Vaccine 32 (2014) 1798–1807
Contents lists available at ScienceDirect
Vaccine journal homepage: www.elsevier.com/locate/vaccine
Measles resurgence in southern Africa: Challenges to measles elimination Messeret E. Shibeshi a , Balcha G. Masresha b , Sheilagh B. Smit c , Robin J. Biellik d , Jennifer L. Nicholson e , Charles Muitherero a , Nestor Shivute a , Oladapo Walker f , Katsande Reggis b , James L. Goodson g,∗ a
Immunization and Vaccines Development, East and South Africa Inter-Country Support Team, World Health Organization, Harare, Zimbabwe Immunization and Vaccines Development, African Regional Office, World Health Organization, Brazzaville, Congo c Measles and Rubella Regional Reference Laboratory, National Institute of Communicable Diseases, Johannesburg, South Africa d Consultant Epidemiologist, Geneva, Switzerland e Department of Epidemiology, Rollins School of Public Health and Laney Graduate School, Emory University, Atlanta, GA, United States f Immunization and Vaccines Development, West Africa Inter-Country Support Team, World Health Organization, Ouagadougou, Burkina Faso g Global Immunization Division, United States Centers for Disease Control and Prevention, Atlanta, GA, United States b
a r t i c l e
i n f o
Article history: Received 12 November 2013 Received in revised form 16 January 2014 Accepted 31 January 2014 Available online 13 February 2014 Keywords: Measles Elimination Africa Immunization Vaccination
a b s t r a c t Introduction: In seven southern African countries (Botswana, Lesotho, Malawi, Namibia, South Africa, Swaziland and Zimbabwe), following implementation of a measles mortality reduction strategy starting in 1996, the number of annually reported measles cases decreased sharply to less than one per million population during 2006–2008. However, during 2009–2010, large outbreaks occurred in these countries. In 2011, a goal for measles elimination by 2020 was set in the World Health Organization (WHO) African Region (AFR). We reviewed the implementation of the measles control strategy and measles epidemiology during the resurgence in the seven southern African countries. Methods: Estimated coverage with routine measles vaccination, supplemental immunization activities (SIA), annually reported measles cases by country, and measles surveillance and laboratory data were analyzed using descriptive analysis. Results: In the seven countries, coverage with the routine first dose of measles-containing vaccine (MCV1) decreased from 80% to 65% during 1996–2004, then increased to 84% in 2011; during 1996–2011, 79,696,523 people were reached with measles vaccination during 45 SIAs. Annually reported measles cases decreased from 61,160 cases to 60 cases and measles incidence decreased to 100% indicate that the intervention reached more persons than the estimated target population. c Planned SIA with expanded age group in response to the outbreak. d Target age in Opuwo district was ≥6 M. e ORI campaign in response to the outbreak.
Sequencher software (Gene Codes Corporation 4.1.4, Ann Arbor, MI) and phylogenetic and molecular evolutionary analyses were conducted using MEGA version 5 software using the maximum likelihood algorithm with bootstrap test of phylogeny relative to WHO measles virus reference strains [19]. 3. Results 3.1. Routine immunization During 1996–2011, MCV1 was recommended to be administered at nine months of age. MCV2 though routine services at 18 months of age was introduced in South Africa in 2000, Lesotho in 2001, Swaziland in 2002, and Botswana in 2011. During
1996–2011, WHO/UNICEF MCV1 coverage estimates increased in all seven countries, with absolute increases ranging from 2% in South Africa to 16% in Swaziland (Table 1). In 2011, MCV1 coverage estimates ranged from 74% in Namibia to 98% in Swaziland. The weighted average of MCV1 coverage estimates in the seven countries decreased from 80% to 65% during 1996–2004, then increased to 84% in 2011 (Fig. 1). Reports of MCV2 coverage began in South Africa in 2000, Lesotho in 2001, and Swaziland in 2002; the most recent available reported data for MCV2 coverage was 70% for Lesotho in 2009, 83% for South Africa in 2010, and 74% for Swaziland in 2010. In Botswana MCV2 was introduced in 2011; however, no reported coverage data was available. By 2012, MCV2 had not been introduced in Malawi, Namibia or Zimbabwe.
M.E. Shibeshi et al. / Vaccine 32 (2014) 1798–1807
1801
b
800 600
South Africa
c
a
400 200 0 800
1
5
9 13 17 21 25 29 33 37 41 45 49 1
5
9 13 17 21 25 29 33 37 41 45 49 1
5
9 13 17 21 25 29 33 37 41 45 49
Namibia e
d
600 400 200 0
1
5
9 13 17 21 25 29 33 37 41 45 49 1
5
800
9 13 17 21 25 29 33 37 41 45 49 1
5
9 13 17 21 25 29 33 37 41 45 49
Zimbabwe
f
600 400 200 0
1
5
9 13 17 21 25 29 33 37 41 45 49 1
5
9 13 17 21 25 29 33 37 41 45 49 1
5
800
9 13 17 21 25 29 33 37 41 45 49
Botswana
600
g
400 200 0
1
5
9 13 17 21 25 29 33 37 41 45 49 1
5
9 13 17 21 25 29 33 37 41 45 49 1
5
800
9 13 17 21 25 29 33 37 41 45 49
Lesotho
600 400
h
200 0 8,000 7,000 6,000 5,000 4,000 3,000 2,000 1,000 0
1
5
9 13 17 21 25 29 33 37 41 45 49 1
5
9 13 17 21 25 29 33 37 41 45 49 1
5
Malawi
i
1
5
9 13 17 21 25 29 33 37 41 45 49 1
5
9 13 17 21 25 29 33 37 41 45 49
9 13 17 21 25 29 33 37 41 45 49 1
5
800
9 13 17 21 25 29 33 37 41 45 49
Swaziland
600
j
400 200 0
1
5
9 13 17 21 25 29 33 37 41 45 49 1
5
9 13 17 21 25 29 33 37 41 45 49 1
5
9 13 17 21 25 29 33 37 41 45 49
Fig. 2. Confirmed* measles cases by epidemiological week, seven southern African countries, 2009 (N = 9546), 2010 (N = 111,186), and 2011 (N = 267). * Confirmed measles cases were defined by laboratory confirmation, epidemiological link, or classified as clinically compatible. Note: In 2009, 33 cases in Namibia had missing date data. In 2010, 23,548 cases in Malawi had missing date data. M: months, Y: years, ORI: Outbreak response immunization campaign, SIA: supplemental immunization activity. a Sub-national ORI campaign in response to the outbreak conducted in September–November 2009, target age 5–19Y, 77% coverage achieved. b Sub-national ORI campaign in response to the outbreak conducted in October–November 2009, target age 5–19Y, 88% coverage achieved. c National planned SIA with expanded age group in response to the outbreak conducted in May–July 2010, target age 6M–15Y, 98% coverage achieved.
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3.2. Supplemental immunization activities During 1996–2011, 45 nationwide or sub-national follow-up SIAs were implemented, including five each in Botswana, Lesotho, and Malawi, six each in Namibia, Swaziland, and Zimbabwe, and 12 in South Africa (Table 1). During the 45 SIAs, a total of 79,696,523 people received measles vaccination and reported coverage was ≥95% in 15 SIAs (34%), 90–94% in 13 SIAs (30%), 80–89% in 12 SIAs (27%), and
Contents lists available at ScienceDirect
Vaccine journal homepage: www.elsevier.com/locate/vaccine
Measles resurgence in southern Africa: Challenges to measles elimination Messeret E. Shibeshi a , Balcha G. Masresha b , Sheilagh B. Smit c , Robin J. Biellik d , Jennifer L. Nicholson e , Charles Muitherero a , Nestor Shivute a , Oladapo Walker f , Katsande Reggis b , James L. Goodson g,∗ a
Immunization and Vaccines Development, East and South Africa Inter-Country Support Team, World Health Organization, Harare, Zimbabwe Immunization and Vaccines Development, African Regional Office, World Health Organization, Brazzaville, Congo c Measles and Rubella Regional Reference Laboratory, National Institute of Communicable Diseases, Johannesburg, South Africa d Consultant Epidemiologist, Geneva, Switzerland e Department of Epidemiology, Rollins School of Public Health and Laney Graduate School, Emory University, Atlanta, GA, United States f Immunization and Vaccines Development, West Africa Inter-Country Support Team, World Health Organization, Ouagadougou, Burkina Faso g Global Immunization Division, United States Centers for Disease Control and Prevention, Atlanta, GA, United States b
a r t i c l e
i n f o
Article history: Received 12 November 2013 Received in revised form 16 January 2014 Accepted 31 January 2014 Available online 13 February 2014 Keywords: Measles Elimination Africa Immunization Vaccination
a b s t r a c t Introduction: In seven southern African countries (Botswana, Lesotho, Malawi, Namibia, South Africa, Swaziland and Zimbabwe), following implementation of a measles mortality reduction strategy starting in 1996, the number of annually reported measles cases decreased sharply to less than one per million population during 2006–2008. However, during 2009–2010, large outbreaks occurred in these countries. In 2011, a goal for measles elimination by 2020 was set in the World Health Organization (WHO) African Region (AFR). We reviewed the implementation of the measles control strategy and measles epidemiology during the resurgence in the seven southern African countries. Methods: Estimated coverage with routine measles vaccination, supplemental immunization activities (SIA), annually reported measles cases by country, and measles surveillance and laboratory data were analyzed using descriptive analysis. Results: In the seven countries, coverage with the routine first dose of measles-containing vaccine (MCV1) decreased from 80% to 65% during 1996–2004, then increased to 84% in 2011; during 1996–2011, 79,696,523 people were reached with measles vaccination during 45 SIAs. Annually reported measles cases decreased from 61,160 cases to 60 cases and measles incidence decreased to 100% indicate that the intervention reached more persons than the estimated target population. c Planned SIA with expanded age group in response to the outbreak. d Target age in Opuwo district was ≥6 M. e ORI campaign in response to the outbreak.
Sequencher software (Gene Codes Corporation 4.1.4, Ann Arbor, MI) and phylogenetic and molecular evolutionary analyses were conducted using MEGA version 5 software using the maximum likelihood algorithm with bootstrap test of phylogeny relative to WHO measles virus reference strains [19]. 3. Results 3.1. Routine immunization During 1996–2011, MCV1 was recommended to be administered at nine months of age. MCV2 though routine services at 18 months of age was introduced in South Africa in 2000, Lesotho in 2001, Swaziland in 2002, and Botswana in 2011. During
1996–2011, WHO/UNICEF MCV1 coverage estimates increased in all seven countries, with absolute increases ranging from 2% in South Africa to 16% in Swaziland (Table 1). In 2011, MCV1 coverage estimates ranged from 74% in Namibia to 98% in Swaziland. The weighted average of MCV1 coverage estimates in the seven countries decreased from 80% to 65% during 1996–2004, then increased to 84% in 2011 (Fig. 1). Reports of MCV2 coverage began in South Africa in 2000, Lesotho in 2001, and Swaziland in 2002; the most recent available reported data for MCV2 coverage was 70% for Lesotho in 2009, 83% for South Africa in 2010, and 74% for Swaziland in 2010. In Botswana MCV2 was introduced in 2011; however, no reported coverage data was available. By 2012, MCV2 had not been introduced in Malawi, Namibia or Zimbabwe.
M.E. Shibeshi et al. / Vaccine 32 (2014) 1798–1807
1801
b
800 600
South Africa
c
a
400 200 0 800
1
5
9 13 17 21 25 29 33 37 41 45 49 1
5
9 13 17 21 25 29 33 37 41 45 49 1
5
9 13 17 21 25 29 33 37 41 45 49
Namibia e
d
600 400 200 0
1
5
9 13 17 21 25 29 33 37 41 45 49 1
5
800
9 13 17 21 25 29 33 37 41 45 49 1
5
9 13 17 21 25 29 33 37 41 45 49
Zimbabwe
f
600 400 200 0
1
5
9 13 17 21 25 29 33 37 41 45 49 1
5
9 13 17 21 25 29 33 37 41 45 49 1
5
800
9 13 17 21 25 29 33 37 41 45 49
Botswana
600
g
400 200 0
1
5
9 13 17 21 25 29 33 37 41 45 49 1
5
9 13 17 21 25 29 33 37 41 45 49 1
5
800
9 13 17 21 25 29 33 37 41 45 49
Lesotho
600 400
h
200 0 8,000 7,000 6,000 5,000 4,000 3,000 2,000 1,000 0
1
5
9 13 17 21 25 29 33 37 41 45 49 1
5
9 13 17 21 25 29 33 37 41 45 49 1
5
Malawi
i
1
5
9 13 17 21 25 29 33 37 41 45 49 1
5
9 13 17 21 25 29 33 37 41 45 49
9 13 17 21 25 29 33 37 41 45 49 1
5
800
9 13 17 21 25 29 33 37 41 45 49
Swaziland
600
j
400 200 0
1
5
9 13 17 21 25 29 33 37 41 45 49 1
5
9 13 17 21 25 29 33 37 41 45 49 1
5
9 13 17 21 25 29 33 37 41 45 49
Fig. 2. Confirmed* measles cases by epidemiological week, seven southern African countries, 2009 (N = 9546), 2010 (N = 111,186), and 2011 (N = 267). * Confirmed measles cases were defined by laboratory confirmation, epidemiological link, or classified as clinically compatible. Note: In 2009, 33 cases in Namibia had missing date data. In 2010, 23,548 cases in Malawi had missing date data. M: months, Y: years, ORI: Outbreak response immunization campaign, SIA: supplemental immunization activity. a Sub-national ORI campaign in response to the outbreak conducted in September–November 2009, target age 5–19Y, 77% coverage achieved. b Sub-national ORI campaign in response to the outbreak conducted in October–November 2009, target age 5–19Y, 88% coverage achieved. c National planned SIA with expanded age group in response to the outbreak conducted in May–July 2010, target age 6M–15Y, 98% coverage achieved.
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3.2. Supplemental immunization activities During 1996–2011, 45 nationwide or sub-national follow-up SIAs were implemented, including five each in Botswana, Lesotho, and Malawi, six each in Namibia, Swaziland, and Zimbabwe, and 12 in South Africa (Table 1). During the 45 SIAs, a total of 79,696,523 people received measles vaccination and reported coverage was ≥95% in 15 SIAs (34%), 90–94% in 13 SIAs (30%), 80–89% in 12 SIAs (27%), and
