk area 6,518,295 99

2003 5–25 yrs Catch-up 33,527,337 102

2007 1–5 yrs Follow-up 310,859 99

Iraq 1995 9–59 mos High-risk area 2,388,439 74

2002 9–59 mos Catch-up phase 1 3,619,402 99

2004 6 yrs Catch-up 862,848 93

2004 9 mos–7 yrs High-risk area 37,688 103

2005 12–59 mos Follow-up 2,650,000 98

2005 12–59 mos Follow-up 900,000 96

2007 12–59 mos Follow-up 3,560,538 92

2009 9-59 mos Follow-up 659,793 94

2009 6 mos–12 yrs Follow-up 10,965,289 91

Jordan 1997 6–15 yrs Catch-up 1,090,250 99

1999 4–6 yrs Catch-up 251,581 63

2005 8–16 yrs Catch-up 175,291 87

Kuwait 1994 6–18 yrs Catch-up 295,239 94

1998 6–11 yrs Follow-up 154,814 93

2007 1–7 yrs High-risk area 38,930 94

Lebanon 2000 1–15 yrs Catch-up 1,059,873 93

2008 9 mos–15 yrs Catch-up 705,117 77

Libya 2005 9 mos–20 yrs Catch-up 2,695,000 98

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Table 2. (Continued)

Country/Area

Morocco 2008 9 mos–14 yrs Catch-up 4,665,375 99

Oman 1994 9 mos–18 yrs Catch-up 705,000 94

Pakistan 2005 12–59 mos High-risk area 1,232,000 77

2007 9 mos–15 yrs Catch-up phase 1 2,511,837 98

West Bank and Gaza 2000 2–15 yrs High-risk area 17,804 89

2004 2–15 yrs Catch-up 415,000 98

Qatar 2000 6–16 yrs Catch-up 80,065 94

2005 9 mos–15 yrs Catch-up 319,321 83

2007 12–59 mos Follow-up 32,437 93

Saudi Arabia 1998 13–19 yrs Catch-up phase 1 1,629,565 96

2004 6–8 yrs Follow-up 1,079,431 97

2007 9 mos–18 yrs Catch-up 6,886,937 98

Somalia 2005 9 mos–15 yrs Catch-up phase 1 319,321 83

2008–09 9–59 mos Follow-up phase 1b _250,087 ₆₆

2009 9–59 mos Follow-up phase 1b _352,622 ₉₀

2009 9–59 mos Follow-up phase 1b _214,864 ₈₇

2009 9–59 mos Follow-up phase 1b _119,171 ₈₂

2009 9–59 mos Follow-up phase 2b 276,994 73

Sudan 1998 9 mos–15 yrs High-risk area 115,200 48

2007 9 mos–5 yrs Follow-up phase 1 1,491,612 96

2008 9 mos–5 yrs Follow-up phase 2 2,728,011 97

Southern Sudan 2003 6 mos–14 yrs Catch-up 1,495,743 94

2004 6 mos–14 yrs Catch-up 385,322 69

2005 6 mos–14 yrs Catch-up phase 1 362,577 76

2008 6 mos–14 yrs Catch-up phase 4 132,282 66

Syria 1998 9 mos–15 yrs Catch-up 6,636,752 99

2004 9–12 yrs High-risk area 324,462 85

Tunisia 1998 7–16 yrs Catch-up 1,754,239 95

2001 9 mos–5 yrs Follow-up 514,900 94

2002 6 mos–5 yrs Follow-up 126,412 99

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rubella IgM antibodies. Participating laboratories are required to report results to the Expanded Program on Immunization (EPI) within 7 days after receipt of specimen in the laboratory. Staff in all 22 national laboratories have been trained in measles and rubella serological testing, participate in global annual pro-ficiency panel testing, and undergo periodic accreditation using a WHO standardized checklist, to review their performance activities, timeliness, and quality indicators. To improve viro-logic surveillance, 17 (77%) of the 22 national laboratories re-ceived training during 2007–2009 in virus detection and molecular characterization. All 17 now have the capacity to do measles and rubella virus isolation or reverse-transcription-polymerase chain reaction (RT-PCR) testing.

The 2 national laboratories selected to serve as RRLs function as specialized diagnostic laboratories, performing virus isolation, virus detection by RT-PCR, and virus sequencing and geno-typing. They also provide quality control by validating IgM tests of the national laboratories and build capacity of the LabNet through training courses.

RESULTS

Vaccination Coverage

For the region overall, the estimated routine MCV1 coverage increased from 67% in 1990 to 82% in 2009 (Figure 1). During 1997–2009, routine MCV1 coverage was high and stable or in-creased in 17 (77%) countries and was low or dein-creased in 5 (23%) countries (Table 1). In 2009, 4 (18%) countries had MCV1 coverage,70% (range, 24%–69%), 5 (23%) countries had MCV1 coverage of 70%–89%; and 13 (59%) countries achieved a coverage of.90%. Of these 13 countries, 11 reported .90% MCV1 coverage in all districts. In the 19 countries with a routine 2-dose schedule, 12 (63%) reported MCV2 coverage .90% nationally in 2009.

During 1994–2009, nearly 300 million children in the EMR were vaccinated through SIAs (Table 2). The largest campaigns were conducted in Iran (33,527,337 persons 5-25 years vaccinated in 2003), Pakistan (66,582,317 children aged 9 months–14 years vac-cinated in 2007–08), Egypt (36,218,900 persons 2-20 years vacci-nated during 2008–09), and Iraq (10,965,289 children 6 months– 12 years old vaccinated in 2009). Six countries (Djibouti, Egypt, Lebanon, Saudi Arabia, Syria, and Tunisia) conducted repeat catch-up campaigns, either to achieve better immunity in the target population or because timely follow-up SIAs were not conducted and large measles outbreaks occurred. Vaccination coverage during initial catch-up campaigns, based on doses administered, was 69%–105% and, during all measles SIAs, was 37%–118%. Disease Surveillance

Before introduction of measles vaccination in the early 1980s,

200,000 clinically diagnosed cases of measles were reported each year in EMR countries [12]. After strengthening measles-control activities throughout the 1980s, reported cases decreased by 70% to 59,058 in 1990, and measles epidemics became smaller in size and the interval between them increased from 2–4 years during 1980–1991 to 5–6 years during 1992–2009 (Figure 1) [13]. Since setting the elimination goal, measles cases in the EMR decreased from 89,518 in 1998 to 12,186 in 2008, an 86% decrease, with a resulting decrease in the measles incidence rate from 188 to 21 confirmed measles cases per 1 million persons during 1998–2008, respectively (Figure 1). Six countries have reported measles incidence,1 case per million persons in the presence of a sensitive and well-functioning surveillance system: Bahrain, Iran, Jordan, West Bank and Gaza Strip, Syria, and Tunisia. Estimated measles mortality in the EMR decreased from 101,000 in 2000 to 7000 in 2008, a 93% decrease [4].

Despite the overall reduction in the number of confirmed measles cases, a number of countries in the region experienced Table 2. (Continued)

Country/Area

United Arab Emirates 1998 9–59 mos Catch-up phase 1 154,960 92

1999 12–18 yrs Catch-up phase 2 168,435 90

2001 9 mos–18 yrs Catch-up 893,000 94

Yemen 2001 12–59 mos Catch-up 2,205,453 94

2006 9 mos–15 yrs Catch-up 9,322,918 98

2007 9 mos–15 yrs High-risk area 1,291,206 91

2009 9–59 mos Follow-up 3,246,804 96

All countries 298,325,513

NOTE.a

The percentage of the population vaccinated may exceed 100% because of underestimation of the size of the target population.

b

Follow-up campaign conducted as part of ‘‘Child Health Days,’’ a campaign to deliver multiple vaccinations and interventions to infants, children and women of child-bearing age.

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large-scale measles outbreaks during 2005–2009. Despite the reported MCV1 coverage rates of .95%, a routine 2-dose schedule, and a catch-up SIA held during the preceding 8 years, measles outbreaks occurred in Lebanon (1947 cases; 2005– 2007), Syria (1295 cases; 2005–2007), Qatar (505 cases; 2006– 2007), Saudi Arabia (5455 cases; 2006–2007), and Egypt (3305 cases; 2006–2008). Large outbreaks also occurred in countries with a higher burden of measles because of incomplete im-plementation of elimination strategies or conflict and insecurity, including Morocco (4920 cases; 2006–2008), Somalia (2230 cases; 2007–2008), Afghanistan (4460 cases; 2008–2009), and Iraq (35,822 cases; 2008–2009).

The number of confirmed cases of measles reported to EMRO increased from 12,186 in 2008 to 36,737 in 2009, largely because of 30,328 confirmed cases in Iraq in 2009 (Of the 30,328 confirmed measles cases reported by Iraq in 2009, 8753 had detailed case investigations with collection of serum specimen for laboratory testing, whereas 21,570 were clinical cases of measles with epi-demiologic linkage to confirmed cases). Of the 15,866 confirmed measles cases with individual case information reported to EM-RO in 2009 (including 8753 of 30,328 cases in Iraq), 53% were male and 47% were female; 17% were,1 year of age, 40% were 1–4 years of age, 20% were 5–14 years of age, and 22% were.15 years of age. During 2009, 48% of these confirmed measles cases were unvaccinated. Of those who were vaccinated, 76% and 24% were vaccinated with 1 dose and.2 doses of MCV, respectively. During 2009, among the 19 countries conducting case-based surveillance, the suspected measles case reporting rate for the EMR was 2.19 cases per 100,000 persons. Nine (47%) of the 19 countries achieved the target reporting rate ofR2 cases per 100,000 persons.

Among the 19 countries, 8 (42%) achieved the target ofR_80% timely and complete case investigations, 16 (84%) achieved the target ofR_{80% suspected cases tested for measles IgM antibody,} and 13 (68%), 18 (95%), and 18 (95%) reached the R 80% targets for timely specimen transportation, adequate specimen collection, and prompt reporting of measles IgM test results, re-spectively. Three countries met all surveillance quality targets. Laboratory Surveillance

Since 2006, all countries have reported measles and rubella laboratory data to EMRO on a monthly basis. Serological testing for measles IgM has increased by 51% in the LabNet, from 6684 to 13,222 serum samples tested in 2006 and 2009, respectively (Table 3). The EMR LabNet has maintained its performance since 2006, obtaining scores.90% on the global annual pro-ficiency tests in all countries. All 22 national laboratories have undergone accreditation reviews, and 20 have passed by ful-filling accreditation criteria.

During 2001–2006, only a few EMR countries were con-ducting virologic surveillance for measles [14, 15]. As a result of training in virus detection and characterization during 2007– 2009, 17 (77%) of the 22 countries have now identified R₁ measles genotypes (B3, C2, D4, D5, D6, D7, D8, and H1), and all countries except one have submitted their measles genotypes to the WHO genotype database (Table 4). The predominant ge-notype in the EMR is D4, detected in 12 (71%) of 17 countries with identified genotypes; the second most frequently identified is B3, detected in 7 (41%) of these countries. In addition, multiple genotypes have been identified in some countries, such as Oman (D5 and D8 associated with endemic transmission and Figure 1. Number of reported measles casesa_{and estimated percentage of children who received their first dose of measles vaccine}b_{–World Health}

Organization (WHO) Eastern Mediterranean Region, 1990–2009.aConfirmed cases of measles reported to WHO and the United Nations Children's Fund (UNICEF) through the Joint Reporting Form Regional Office for the Eastern Mediterranean Region.b_{By age 12 months or later if the first dose was}

scheduled after age of 12 months. Data are from WHO and UNICEF estimates.cThis goal, to reduce measles mortality by 50% from 1999 to 2005, has been achieved.dThis goal is to reduce measles mortality by 90% from 2006 to 2010.

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B3 and D4 associated with importations) and Morocco (B3, C2, D4, D7, and D8, with C2 the most frequently identified and probable endemic strain) [16].

DISCUSSION

Substantial progress has been made toward measles elimination in the EMR. The global goal of 90% reduction in measles-associated mortality by 2010 was achieved in the region by 2007. Similarly, there was an 86% decrease in the number of con-firmed measles cases reported during 1998–2008, despite in-tensification of surveillance and case detection during this period. These reductions were the result of full implementation of the recommended regional measles elimination strategies by several countries and the result of efforts by all countries to

increase population immunity to measles and to develop sen-sitive surveillance and timely response for measles cases and outbreaks. These efforts were aided by a high political com-mitment at national and regional levels to accelerate measles elimination in the EMR.

EMR member countries have increased population immunity and reduced the burden of measles through 2 main strategies. Most countries have increased or maintained a high routine MCV1 coverage during the elimination phase. All countries have also provided a second dose of measles vaccine to all children, either through introduction of MCV2 into the routine immu-nization program or by conducting catch-up measles SIAs during 1994–2008. Many countries have also conducted peri-odic follow-up campaigns to prevent the build-up of susceptible persons in the population.

Table 3. Suspected Measles Cases, Serum Samples Tested for Measles and Rubella Immunoglobulin M (IgM) Antibodies, and Positive IgM Tests for Measles and Rubella – WHO Eastern Mediterranean Region, 2005–9

Year Suspected measles cases Samples tested Measles IgM1 Rubella IgM1

2005 15,070 6,636 1,438 711 2006 21,388 7,317 2,384 762 2007 32,282 16,054 4,872 1,012 2008 15,765 10,569 4,038 840 2009 19,812 13,222 4,695 569 Total 104,317 53,798 17,427 3,894

Table 4. Measles Genotypes Identified in the WHO Eastern Mediterranean Region and Reported to the WHO Genotype Database, 2007–2009

Country Genotype associated with endemic transmission Genotype associated with importation

Afghanistan D4 Bahrain D4 D4 Djibouti B3a Egypt D4 Iran D4 H1 Iraq D4 Jordan D4 Kuwait B3, D5, D8 Lebanon — Libya B3 Morocco C2 (interrupted), D8 D4 Oman D8, D5 B3, D4 Pakistan D4

West Bank & Gaza Strip —

Qatar D4 Saudi Arabia — Somalia — Sudan B3, D4 Syria D4 Tunisia B3

United Arab Emirates —

Yemen B3

NOTE.a

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In addition, enhanced measles surveillance has been success-fully implemented throughout the region, including the labora-tory investigation of suspected measles cases. By 2009, 19 (86%) countries had instituted nationwide measles case-based surveil-lance (CBS). The sensitivity of measles surveilsurveil-lance in the region is increasing, timeliness and completeness of investigations are improving, most cases investigated have serum specimens ob-tained for laboratory testing, and most specimens are being sent to national laboratories promptly and in good condition.

The EMR LabNet has made considerable progress since the period 2005–2006 in support of measles and rubella surveillance, by expanding and establishing a national measles and rubella laboratory in all countries in the region with full serologic testing capability. Laboratories are functioning at a high level of pro-ficiency, handling an increasing volume of specimens, and providing critical information on both measles and rubella cases. They meet performance indicators for measles case-based sur-veillance, including timeliness of reporting laboratory test results to the national EPI program and EMRO. During the past 3 years, the LabNet has increased its capacity in molecular tech-niques, quality control standards, and analysis and validation of results. In consequence, substantial progress has been made in identifying circulating measles genotypes in 17 EMR countries. Nonetheless, the region will not achieve a sustained measles incidence of,1 case per million population by the end of 2010. The number of measles cases and disease incidence decreased significantly from 1998 through 2008, but remains well above the elimination threshold. A number of countries have experienced outbreaks, both those with resource constraints and security challenges and also those with good resources and generally high-quality immunization programs. Iraq, in particular, experienced a large-scale outbreak during 2008–2009, accounting for.80% of the total regional measles cases in 2009, that resulted, in part, from decreasing population immunity over 5–6 years because of con-flict and insecurity in most areas of the country.

The EMR still faces several challenges to achieve measles elimination, including increasing population immunity to measles. Routine MCV1 coverage (82%) is still too low to achieve elimination, and although numerous SIAs have been conducted during the last 15 years, vaccination coverage has been variable and might have been overestimated for some campaigns. In some cases, follow-up SIAs were not done in a timely manner, and outbreaks occurred before population immunity could be boosted. In other instances, outbreaks have occurred in high-risk subpopulations, such as nomadic groups or communities bordering neighboring countries where measles is endemic or epidemic, despite overall high population im-munity. Countries have been most successful when they have conducted high-quality campaigns and achieved high coverage with routine MCV1 and MCV2 doses.

In addition, measles surveillance is still suboptimal in some EMR member countries and areas. In Pakistan and Morocco,

measles and rubella surveillance is conducted through sentinel surveillance. In Somalia and southern Sudan, measles surveillance is largely aggregate reporting, and the number of reported measles cases underestimates the true incidence of measles because many persons cannot seek medical attention and reporting of identified cases is incomplete at each level of the reporting system.

Some countries or areas in the EMR where the burden of measles remains high (notably Afghanistan, Iraq, Pakistan, Somalia, and southern Sudan) have major challenges in establishing comprehensive measles elimination activities be-cause of competing public health priorities, natural disasters, or civil unrest. Armed conflict and war present major challenges for measles elimination in several areas. Unpredictable mass pop-ulation movements and resettlements complicate the delivery of routine immunization services and planning of SIAs. Con-ducting SIAs in conflict settings and in areas with no local government requires establishing close linkages with the local community, establishing ‘‘days of tranquility’’ for vaccination activities during SIAs, and other special efforts to reach the target population. Even with these efforts, vaccination coverage during SIAs is often suboptimal. High-quality follow-up campaigns are needed in these countries to reduce the number of susceptible persons. Such campaigns will require considerable resources that usually must be provided by donors outside the country.

To achieve elimination of measles in the EMR, a number of activities will need to be developed or enhanced to fully implement the 4 strategies. First, member countries with low MCV1 coverage need to enhance their routine immunization programs to improve first-dose coverage as a foundation for population immunity. Second, it may be necessary for many, if not all, member countries to conduct follow-up SIAs every 3–4 years until elimination is achieved. Third, increased ef-forts are needed in both stable and conflict-affected member countries to target and reach high-risk populations (refu-gees, internally displaced persons, migrant workers and no-madic groups) with MCV1 and MCV2. Fourth, in-depth reviews of immunization services, including independent surveys of vaccination coverage and assessment of data quality, are needed to identify and correct programmatic shortfalls in those countries with high coverage of MCV1, a routine 2-dose schedule, and recently implemented SIAs that have experienced periodic outbreaks. Fifth, there is a need for increased communication and coordination be-tween member countries and EMRO to improve surveil-lance, epidemiological analysis, and outbreak response. Last, continued technical and financial support to low-income countries will be needed to interrupt measles transmission and prevent outbreaks.

Achieving, maintaining, and certifying measles elimina-tion in the EMR will be challenging and will require extensive surveillance and monitoring of performance. Laboratory-based surveillance for measles is a cornerstone of the

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elimination strategy to confirm measles infection in persons with suspect measles and to determine whether identified measles virus is indigenous or imported. Although consid-erable progress has been made in improving measles viro-logic surveillance, further efforts are needed to enhance molecular epidemiologic surveillance to document viral transmission pathways and confirm the interruption of en-demic measles virus circulation in the EMR.

Funding

This work was supported by the World Health Organization (to B. N., H. A., N. T., E. M., and R. B.) and Centers for Disease Control and Pre-vention (Dr Alexander).

Acknowledgments

We thank the ministries of health of Afghanistan, Bahrain, Djibouti, Egypt, Iran, Iraq, Jordan, Kuwait, Lebanon, Libya, Morocco, Oman, Pakistan, West Bank and Gaza Strip, Qatar, Saudi Arabia, Somalia, Sudan, Syria, Tunisia, United Arab Emirates, and Yemen and the health authorities of the Pales-tinian populations served by the United Nations Relief Works Agency.

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