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. Author manuscript; available in PMC: 2023 Jun 26.
Published in final edited form as: Vaccine. 2014 Feb 13;32(16):1798–1807. doi: 10.1016/j.vaccine.2014.01.089

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,*
PMCID: PMC10292670  NIHMSID: NIHMS752934  PMID: 24530936

Abstract

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 <1 case per million during 1996–2008. During 2009–2010, large outbreaks that included cases among older children and adults were reported in all seven countries, starting in South Africa and Namibia in mid-2009 and in the other five countries by early 2010. The measles virus genotype detected was predominantly genotype B3.

Conclusion:

The measles resurgence highlighted challenges to achieving measles elimination in AFR by 2020. To achieve this goal, high two-dose measles vaccine coverage by strengthening routine immunization systems and conducting timely SIAs targeting expanded age groups, potentially including young adults, and maintaining outbreak preparedness to rapidly respond to outbreaks will be needed.

Keywords: Measles, Elimination, Africa, Immunization, Vaccination

1. Introduction

Measles caused an estimated 2.6 million deaths worldwide in 1980 [1]. Following widespread use of measles vaccine, estimated measles deaths decreased globally to 158,000 in 2011 [2]. In 2012, the World Health Organization (WHO) Global Vaccine Action Plan (GVAP) set a goal for measles elimination in five of the six WHO regions by 2020 [3]. In September, 2013 the WHO South-East Asia Region adopted a measles elimination goal by 2020; therefore, for the first time, all six WHO regions have a goal for measles elimination by 2020 or earlier [4].

During the early 1990s, the WHO Region of the Americas (ROA) pioneered a measles elimination strategy that included (1) an initial one-time nationwide ‘catch-up’ supplemental immunization activity (SIA) targeting children nine months to 14 years of age, (2) ‘keep-up’ measles vaccination through routine immunization of successive birth cohorts, (3) periodic ‘follow-up’ SIAs targeting children born since the initial SIA to prevent accumulation of susceptible individuals, and (4) establishing case-based measles surveillance [5]. The ROA goal of measles elimination, established in 1994, was achieved by 2002 [6]. In 2003, ROA countries adopted a goal for rubella elimination by 2010 and started implementing large, one-time ‘speed-up’ SIAs using combined measles-rubella-containing (MR) vaccine targeting children and adults, generally up to 29 or 39 years of age [7]. The last endemic rubella case was reported in 2009 [8]. The added benefit of combined MR SIAs was that adults who remained measles-susceptible were vaccinated, thus reducing the accumulation of measles-susceptible persons [9].

In 1996, seven southern African countries (Botswana, Lesotho, Malawi, Namibia, South Africa, Swaziland, and Zimbabwe) with relatively high (~80%) MCV1 coverage in the WHO African Region (AFR) started implementing a measles mortality reduction strategy that was adapted from the ROA strategy [10]. During 1996–2000 in these seven countries, a nationwide “catch-up” measles SIA targeting children nine months to 14 years of age was completed, annually reported measles cases decreased from 61,160 to 7057 and reported measles deaths decreased to zero [10,11].

In 2001, based on the success in these seven countries, all 46 WHO-AFR countries became part of a global initiative to reduce estimated measles mortality by 50% by 2005, compared with the 1999 estimate [12]. The WHO-UNICEF recommended measles mortality reduction strategies included (1) first dose of measles-containing vaccine through routine services (MCV1) for children at nine months of age, (2) a one-time nationwide catch-up SIA targeting children nine months to 14 years of age and periodic follow-up SIAs targeting children 9–59 months of age, (3) measles case-based surveillance with laboratory testing, and (4) improved measles case management [13]. Additionally, in 2010 the World Health Assembly established the following WHO-recommended targets to measure progress towards measles eradication: (1) reduce annual measles incidence to <1 laboratory-confirmed or epidemiologically-linked case per million and maintain that level; (2) >95% coverage annually of both MCV1 and a second dose of measles-containing vaccine (MCV2) both nationally and in every district or equivalent administrative unit [14,15].

During 2000–2008, in AFR, reported measles cases decreased 93% and estimated measles deaths decreased 92% from 371,000 to 28,000 [16]. However, measles-susceptible persons accumulated over a prolonged time period with suboptimal vaccination coverage, and during 2009–2010, confirmed measles outbreaks occurred in 28 AFR countries, including the seven southern African countries that started SIA implementation in 1996. In 2011, AFR countries adopted a goal for measles elimination by 2020 [17]. To inform AFR measles elimination efforts and identify likely causes of the measles resurgence, measles vaccination, epidemiological and laboratory surveillance data in the seven southern African countries from 1996 to 2011 were analyzed.

2. Methods

2.1. Routine immunization

WHO/UNICEF MCV1 coverage estimates for children aged one year and MCV2 coverage estimates reported by countries using the WHO/UNICEF joint reporting form (JRF) were analyzed [11].

2.2. Supplemental immunization activities

SIA administrative coverage, calculated by dividing the number of children vaccinated by the number of children targeted for vaccination, reported by each country to WHO were reviewed.

2.3. Measles surveillance

Annual measles cases reported by each country using the JRF during 1996–2011 and national measles case-based surveillance data reported by each country to WHO during 2009–2011 were analyzed [11]. JRF-reported cases were classified as suspected cases for analysis, since these data were either from case-based surveillance or the Integrated Disease Surveillance and Response system of aggregate numbers of suspected measles cases [18]. For surveillance, the suspected measles case definition used was an illness characterized by maculopapular rash, fever and ≥1 of the following symptoms: conjunctivitis, coryza, and cough, or any patient in whom the clinician suspects measles. Investigations of suspected cases included collection of information on sex, place of residence (urban/rural), age, vaccination status, and collection of a serum specimen for laboratory testing. According to WHO-AFR guidelines, suspected measles cases were classified as confirmed by laboratory, epidemiologic linkage and/or clinical criteria. Laboratory-confirmed measles cases were defined as having measles-specific immunoglobulin M (IgM) antibody positive test result, and not receiving a measles vaccination during the 30 days prior to rash onset. An epidemiologically-linked case was defined based on WHO-AFR guidelines as meeting the suspected measles case definition and having contact (i.e., lived in the same district or adjacent districts with plausibility of transmission) with a laboratory-confirmed measles case with rash onset within the preceding 30 days. A clinically-compatible case was defined as meeting the measles case definition, and with no sample available for laboratory testing and no evidence of epidemiological linkage to a laboratory-confirmed case.

Data were analyzed using SAS version 9.3 (SAS Institute). Testing for measles-specific IgM antibody was performed at national measles laboratories using a standard enzyme-linked immunosorbant assay (Enzygnost ELISA™, Siemens, Marburg, Germany). RNA was extracted from available specimens using the QIAamp® viral RNA mini kit (QIAGEN®), and amplified by RT-PCR using primers MeV214 and MeV216 designed to target a 634 nucleotide region coding for the 3’terminus of the nucleoprotein (N) gene (measles genotyping kit v2.0 CDC, Atlanta). Sequences were analyzed using 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).

Table 1.

Measles supplementary immunization activities (SIA) and estimated coveragea with the routine first dose measles-containing vaccine (MCV1), seven southern African countries, 1996–2011.

Country Extent of SIA Dates of SIA Target age group Target population Number of target population vaccinated SIA vaccination coverage (%)b 1996 MCV1 coverage (%) 2011 MCV1 coverage (%)
Botswana National Jul–Aug 97 9M–14Y 344,280 347,265 101 89 94
National May 98 9M–14Y 234,960 246,420 105
National May 01 9–59M 160,000 136,000 85
National Oct 05 9–59M 180,450 179,587 100
National Nov 09 9–59M 171,038 195,841 115
Lesotho National Oct 99 9–59M 266,329 159,933 60 82 85
National Oct 00 5–14Y 624,994 469,005 75
National Apr–May 03 9–59M 204,786 178,522 87
National Oct 07 9–59M 212,800 196,416 92
Nationalc Sep 10 6M–15Y 615,109 558,335 91
Malawi National Oct 98 9M–14Y 4,179,229 4,747,452 114 90 96
Sub-national Aug 02 9–59M 1,583,664 1,906,985 120
National Sep 05 9–59M 1,851,176 2,137,152 115
National Oct 08 9–59M 2,120,557 2,087,375 98
Nationalc Aug 10 9M–15Y 6,370,409 6,785,428 107
Namibia National Jun 97 9M–14Y 737,977 677,538 92 61 74
National Jun 00 9–59M 285,504 257,590 90
National Jun 03 9–59M 340,000 318,240 94
Sub-national Aug 06 9–59M 353,270 318,905 90
National Jun 09 9–59M 246,501 256,006 104
Sub-national Feb–Mar 10 6–59Md NA NA Range by district 88–115
South Africa Sub-national Aug 96 9M–14Y 3,559,252 3,317,400 93 76 78
Sub-national Aug 96 9M–4Y 2,173,753 1,786,048 82
National May 97 5–14Y 4,045,498 3,495,415 86
Sub-national May 97 9M–14Y 4,278,598 3,281,321 77
National May 00 9–59M 3,384,890 3,005,319 89
National Jul 04 9–59M 3,791,127 3,501,447 92
Sub-national Apr–May 05 9–59M 2,674,829 2,273,604 85
National May 07 9–59M 4,349,921 3,880,585 89
Sub-nationale May 09 9–59M 229,514 186,334 81
Sub-nationale Sep–Nov 09 5–19Y 396,114 304,981 77
Sub-nationale Oct–Nov 09 5–19Y 2,566,587 2,251,305 88
Nationalc May–Jul 10 6M–15Y 14,930,510 14,592,721 98
Swaziland National Jun 98 9–59M 147,545 146,626 99 82 98
National May 99 5–14Y 276,732 244,739 88
National Jun 02 9–59M 157,381 127,829 81
National Jul 06 9–59M 153,504 140,143 91
National Jul 09 9–47M 91,124 87,592 96
National Oct–Nov 10 9–59M 125,845 112,740 90
Zimbabwe National Jun 98 9M–14Y 5,279,248 4,929,475 93 88 92
National Jun–Jul 02 9–59M 1,808,552 1,537,263 85
Sub-national Jul 03 9–59M 375,782 353,235 94
National Jun 06 9–59M 1,479,957 1,407,510 95
National Jun 09 9–59M 1,523,344 1,408,589 92
Nationale May 10 6M–14Y 5,310,480 5,164,307 97
Total 80 84
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M: months, Y: years, NA: not available, ORI: Outbreak response immunization campaign, SIA: supplemental immunization activity.

a

WHO/UNICEF estimates of MCV1 coverage among children aged one year.

b

Values >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.

Fig. 1.

Fig. 1.

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Reported measles cases*, estimated coverage** with the routine first dose of measles-containing vaccine (MCV1), and measles supplemental immunization activities*** (SIAs), seven southern African countries, 1996–2011.

*Measles cases reported annually to WHO by member states through the WHO/UNICEF Joint Reporting Form.

**Population-weighted average using United Nations Development Programme population estimates and annual national WHO/UNICEF MCV1 coverage estimates for children aged 1 year for 1996–2011

***In each country, measles SIAs started with an initial catch-up SIA targeting all children aged 9 months to 14 years and then periodic follow-up SIAs, generally targeting all children born since the last SIA, conducted nationwide every 2–4 years targeting children aged 9–59 months, in some cases, expanded age groups were used in follow-up SIAs.

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.

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 <80% in four SIAs (9%) (Table 1).

3.3. Measles surveillance

From 1996 to 1999, the number of annually reported measles cases from the WHO/UNICEF JRF in the seven countries decreased 95%, from 61,160 to 2988 (Fig. 1). The number of reported cases in 2000 increased to 7057 due to an increase in reported cases from Botswana and South Africa. During 2001–2008, the number of annually reported measles cases decreased 98%, from 2528 to 60 and measles incidence decreased 98% from 33 cases per million to <1 case per million, with all seven countries reporting decreases in cases and incidence.

During 2001–2004, isolated outbreaks occurred; the number of JRF-reported suspected measles cases was 1166 in 2001 and 1043 in 2002 from South Africa, 1278 in 2002 from Namibia, and 1116 from Malawi in 2004. During 2006–2008, between zero and 242 suspected measles cases were reported annually through the JRF from each of the seven countries. However, during 2009–2010, large outbreaks were reported in all seven countries. Starting in epidemiologic week (epi-week) 24 of 2009, clusters of confirmed cases were reported in South Africa, primarily from the Tshwane and Johannesburg municipal districts in Gauteng Province (Figs. 2 and 3).

Fig. 2.

Fig. 2.

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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.

aSub-national ORI campaign in response to the outbreak conducted in September–November 2009, target age 5–19Y, 77% coverage achieved.

bSub-national ORI campaign in response to the outbreak conducted in October–November 2009, target age 5–19Y, 88% coverage achieved.

cNational planned SIA with expanded age group in response to the outbreak conducted in May–July 2010, target age 6M–15Y, 98% coverage achieved.

dSub-national ORI campaigns in response to the outbreak conducted September–December 2009 in 6 districts, target age 6–59M, coverage achieved NA.

eSub-national ORI campaigns in response to the outbreak conducted in February–March 2010 in 4 districts, target age 6–59M in 3 districts, >6M in 1 district, irrespective of previous vaccination status, coverage range by district 88–115%.

fNational ORI campaign in response to the outbreak conducted in May 2010, target age 6M-14Y, 97% coverage achieved.

gNational campaign conducted in November 2009, target age 9–59M, 115% coverage achieved.

hNational planned SIA with expanded age group in response to the outbreak conducted in September 2010, target age 6M–15Y, 91% coverage achieved.

iNational planned SIA with expanded age group in response to the outbreak conducted in August 2010, target age 9M–15Y, 107% coverage achieved.

jNational campaign conducted in October–November 2010, target age 9–59M, 90% coverage achieved.

Fig. 3.

Fig. 3.

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Annualized reported confirmed measles incidence* and measles virus genotypes detected by district, seven southern African countries, 2009–2011.

*Annualized reported measles incidence was calculated by dividing the number of reported confirmed measles cases from national measles case-based surveillance data by annual population estimates from national census projections.

Note: Each genotype symbol on the map indicates between 1 and 37 specimens of that genotype in a district.

Reported confirmed cases increased sharply starting in epi-week 35 in South Africa, and peaked with 674 cases in epi-week 40. The outbreak in South Africa coincided with an increase in confirmed cases in Namibia starting in epi-week 31, 2009 (Fig. 2). In July–December 2009 in Namibia, confirmed measles incidence ≥50 cases per million was reported in 21 districts in northern Namibia and along the Angola border, including Opuwo district with the highest confirmed measles incidence, 12,454 cases per million (Fig. 3). Increases in confirmed cases started in Botswana, Malawi, and Zimbabwe by epi-week one, 2010 and in Lesotho and Swaziland by epi-week five, 2010 (Fig. 2). Weekly reported confirmed cases reached peaks of 107 cases in epi-week six in Botswana, 209 cases in epi-week 11 in Lesotho, 555 cases in epi-week 16 in Zimbabwe, 42 cases in epi-week 23 in Swaziland, and 6869 cases in epi-week 25 in Malawi. After January 2011, sporadic cases occurred in all seven countries.

During 2009–2011, through measles case-based surveillance in the seven countries, 181,826 suspected measles cases were reported (Table 2). Of these, 51,700 (28%) had a specimen sent for laboratory testing to detect measles-specific IgM; 21,265 (41%) tested positive, 28,691 (55%) tested negative, 891 (2%) had indeterminate test results, and 853 (2%) had unknown test results (Table 2). During 2009–2011, 144,580 confirmed cases were reported from the seven countries (Table 3); of these, 21,265 (15%) were laboratory-confirmed, 115,767 (80%) were confirmed by epidemiological link, and 7548 (5%) were confirmed by clinically compatible classification (data not shown). Malawi accounted for 108,717 (75%) confirmed cases. In six of the seven countries (all except Namibia), measles incidence peaked in 2010, ranging from 237 cases per million population in South Africa to 7293 cases per million population in Malawi (Table 3).

Table 2.

Laboratory results for measles-specific IgM antibody testing of suspected measles cases, seven southern African countries, 2009–2011.

Suspected measles cases Measles IgM laboratory test result
 Rubella IgM laboratory test result
Measles IgM tested
 IgM +
 IgM−
 Indeterminate
 Unknown
 Positivity Ratea Rubella IgM tested
 Rubella IgM +
Country Year n n % n % n % n % n % % n % n %
Botswana 2009 595 592 99 177 30 294 50 24 4 97 16 36 535 90 4 1
2010 1411 1117 79 563 50 491 44 62 6 1 0 50 534 38 13 2
2011 735 735 100 6 1 596 81 1 0 132 18 1 497 68 193 39
Total 2741 2444 89 746 31 1381 57 87 4 230 9 34 1566 57 210 13
Lesotho 2009 189 189 100 20 11 166 88 3 2 0 0 11 188 99 73 39
2010 2728 702 26 372 53 281 40 49 7 0 0 53 746 27 78 10
2011 169 150 89 0 0 150 100 0 0 0 0 0 150 89 78 52
Total 3086 1041 34 392 38 597 57 52 5 0 0 38 1084 35 229 21
Malawi 2009 529 528 100 16 3 511 97 1 0 0 0 3 316 60 40 13
2010 109,267 852 1 370 43 477 56 0 0 5 1 44 851 1 26 3
2011 659 651 99 21 3 630 97 0 0 0 0 3 651 99 223 34
Total 110,455 2031 2 407 20 1618 80 1 0 5 0 20 1818 2 289 16
Namibia 2009 2716 951 35 344 36 522 55 61 6 24 3 37 802 30 25 3
2010 2234 698 31 167 24 489 70 42 6 0 0 24 622 28 157 25
2011 875 854 98 59 7 453 53 9 1 333 39 11 852 97 134 16
Total 5825 2503 43 570 23 1464 58 112 4 357 14 27 2276 39 316 14
South Africa 2009 15,246 15,204 100 6086 40 8559 56 559 4 0 0 40 15,215 100 3009 20
2010 23,264 16,189 70 11,904 74 4028 25 0 0 257 2 75 5910 25 1236 21
2011 8632 8610 100 116 1 8460 98 34 0 0 0 1 8590 100 3226 38
Total 47,142 40,003 85 18,106 45 21,047 53 593 1 257 1 46 29,715 63 7471 25
Swaziland 2009 240 240 100 16 7 223 93 1 0 0 0 7 240 100 135 56
2010 769 617 80 301 49 311 50 5 1 0 0 49 614 80 94 15
2011 77 77 100 0 0 77 100 0 0 0 0 0 77 100 19 25
Total 1086 934 86 317 34 611 65 6 1 0 0 34 931 86 248 27
Zimbabwe 2009 853 401 47 127 32 264 66 6 1 4 1 32 351 41 29 8
2010 9762 1468 15 600 41 836 57 32 2 0 0 41 482 5 97 20
2011 876 875 100 0 0 873 100 2 0 0 0 0 873 100 448 51
Total 11,491 2744 24 727 26 1973 72 40 1 4 0 27 1706 15 574 34
Total 181,826 51,700 28 21,265 41 28,691 55 891 2 853 2 42 39,096 22 9337 24
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a

The number of IgM+ divided by the number with a known test result.

Table 3.

Confirmed measles cases by sex, setting, age group, and vaccination status, seven southern African countries, 2009–2011.

Country Year Annual Incidence per 1 milliona Casesb Male
 Settingc
 Age Group
 Vaccination Status
n n % Urban Rural <9 M 9M–4Y 5–9Y 10–14Y ≥15 Y 1 dose ≥2 doses None Missing
n % n % n % n % n % n % n % n % n % n % n %
Botswana 2009 137 271 126 47 129 48 139 52 25 9 30 11 30 11 75 28 109 41 35 13 14 5 3 1 219 81
2010 454 912 454 50 223 24 689 76 100 11 89 10 118 13 245 27 357 39 206 23 173 19 11 1 522 57
2011 3 7 3 43 2 29 5 71 2 29 0 0 3 43 1 14 1 14 1 14 2 29 1 14 3 43
Total 1190 583 49 354 30 833 70 127 11 119 10 151 13 321 27 467 39 242 20 189 16 15 1 744 63
Lesotho 2009 11 23 NA NA NA NA NA NA 0 0 3 13 8 35 9 39 3 13 1 4 2 9 0 0 20 87
2010 1112 2415 1108 48 NA NA NA NA 162 7 489 20 714 30 708 29 338 14 70 3 123 5 48 2 2174 90
2011 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Total 2438 1108 48 NA NA NA NA 162 7 492 20 722 30 717 29 341 14 71 3 125 5 48 2 2194 90
Malawi 2009 1 17 11 65 1 6 16 94 3 18 6 35 7 41 1 6 0 0 3 18 0 0 14 82 0 0
2010 7293 108,679 54,746 51 81 22 287 78 14,566 14 29,822 28 16,663 16 16,087 15 30,244 28 48 <1 1 <1 266 <1 108,364 100
2011 1 21 7 33 0 0 21 100 5 24 4 19 4 19 2 10 6 29 4 19 0 0 4 19 13 62
Total 108,717 54,764 51 82 20 324 80 14,574 14 29,832 28 16,674 16 16,090 15 30,250 28 55 <1 1 <1 284 <1 108,377 100
Namibia 2009 910 2041 1057 52 1179 94 75 6 407 20 427 21 170 8 119 6 889 44 92 5 20 1 628 31 1301 64
2010 632 1442 708 49 76 13 513 87 77 5 418 29 340 24 194 14 405 28 290 20 56 4 408 28 688 48
2011 37 87 43 49 69 79 18 21 10 11 25 29 19 22 10 11 23 26 26 30 3 3 8 9 50 57
Total 3570 1808 51 1324 69 606 31 494 14 870 25 529 15 323 9 1317 37 408 11 79 2 1044 29 2,039 57
South Africa 2009 134 6646 3450 54 1384 90 146 10 1576 24 1498 23 521 8 685 10 2366 36 18 <1 17 <1 105 2 6,506 98
2010 237 11,904 808 52 NA NA NA NA 4344 36 2477 21 1005 8 1723 14 2355 20 NA NA NA NA NA NA 11,904 100
2011 3 150 74 52 NA NA NA NA 35 23 53 35 9 6 21 14 32 21 NA NA NA NA NA NA 150 100
Total 18,700 4332 53 1384 90 146 10 5955 32 4028 22 1535 8 2429 13 4753 25 18 <1 17 <1 105 1 18,560 99
Swaziland 2009 15 17 13 76 0 0 17 100 5 29 1 6 0 0 9 53 2 12 1 6 0 0 0 0 16 94
2010 386 458 244 53 22 5 436 95 67 15 69 15 71 16 167 36 84 18 9 2 11 2 41 9 397 87
2011 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Total 475 257 54 22 5 453 95 72 15 70 15 71 15 176 37 86 18 10 2 11 2 41 9 413 87
Zimbabwe 2009 45 564 233 46 77 17 379 83 26 5 212 38 196 35 110 20 20 4 11 2 9 2 541 96 3 <1
2010 710 8924 3978 45 5164 58 3760 42 859 11 2522 33 1743 23 1316 17 1184 16 711 8 388 4 5907 66 1,918 21
2011 0 2 2 100 0 0 2 100 0 0 2 100 0 0 0 0 0 0 1 50 1 50 0 0 0 0
Total 9,490 4213 45 5241 56 4141 44 885 11 2736 33 1939 24 1426 17 1204 15 723 8 398 4 6448 68 1,921 20
Total 144,580 67,065 51 8407 56 6503 44 22,269 16 38,147 27 21,621 15 21,482 15 38,418 27 1527 1 820 1 7985 6 134,248 93
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M: months, Y: years, NA: not available.

Data: Case-based surveillance data. 2009 and 2010 data from South Africa include measles case-based surveillance data and measles laboratory data.

a

Annual measles incidence was calculated using confirmed measles cases as reported by countries using measles case-based surveillance to the World Health Organization (WHO) African Regional Office and population estimates from the United Nations Population Division.

b

Confirmed by laboratory testing, epidemiological link, or clinically compatible as reported by countries using measles case-based surveillance to the WHO African Regional Office.

c

Setting classification reported as either urban or rural; percents are of those without a missing value.

Of 144,580 confirmed cases reported during 2009–2011, 14,910 (10%) had information on residence; of these, 8407 (56%) were from urban settings (Table 3). The proportion of reported cases from an urban setting was highest in 2009 in Namibia (94%) and in 2010 in Zimbabwe (58%). Of the 141,937 (98%) cases with age information, 38,418 (27%) were adults ≥15 years of age (Table 3); of these 14,065 (37%) were 15–19 years, 7981 (21%) were 20–24 years, 7474 (19%) were 25–29 years, and 8898 (23%) were ≥30 years of age. Information about vaccination status was missing for 134,248 (93%) confirmed cases. However, of the 10,332 (7%) confirmed cases with vaccination history, 7985 (77%) were unvaccinated for measles (Table 3).

During 2009–2011, genotype data were available for 282 reported cases: two from Swaziland, 16 from Lesotho, 16 from Botswana, 25 from Malawi, 34 from Zimbabwe, 64 from Namibia, and 125 from South Africa (Fig. 3 and Supplemental Fig. 1). Of the 282 genotype results, 229 (81%) were B3, 51 (18%) were B2, one (<1%) was D4, and one (<1%) was D8. The genotype B3 viruses were of a single strain detected in all seven countries and found to be closely related to measles virus previously detected in West Africa; in Namibia, the genotype B2 strain was found to be closely related to measles virus previously detected in Angola and the Democratic Republic of the Congo. The genotype D8 was detected in 2009 and the genotype D4 was detected in 2010, both in South Africa.

4. Discussion

Following intensive efforts to control measles in southern Africa starting in 1996, reported measles incidence was reduced to <1 per million population in Botswana, Lesotho, Malawi, Namibia, South Africa, Swaziland and Zimbabwe during 2006–2008. Thereafter, these seven countries experienced large outbreaks, starting in 2009 in South Africa and Namibia before spreading to neighboring countries, predominantly with a single strain of measles virus genotype B3 previously detected in West Africa. Of confirmed measles cases during the resurgence, 16% were among infants <9 months of age and 27% among adults.

Outbreak investigations conducted during the resurgence determined that the principal cause of these outbreaks was failure to vaccinate eligible persons, causing measles-susceptibility that accumulated over a prolonged time period [20–27]. During the past decade, the significant reduction in measles burden likely led to complacency in measles vaccination efforts, including SIA planning and implementation and routine immunization services. Additionally, suboptimal vaccination coverage contributed to outbreaks among known at-risk subpopulations, for example, the nomadic populations in Namibia, and the apostolic religious communities reluctant to accept vaccinations for faith-based reasons in Zimbabwe, Malawi, Botswana, Swaziland and South Africa [28]. Measles outbreak response immunization (ORI) activities conducted during the resurgence included ‘selective’ vaccination of unvaccinated children 6–59 months of age at routine services and ‘non-selective’ mass campaigns targeting age groups ranging from 6–59 months to ≥6 months of age. Following ORI, cases decreased; however, ORI implementation generally was not rapid and occurred months after the start of outbreaks.

In some settings, immunization program data were found to be unreliable for guiding vaccination efforts. For example, in South Africa, during 2005–2011, reported MCV1 coverage ranged from 83% to 99% while WHO/UNICEF estimates that incorporate available survey results ranged from 63% to 78% [29,30]. In the seven countries prior to the resurgence, reported SIA administrative coverage estimates were high; however post-SIA coverage surveys were not routinely conducted to validate reported coverage and outbreaks occurred among children in SIA target age groups, suggesting suboptimal SIA coverage and inaccuracies in reported coverage.

These findings should be considered with several limitations. First, reported vaccination coverage data may be biased by inaccurate estimates of target populations and reporting of doses delivered. Second, surveillance systems do not detect all measles cases because reporting is incomplete from communities and health facilities. Third, although adequate case investigation is recommended for >80% of suspected cases, 90% and 93% of the cases had missing information for urban/rural and vaccination status, respectively. Therefore, analysis of residence and vaccination status might not be representative of all cases. Finally, comparing annual reported measles case totals and incidence is difficult when sensitivity and completeness of reporting vary by country and by year.

The 2010 World Cup soccer games hosted by South Africa during June–July, 2010, coincided with the peak of the measles outbreak in that country, resulting in infection of susceptible visitors and subsequent exportation of measles virus to several countries. In general, the Southern Africa economic block has a relatively high volume of cross-border movement by traders, business people, students, tourists and migrant workers; international migration and travel provide opportunities for measles virus importations [31]. In countries that share open borders and frequent migration, coordinated vaccination strategies, including synchronized SIAs prior to large public gatherings, e.g. international sporting events, could be considered to prevent outbreaks.

Optimal ORI strategies, including timing, geographic scope, and target age groups are uncertain and remain a global research priority [32]. Infants born with transferred maternal antibodies from vaccine-induced protection rather than from naturally acquired measles virus infection generally result in lower geometric mean titers that wane faster, leaving the infant unprotected in early infancy [33,34]. Also, children born to HIV-infected mothers have lower concentrations of passively acquired maternal antibodies [35,36], and measles antibody titers decline more rapidly after vaccination among HIV-infected compared with non-HIV infected persons [36–38]. Therefore, WHO recommends ORI target age groups include young infants starting at 6 months of age, and in areas with high incidence of both HIV infection and measles, the first dose of measles vaccine may be offered as early as 6 months of age, in addition to the routine two-dose schedule [39].

The relative contribution of HIV infection to measles virus transmission in southern Africa appears to have been minimal [27,40,41]. In 2002 in South Africa and during 2009–2011 in South Africa and Malawi, investigations determined the outbreaks were caused primarily by suboptimal vaccination coverage and that high HIV-prevalence played a minor role in the accumulation of measles-susceptible persons [40,42]. Moreover, Biellik et al. reported in 2002 that measles was nearly eliminated in these countries despite high HIV prevalence [10].

To achieve measles elimination, high population immunity is needed and WHO recommends >95% two-dose measles vaccination coverage at the national and district levels as a measure to monitor progress toward measles elimination [14]. To achieve high coverage, routine outreach services to communities known to be measles-susceptible or with poor access to immunization services are needed. Additionally, these communities should be included in SIA micro-planning and SIA planning should start 6–8 months prior to implementation [43]. The shift of measles epidemiology towards older age groups is well documented [44]; therefore, adequate resources should be made available to ensure timely SIA implementation, and if indicated, using expanded target age groups [14,39,45].

Measles and rubella elimination strategies, including using MR vaccine, were effectively integrated in the ROA, leading to elimination of both measles and rubella. However, in AFR, by the start of 2013, MR vaccine was not publicly available in 43 of the 46 countries and rubella virus circulated widely [46]. In 2012, the GAVI Alliance committed funding for eligible countries to introduce rubella-containing vaccine starting with a one-time MR SIA targeting children nine months to 14 years of age. But, unlike the ‘speed-up’ MR SIAs in ROA that started within ten years after initial measles SIAs and included adults, MR SIAs in AFR will start >17 years after initial measles SIAs and will not include adults; therefore, existing measles susceptibility among adults will remain, increasing the need for high population immunity among infants and children needed to achieve elimination.

The Measles & Rubella Initiative 2012–2020 Global Measles and Rubella Strategic Plan, with goals aligned to the GVAP, aims to (i) achieve and maintain high levels of population immunity through high coverage with two doses of MR vaccines, (ii) establish effective surveillance to monitor disease and evaluate progress, (iii) develop and maintain outbreak preparedness for rapid response and appropriate case management, (iv) communicate and engage to build public confidence in and demand for vaccination, and (v) conduct research and development to support operations and improve vaccination and diagnostic tools [47]. To implement these strategies and improve data quality for guiding program efforts, adequate resources and intensified efforts are needed to achieve measles elimination in AFR by 2020.

Supplementary Material

Supplementary Material

Acknowledgements

The authors gratefully acknowledge the work of all immunization officers, surveillance medical officers, and measles laboratory personnel across AFR involved in the implementation of the strategies for measles control. We also thank the Measles & Rubella Initiative for providing financial and technical assistance to member states for strategy implementation and efforts to achieve measles elimination in AFR.

The findings and conclusions in this report are those of the authors and do not necessarily represent the official position of the World Health Organization or the U.S. Centers for Disease Control and Prevention.

Footnotes

Conflicts of interest

We declare that we have no conflict of interest.

Authors declare that this article has not been previously presented.

Financial interest: The authors do not have a financial or proprietary interest in a product, method, or material or lack thereof.

Appendix A. Supplementary data

Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.vaccine.2014.01.089.

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