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

Preplanned National Measles VaccinationCampaign at the Beginning of a MeaslesOutbreak—Sierra Leone, 2009–2010

David E. Sugerman,1 Amadou Fall,2 Marie-Therese Guigui,3 Michael N'dolie,4 Terry Balogun,4 Alie Wurie,5 andJames L. Goodson1

1Centers for Disease Control and Prevention, Global Immunization Division, Atlanta, Georgia; 2World Health Organization, Inter-Country Support Teamfor West Africa, Ouagadougou, Burkina Faso; 3UNICEF, Health Specialist for Measles, Yellow Fever, and Health Emergencies, Regional Office for Westand Central Africa, Dakar, Senegal; 4Expanded Programme on Immunization, World Health Organization, and 5Ministry of Health and Sanitation,Expanded Programme on Immunization, Freetown, Sierra Leone

Background. Large-scale measles outbreaks occurred throughout Africa from 2008-2010. In Sierra Leone, in

November 2009, preceding a measles supplemental immunization activity (SIA), the largest measles outbreak in a

decade started.

Methods. We analyzed data from the national measles case-based surveillance system, developed a susceptibility

profile of the population, and calculated vaccine effectiveness (VE) among children 12-59 months of age.

Results. From November 1, 2009 to July 13, 2010, 1,094 confirmed cases, including 9 deaths, were reported; 716

(66%) were ,5 years of age. B3 genotype was identified. Measles attack rates per 100,000 population were highest

among infants aged 6–8 months (56.4) and in Bo district (49.4). Districts with higher estimated SIA coverage tended to

have lower attack rates (Spearman Correlation Coefficient 520.63), p 5 0.07. Among 473 cases with information on

vaccination status, 222 (47%) were unvaccinated; estimated VE was 74%. The 2009 measles SIA led to 165,000 fewer

estimated susceptible individuals.

Conclusions. The 2009 measles SIA reduced the overall magnitude of the outbreak, though routine and SIA

coverage was insufficient to prevent it entirely. Maintaining high coverage through routine services and SIAs in all

districts and conducting follow-up SIAs prior to the end of the low transmission season may prevent future

outbreaks.

Global goals for measles control were first set by the

World Health Assembly in 1989 [1] and by the World

Health Summit for Children in 1990 [2]. In sub-Saharan

Africa during the 1970s, the Expanded Programme

of Immunizations (EPI) was established and included a

single dose of measles vaccine at 9 months of age for

measles control. In 2000, the countries of the World

Health Organization (WHO) African Region (AFR)

became part of a global initiative with a goal to reduce

the number of measles deaths by 50% by 2005, com-

pared with the number of such deaths in 1999 [3]. To

achieve this goal, the WHO and the United Nations

Children’s Fund (UNICEF) recommended the measles

mortality reduction strategy in Africa that included

improving case management, establishing case-based

surveillance with laboratory confirmation of suspected

measles cases, providing the first dose of measles-

containing vaccine (MCV1) for all children, and pro-

viding a second opportunity for measles vaccination

through supplemental immunization activities (SIAs),

regardless of previous vaccination status or history of

measles disease [4].

The SIA component of the strategy included an initial

wide-age-range ‘‘catch-up’’ SIA to target children from

9 months through 14 years of age to rapidly reduce the

number of individuals who are susceptible to measles

and included periodic ‘‘follow-up’’ SIAs every 3–5 years

Potential conflicts of interest: none reported.Supplement sponsorship: This article is part of a supplement entitled ''Global

Progress TowardMeasles Eradication and Prevention of Rubella and Congenital RubellaSyndrome,'' which was sponsored by the Centers for Disease Control and Prevention.Reprints or correspondence: David E. Sugerman, MD, MPH, Global Immunization

Division, Centers for Disease Control and Prevention, 1600 Clifton Rd, NE; MS-E05,Atlanta, GA 30333 (ggi4@cdc.gov).

The Journal of Infectious Diseases 2011;204:S260–S269Published by Oxford University Press on behalf of the Infectious Diseases Society ofAmerica 2011.0022-1899 (print)/1537-6613 (online)/2011/204S1-0033$14.00DOI: 10.1093/infdis/jir110

S260 d JID 2011:204 (Suppl 1) d Sugerman et al

at CD

C P

ublic Health Library &

Information C

enter on July 27, 2011jid.oxfordjournals.org

Dow

nloaded from

to target children born since the previous SIA [5]. Following

implementation of the measles mortality reduction strategy

starting in 2001, the 50% measles mortality reduction goal was

achieved [3], and a new goal was established to achieve 90%

reduction by 2010, compared with measles mortality in 2000 [6].

Although substantial progress toward this goal was made from

2000 through 2008, several large measles outbreaks occurred

throughout the region during the period 2008–2010 [7], in-

cluding an outbreak in Sierra Leone.

Sierra Leone is located in West Africa, with an estimated

population of 5.8 million in 2010 [8], and is administratively

divided into 4 provinces (Northern, Eastern, Southern, and

Western Area) and 14 districts. Emerging from a crippling,

decade-long civil war (1991–2001) that led to .50,000 deaths

and a million internally displaced persons [9], Sierra Leone

remains one of the least developed nations in the world [10]

and has the world’s highest mortality rate among those ,5

years of age (290 deaths per 1000 live births) [11]. In addition,

after the civil war, donor funds dropped, health personnel

dispersed, and the already limited health infrastructure was

destroyed [12].

In Sierra Leone, EPI was established in 1974 [12]. Measles

vaccination coverage remained low (,50%) until the push to-

ward universal child immunization (UCI) occurred in the 1980s

[13]. During the period 1980–1990, prior to the civil war, rou-

tine MCV1 coverage increased from 36% to 75%, and the an-

nual number of reported measles cases decreased from 3625 to

830 [14]. During the civil war, MCV1 coverage estimates varied

considerably each year (28%–79%), leading to a resurgence of

measles with 3575 reported cases in 2000 (Figure 1).

As part of the WHO AFR measles mortality reduction strategy

adopted by member states in 2001, SIAs started in Sierra Leone in

November 2003 with a nationwide ‘‘catch-up’’ SIA targeting

children 9 months–14 years of age with measles vaccination and

had reported administrative coverage of 93% (administrative

coverage is calculated by dividing the total number of doses ad-

ministered to children in the target age group by the number of

children in that age group) (Table 1). Three years later, in No-

vember 2006, a nationwide ‘‘follow-up’’ SIA was conducted that

targeted children 9 months–4 years of age; 100% administrative

coverage with measles vaccine was reported [13]. In 2009, a

second nationwide ‘‘follow-up’’ SIA targeted children 9–59

months of age with measles vaccination and those 9 months of

age and older with yellow fever vaccination in 6 select districts.

Following this SIA, administrative coverage with measles vacci-

nation was 101%; however, a post-SIA cluster survey estimated

measles vaccination coverage was 84% by verbal history and

66% by vaccination card [15]. In Sierra Leone, following

Figure 1. Number of measles cases reported and estimated percentage of children who received the first dose of measles-containing vaccine throughroutine services, Sierra Leone, 1980–2009. *Confirmed cases of measles reported to the World Health Organization (WHO) and the United NationsChildren's Fund (UNICEF) through the Joint Reporting Form Regional Office for the Africa Region (1980–2008). �Vaccination coverage data from SierraLeone Expanded Programme of Immunizations (1980–1998) and WHO and UNICEF estimates (1999–2009) [14]. � Supplemental immunization activity(SIA).

Sierra Leone Measles Outbreak, 2009–2010 d JID 2011:204 (Suppl 1) d S261

at CD

C P

ublic Health Library &

Information C

enter on July 27, 2011jid.oxfordjournals.org

Dow

nloaded from

Table 1. History of Measles Supplemental Immunization Activities in Sierra Leone, 2003–2009

Year Dates Target age

Target

population Age in November 2009 Integrated interventions

Measles vaccine coverage (%)

Admina Cluster survey

2003b 1–6 Nov 9 Months to14 years

2,585,894 6 Years and 9 monthsto 21 years

None 93 .

2006b 20–26 Nov 9–59 Months 721,063 3 Years and 9 months to7 years and 11 months

Vitamin A, mebendazole,and LLINc (,5 years ofage) in all 14 districts

100 .

2009d 24–29 Nov 9–59 Months 824,366 9 Months to 4 years and11 months

Yellow fever vaccine (R9 monthsof age) in 6 districts plus oralpolio vaccine, albendazole,and vitamin A (,5 yearsof age) in all districts

101 66 (95% confidence interval,52–97) by card;

84 (95% confidence interval,81–87) by verbal history

NOTE. SIA, supplemental immunization activity.a Administrative coverage, calculated by dividing the total number of doses administered to children in the target age group by the census-estimated number of children in that age group. Coverage .100% is due to an

underestimation of the target population or vaccination of children from other areas.b 2006 National Measles-Malaria Campaign Report, 2006, performed by the Sierra Leone Ministry of Health and Sanitation [13].c Long-lasting insecticidal nets.d Yellow Fever and Measles Post-Campaign Immunization Coverage Survey in Sierra Leone, 29 December 2009–30 January 2010 performed by the World Health Organization, Statistics Sierra Leone, and Expanded

Programme of Immunizations, Sierra Leone [15].

S262dJID

2011:204(Suppl1)

dSu

german

etal

at CDC Public Health Library & Information Center on July 27, 2011 jid.oxfordjournals.org Downloaded from

implementation of the measles mortality reduction strategy,

estimated MCV1 coverage increased from 37% in 2000 to 66%

in 2008, and reported cases decreased from 3575 measles cases

in 2000 to a total of 1916 cases during 2001–2008 (ranging

from 0 cases in 2007 to 649 cases in 2001) (Figure 1). The

average estimated annual measles incidence decreased by

95%, from 10.0 cases per 100,000 population during 2001–2004

to 0.5 cases per 100,000 population during 2005–2008 [16].

However, on 1 November 2009 and immediately prior to the

implementation of a nationwide follow-up SIA on 24 November,

a laboratory-confirmed measles outbreak began, with initial cases

reported from Bombali, Bo (the country’s second largest city),

Koinadugu, and surrounding districts (Port Loko, Kenema, and

Tonkolili).

In response to the measles outbreak, an outbreak inves-

tigation was conducted jointly by the Sierra Leone Ministry of

Health and Sanitation, WHO, UNICEF, and the Centers for

Disease Control and Prevention (CDC). To identify the likely

cause of the outbreak and to describe measles epidemiology, we

reviewed measles vaccination coverage data through routine

service delivery and SIAs and analyzed measles case-based

surveillance data. We report the findings of the outbreak

investigation along with recommendations for preventing

potential measles outbreaks in the future.

METHODS

Description of the OutbreakA suspected measles case was defined as a generalized maculo-

papular rash and fever and at least one of the following: cough,

coryza (runny nose), or conjunctivitis in any person from 1

November 2009 through 13 July 2010 [17]. Surveillance officers

used individual case investigation forms to collect data on sus-

pected cases (age, sex, address, number of measles vaccine doses

received, and data of last measles vaccination) and entered these

into a case-based database. An attempt was made to collect se-

rum samples within 30 days of rash onset for laboratory testing;

confirmation was made by detection of measles im-

munoglobulin (Ig) M antibody at the WHO regional reference

laboratory at the Pasteur Institute in Abidjan, Ivory Coast, using

a standard commercial indirect enzyme-linked immunosorbent

assay (ELISA) (Enzygnost for IgM; Siemens) [18]. Following the

WHO AFR measles surveillance guidelines [17], laboratory

confirmation of cases was discontinued after the outbreak was

confirmed as measles, and additional cases were line-listed by

district health officers. Line-listed cases met the suspected

measles case definition and were confirmed by an epidemio-

logical link established for cases that did not have a specimen

collected for laboratory testing (ie, contact with a laboratory-

confirmed case who had rash onset within the preceding 30 days

or lived in the same or adjacent district with a laboratory-

confirmed case) [17].

Epidemiologic and laboratory data were entered in the

national measles case-based surveillance database. An out-

break of measles was defined as R3 laboratory-confirmed

measles cases in a health facility or district in 1 month [17].

Vaccination coverage through routine services or SIAs was

calculated using the administrative method by dividing the

total number of doses administered to children in the target

age group by the number of children in the target age group

according to the 2004 census. An outbreak-related case was

defined as a confirmed measles case with date of rash onset

during the period 1 November 2009–13 July 2010. Age-

specific and district-specific attack rates were calculated by

dividing the number of confirmed measles cases in each age

group or district by the total population in that age group or

district according to the 2004 census.

Oral fluid specimens were collected from a convenience

sample of 14 individuals with laboratory-confirmed measles

cases who were identified during site visits to health centers in

Western Area, Bonthe, and Port Loko districts to determine the

measles virus genotype. The specimens were shipped to the

WHO regional measles reference laboratory at the National In-

stitute for Communicable Diseases (NICD) in Johannesburg,

South Africa. Standard real-time reverse-transcription poly-

merase chain reaction (RT-PCR) was used to amplify a region of

the measles genome for sequence analysis and genotyping.

Specific complimentary DNA of measles virus nucleoprotein was

synthesized by RT-PCR and aligned, and phylogenetic trees were

constructed using standardized methods [19]. All new sequences

were submitted to GenBank (National Institutes of Health).

Vaccine EffectivenessVaccine effectiveness (VE) was calculated using the screening

method with the formula VE51-[(PCV/(1-PCV))*((1-PPV)/

PPV)], where PCV refers to the proportion of cases vaccinated

and PPV refers to the proportion of the population vaccinated

[20, 21]. The analysis was restricted to cases in individuals aged

12–59 months at the time of rash onset; the estimated

proportion of the population vaccinated during the period

2004–2008 was based on WHO and UNICEF MCV1 coverage

estimates.

Susceptibility ProfileA spreadsheet-based formula was used to calculate the estimated

number of susceptible individuals for each birth cohort in Sierra

Leone during the 30 years prior to the start of the outbreak [22].

The surviving birth cohort for each year was calculated by ap-

plying an annual population growth rate (1.8%) estimated from

the 2008 Demographic and Health Survey [23] to the 2004 census

data. The estimated number of individuals susceptible to measles

by age in November 2009 was calculated based on Sierra Leone

EPI MCV1 administrative coverage estimates during 1980–1998

and the WHO and UNICEF coverage estimates for each year

Sierra Leone Measles Outbreak, 2009–2010 d JID 2011:204 (Suppl 1) d S263

at CD

C P

ublic Health Library &

Information C

enter on July 27, 2011jid.oxfordjournals.org

Dow

nloaded from

during 1999–2009 [14], measles SIA administrative coverage for

2003 and 2006, and an estimate from a cluster survey for the 2009

measles SIA vaccination coverage by verbal history. For the sus-

ceptibility profile calculation, the following assumptions were

used: VE was 85% through routine services delivery and 90%

through SIAs, infants ,6 months of age were protected by ma-

ternal antibodies, unvaccinated children 6 months–14 years of

age were considered to be susceptible, half of unimmunized in-

dividuals 15–19 years of age were protected by natural immunity,

and adults R20 years of age were no longer susceptible [22]. We

also assumed that the likelihood of vaccination at each oppor-

tunity was independent (ie, those covered by routine services had

equal chances to be vaccinated by SIAs) and, therefore, multiplied

the remaining susceptible individuals after routine immunization

by the SIA coverage in that year. To control for the likely inflation

of SIA administrative coverage, we subtracted the 17% difference

between the reported coverage by verbal history in the 2009 SIA

cluster survey (84%) and reported administrative coverage

(101%) after the 2009 SIA from the administrative coverage re-

ported in the 2006 and 2003 SIAs.

Data AnalysisData analysis was performed using Excel (Microsoft Corporation);

Epi Info for Windows, version 3.3.2 (CDC); and SAS, version 9.2

(SAS Institute). Correlations of 2 continuous variables were

quantified using Spearman’s rank order correlation coefficient.

RESULTS

Description of Outbreak and Measles SupplementalImmunization ActivitiesFrom 1 January through 31 October 2009, 5 laboratory-

confirmed measles cases were detected (during epidemiologic

weeks 6–13). From 1–20 November 2009 (epidemiologic weeks

44–46), a cluster of laboratory-confirmed measles cases was

detected in Bombali, Bo, and Koinadugu (Figure 2). The

planned nationwide measles SIA targeting children 9 months to

4 years of age was implemented 24–29 November. National

administrative coverage was reported as 101% (ranging from

99% in Tonkolili to 108% in Western Area–Urban Districts),

whereas the estimated national coverage by cluster survey was

84% (ranging from 71% in Tonkolili to 100% in Kailahun)

(Table 2). Bo, with the highest attack rate (49 cases per 100,000

population) was not selected for the cluster survey, although it

had reported low routine coverage from 2002 through 2009

(69%), whereas Bombali (34 cases per 100,000 population) had

83% SIA coverage by cluster survey. The 3 districts with the

highest SIA coverage by cluster survey, Kambia (92%), Kailahun

(100%), and Western Area–Rural (91%), had the fewest re-

ported measles cases (range, 0–4 cases) during the outbreak.

Although not statistically significant, districts with higher esti-

mated campaign coverage tended to have lower measles attack

rates (Spearman correlation coefficient 5 20.63).

Figure 2. Number of confirmed cases of measles by week of rash onset (n5 970), Sierra Leone, 1 October 2009–13 July 2010. *Cases reported to theSierra Leone Ministry of Health and Sanitation (MOHS) measles case-based surveillance system and confirmed by the MOHS as either immunoglobulin(Ig) M antibody positive or epidemiologically linked to an IgM antibody–positive case. �Supplemental immunization activity (SIA).

S264 d JID 2011:204 (Suppl 1) d Sugerman et al

at CD

C P

ublic Health Library &

Information C

enter on July 27, 2011jid.oxfordjournals.org

Dow

nloaded from

During weeks 49–52 of 2009, 31 additional cases were re-

ported (Figure 2); of these, 75% were in individuals aged 9

months to 4 years of age who were therefore eligible for vacci-

nation during the SIA. Starting in week 1 of 2010, weekly case

counts sharply increased, peaked at 92 cases during week 7 in

February 2010, and gradually decreased to 26 cases in week 28

during July 2010. From 1 November 2009 to 13 July 2010, a total

of 1094 confirmed measles cases were reported, and 12 of the 14

districts had R3 laboratory-confirmed measles cases.

Of the 1094 outbreak cases, 970 (89%) included day of rash

onset, and 1083 (99%) had information on age. Among these

cases, 292 (27%) were in individuals ,1 year of age and 424 (39

%) were in individuals 1–4 years of age; age-specific attack rates

were highest (56.4 cases per 100,000 population) among infants

6–8 months of age and those 9–11 months of age (40.6 cases per

100,000 population) (Table 3). Of the 1094 cases (100%) with

information on district, 380 (35%) were from Bo, 233 (21%)

were from Bombali, and 126 (12%) were from Koinadugu; these

3 districts had the highest attack rates in the country. Of the 1094

outbreak cases, 473 (43%) had information on vaccination status

and 462 (42%) had information on age and vaccination status.

Among those individuals with information on vaccination

Table 3. Measles Attack Rate by Age Category, Sierra Leone, 1 November 2009–13 July 2010

Age group No. of casesa Percentage of cases Attack rate, cases per 100,000 population Percentage vaccinatedb

0–5 Months 65 6.0 13.9 0.0

6–8 Months 132 12.2 56.4 1.5

9–11 Months 95 8.8 40.6 32.6

1–4 Years 424 39.2 11.8 36.3

5–9 Years 185 17.1 4.2 22.2

10–14 Years 94 8.7 2.8 18.1

R15 Years 88 8.1 0.7 6.8

Total 1,083 100.0 4.3 23.2

NOTE. SIA, supplemental immunization activity.a Confirmed measles cases reported to the Sierra Leone Ministry of Health and Sanitation (MOHS) measles case-based surveillance system and confirmed by

the MOHS as either immunoglobulin (Ig) M antibody positive or epidemiologically linked to an IgM antibody positive case (10 cases were missing age data).b The number of cases reporting prior vaccination through either routine services or SIA divided by all cases.

Table 2. Measles Cumulative Attack Rates and Measles Vaccine Coverage by District of Residence, Sierra Leone, November 1, 2009–July 13, 2010

Routine

coveragea, %

2009 SIA coverage

District Population Cluster surveyb, % Admin, % CasescAttack rate, cases per

100,000 population

Bo 769,126 69.3 . 98.8 380 49.4

Bombali 689,020 95.6 82.6 101.7 233 33.8

Koinadugu 456,258 68.6 87.9 99.8 126 27.6

Kenema 844,440 86.6 . 98.5 124 14.7

Tonkolili 593,554 98.4 70.9 98.6 70 11.8

Port Loko 770,372 84.6 75.0 97.6 86 11.2

Western area–urban 764,484 49.4 82.1 107.6 44 5.8

Bonthe 231,100 63.6 82.9 97.8 5 2.2

Kono 579,144 85.0 . 103.5 11 1.9

Pujehun 387,734 70.9 . 93.2 6 1.6

Moyamba 426,394 82.0 . 101.8 4 0.9

Kambia 461,230 77.6 91.7 99.0 4 0.9

Kailahun 616,340 71.0 100.0 101.3 1 0.2

Western area–rural 169,807 62.4 91.4 100.3 0 0.0

Total 8,474,996 77.5 83.8 100.7 1094 12.9

NOTE. SIA, supplemental immunization activity.a Mean measles-containing vaccine coverage reported by Expanded Programme of Immunizations, Sierra Leone, from 2002-2009.b Yellow Fever and Measles Post-Campaign Immunization Coverage Survey in Sierra Leone, 12/29/2009-1/30/2010 performed by the World Health Organization,

Statistics Sierra Leone, and EPI Sierra Leone [15].c Confirmed measles cases reported to the Sierra Leone Ministry of Health and Sanitation (MOHS) measles case-based surveillance system and confirmed by

the MOHS as either immunoglobulin (Ig) M antibody positive or epidemiologically linked to an IgM antibody positive case.

Sierra Leone Measles Outbreak, 2009–2010 d JID 2011:204 (Suppl 1) d S265

at CD

C P

ublic Health Library &

Information C

enter on July 27, 2011jid.oxfordjournals.org

Dow

nloaded from

status, 222 (47%) were unvaccinated. A majority of cases in all

age groups were either unvaccinated or had unknown or un-

documented vaccination status (Table 3). Among the outbreak

cases, 9 deaths were reported, including 6 from the Medecins

Sans Frontieres Gondama Hospital in Bo district. Among the 9

reported measles deaths, the mean age of case-patients was 11

months (range, 5 months to 3 years), and 4 (44%) of the deaths

occurred in individuals with reported vaccination.

Virus sequence information was obtained from 11 (73%) of

the oral fluid samples. All 11 sequences represented by GenBank

accession numbers HQ651715-HQ651725 were genotype B3

and were closely related to sequences obtained from measles

cases detected in West Africa during 2009. Measles genotype B3

is the most frequently detected measles genotype in sub-Saharan

Africa [24].

Vaccine EffectivenessAmong the 424 case-patients who were 12–59 months of age,

156 (36%) were vaccinated. VE among children 12–59 months

of age was estimated to be 74%, assuming the PPV to be 68%

and assuming that all case-patients with missing or unknown

vaccination status were unvaccinated.

Susceptibility ProfileThe WHO and UNICEF estimates of MCV1 coverage were %75%

before 1995 and ranged from 28% to 79% during 1996–2009, with

fluctuation during the 1991–2001 civil war (Figure 1). All birth

cohorts since 1990 were targeted by at least 1 measles SIA, and

children 3–4 years and 6–7 years of age were targeted by 2 SIAs. At

the start of the outbreak, in November 2009, children who were 3

years of age were targeted by both the 2006 and 2009 SIAs, and

children aged 6 years were targeted by the 2003 and 2006 SIAs

(Figure 3). Infants 6–8 months of age were too young to be eligible

for the 2009 SIA and were considered to be susceptible to measles

infection due to waning maternal antibodies. From the catch-up

SIA in November 2003 until just before the second follow-up SIA

in November 2009, the estimated cumulative number of suscep-

tible individuals was 2.8–3.2 times the surviving annual birth co-

hort, with ,1000 total reported measles cases during this

timeframe. The 2009 SIA reduced the estimated number of sus-

ceptible individuals by 1 annual birth cohort (Table 4).

DISCUSSION

The 2009–2010 measles outbreak was the largest in Sierra Leone

in the past decade and was likely caused by an accumulation of

individuals who were susceptible to measles, primarily due to

nonvaccination. This outbreak was much smaller than other

outbreaks that have occurred throughout sub-Saharan Africa

during 2009-2010 [7]; the November 2009 SIA was estimated to

have reduced the total number of susceptible individuals by 1

Figure 3. Confirmed measles cases (n5 1083) and estimated susceptible individuals (n5 268,900) by age, Sierra Leone, November 2009–July 2010.*Supplementation immunization activity (SIA); the bracket indicates the age group targeted by the SIA.

S266 d JID 2011:204 (Suppl 1) d Sugerman et al

at CD

C P

ublic Health Library &

Information C

enter on July 27, 2011jid.oxfordjournals.org

Dow

nloaded from

annual birth cohort, likely blunting the magnitude of the out-

break. The wide age distribution of cases (patient age, 0–44

years) indicates that the accumulation of susceptible individuals

occurred over several years; however, the large proportion of

case-patients ,5 years of age (66%) suggests recent gaps in the

quality of SIA implementation and routine vaccination services.

Routine measles vaccination coverage remains suboptimal, and

national estimates have never reached .80%. Despite reported

administrative coverage .100% for the 2009 measles SIA, sur-

vey coverage by verbal history was only 84%, and 48% of out-

break cases occurred among children in the age group that was

targeted by the SIA. These findings highlight the risk of an

outbreak due to the buildup of susceptible individuals among

the ,5-year-old population from vaccine ineligibility (age of 6–

8 months), low vaccination coverage through routine services

(60%–71%), and vaccination coverage below 95% during the

2006 and 2009 SIAs.

In 2009, the WHO released revised measles outbreak response

guidelines that include recommendations for conducting ‘‘se-

lective’’ and ‘‘nonselective’’ outbreak response immunization

(ORI) [25]. Selective ORI includes providing measles vacci-

nation through routine service sites for all unvaccinated children

6–59 months of age or for a specific age group based on the

measles epidemiology and is recommended when a measles

outbreak is suspected. Nonselective ORI refers to a mass vacci-

nation campaign targeting all children in a specific age group

and geographic area and is recommended when a measles out-

break is confirmed and adequate resources are available.

The 2009–2010 measles outbreak started 3 weeks before

implementation of the planned nationwide measles SIA, at the

end of the low season for measles virus transmission. The SIA

may have served as a nonselective ORI and potentially prevented

additional measles cases; however, cases continued to be reported

after the SIA, with high attack rates among children ,5 years of

Table 4. Susceptibility Profile Showing Estimated Number of Individuals Susceptible to Measles by Age in November 2009, SierraLeone

With 2009 SIA Without 2009 SIA

Age in

Nov 2009 Birth year

Routine

coverage in

birth yeara, %

SIA coverage, %bNo. of

susceptible

individuals (31000)c

Cumulative no. of

susceptible

individuals (31000)

No. of susceptible

individuals

(31000)d

Cumulative no. of

susceptible

individuals (31000)2003 2006 2009

0–5 Months 2009 71 . . . 0.0 0.0 0.0 0.0

6–8 Months 2009 71 . . . 42.6 42.6 42.6 42.6

9–11 Months 2009 71 . . 84 4.1 46.8 16.9 59.6

1 Year 2008 66 . . 84 17.9 64.7 73.6 133.1

2 Years 2007 60 . . 84 19.7 84.4 80.7 213.8

3 Years 2006 65 . 83 84 7.8 92.2 31.8 245.6

4 Years 2005 71 . 83 84 4.0 96.2 15.9 261.5

5 Years 2004 76 . 83 . 14.0 110.2 14.0 275.5

6 Years 2003 73 76 83 . 15.2 125.4 15.2 290.7

7 Years 2002 62 76 83 . 5.7 131.1 5.7 296.4

8 Years 2001 50 76 . . 26.8 157.9 26.8 323.3

9 Years 2000 37 76 . . 31.4 189.4 31.4 354.7

10 Years 1999 62 76 . . 21.3 210.7 21.3 376.0

11 Years 1998 68 76 . . 18.7 229.3 18.7 394.6

12 Years 1997 28 76 . . 33.1 262.4 33.1 427.7

13 Years 1996 79 76 . . 14.0 276.4 14.0 441.7

14 Years 1995 43 76 . . 26.6 303.0 26.6 468.3

15 Years 1994 44 76 . . 12.9 315.8 12.9 481.2

16 Years 1993 67 76 . . 8.7 324.5 8.7 489.9

17 Years 1992 61 76 . . 9.5 334.1 9.5 499.4

18 Years 1991 54 76 . . 10.5 344.6 10.5 509.9

19 Years 1990 75 76 . . 6.9 351.5 6.9 516.9

NOTE. SIA, supplemental immunization activity.a World Health Organization and United Nations Children’s Fund estimates of coverage with the first dose of measles-containing vaccine. For 4 years with

missing information (1985–1987, 1989), the estimate from the previous year with an estimate was used.b For the 2009 SIAs, the coverage estimate by cluster survey was used [15]. For the 2003 and 2006 SIAs, administrative coverage was calculated by dividing the

total number of doses administered to children in the target age group by the census-estimated number of children in that age group and subtracting the difference

(17%) between the estimated coverage by verbal history in the 2009 SIA cluster survey and the 2009 reported administrative coverage.c Children ,6 months of age or R20 years of age were considered to be 100% immune.

Sierra Leone Measles Outbreak, 2009–2010 d JID 2011:204 (Suppl 1) d S267

at CD

C P

ublic Health Library &

Information C

enter on July 27, 2011jid.oxfordjournals.org

Dow

nloaded from

age. Children ,9 months of age were too young to be eligible for

routine measles vaccination or for the 2009 SIA, and maternal

antibodies may have waned, placing them at risk in the face of an

outbreak. Some of the 132 cases and 3 deaths that occurred

among infants 6–8 months of age might have been prevented if

WHO-recommended ORI strategies were implemented,

including providing measles vaccination through routine service

sites starting at 6 months of age (selective ORI) or through tar-

geted campaigns in affected districts (nonselective ORI) if

resources were available. However, measles vaccine efficacy is

greatly reduced when given to infants ,9 months of age [26, 27];

therefore, it is recommended by the WHO that infants who

receive measles vaccination before the age of 9 months must be

revaccinated after the age of 9 months with at least a 1-month

interval between doses [25]. If measles vaccination coverage

through routine services and SIAs was higher prior to the out-

break, then infants ,9 months of age may have been otherwise

protected by herd immunity.

The outbreak in Sierra Leone began at the tail end of the rainy

season, the low-transmission period for measles virus (August–

December) and peaked during the high-transmission that oc-

curs during the dry season (January–July); a similar pattern has

been observed in previous large measles outbreaks in West Af-

rica [28–30]. The WHO AFR SIA field guide suggests that SIA

implementation should be during the low-transmission season

for measles virus [17], although it does not specify early, middle,

or late. Considering that large outbreaks may start during the

end of the low transmission season for measles virus leading to

established circulation in the community, the optimal timing for

SIAs in West Africa may be during August–September and prior

to the end of the low-transmission season.

It is postulated that countries are at risk of a measles outbreak

when the number of susceptible children of preschool age ex-

ceeds the size of an annual birth cohort [31]. In this outbreak,

which occurred 3 weeks before the 2009 SIA, the estimated

number of susceptible children % 5 years of age was 1.6 times

greater than the annual birth cohort, although, following the

2009 SIA, the estimated number of susceptible individuals de-

creased to nearly half the annual birth cohort, likely reducing the

overall number of cases. Forty-four cases (6%) were in patients

who were .21 years of age and who were not reached by the

2006 follow-up SIA or 2003 catch-up SIA. A reduction in cases

was noted from children targeted by one SIA (children 2 and 5

years of age) to those reached by overlapping SIAs (children 3–4

years and 6–7 years of age). These findings suggest inadequate

coverage during each SIA and demonstrate the benefits of ex-

panding the age range for follow-up SIAs. Finally, based on the

susceptibility profile, Sierra Leone was at risk for an outbreak

from 2003 until the start of the 2009 SIA. To prevent measles

outbreaks, nationwide SIAs should be implemented in countries

before a build-up of a high number of susceptible individuals

occurs, especially when measles virus continues to circulate in

neighboring countries or when large measles outbreaks are oc-

curring throughout the region.

The findings of this investigation should be considered in light

of several limitations. The extent of community exposure to

measles virus and underreporting of measles cases from health

facilities, including those cases in individuals who never sought

treatment, was unknown; our findings are only representative of

cases reported to the surveillance system. The majority of

outbreak-related cases were in individuals with missing vacci-

nation status, which prevented a more accurate VE screening

value. A higher estimate of PPV would result in higher VE and

would support our conclusion that vaccine failure did not play a

substantial role in the outbreak. The 2003 and 2006 SIA coverage

estimates were based on administratively collected data and were

not validated by a population-based probability survey; if either

the numerator or denominator figures were inaccurate, then

coverage may have been incorrect, as evidenced by admin-

istratively reported SIA coverage .100%, thereby artificially

lowering the estimated number of susceptible individuals.

Despite these limitations, the Sierra Leone measles outbreak

investigation illustrated the benefit of measles SIAs, while

highlighting the challenges that low vaccination coverage pres-

ents to measles control. Ongoing suboptimal routine measles

vaccination coverage in Sierra Leone will lead to periodic mea-

sles outbreaks in the future. To ensure that all children receive

the recommended 2 doses of measles vaccine, improved measles

vaccination coverage through both routine services and SIAs is

needed. Follow-up SIAs must attain high (.95%) vaccination

coverage in all districts and should be completed prior to the end

of the low-transmission season.

Funding

World Health Organization (to A. F., M. N., and T. B.), United Nations

Children’s Fund (to M. -T. G.), the Ministry of Health and Sanitation of

Sierra Leone (to A. W.), and the Centers for Disease Control and Prevention

(to D. E. S. and J. L. G.).

Acknowledgments

We thank the Expanded Programme of Immunization staff in Sierra

Leone; Chantal Akoua-Koffi, Herve Kadjo, Marius Adagba N’Takpe,

Jeannie Gbahouo, Bertin Kouakou, and Aboulaye Ouattara from the

Pasteur Institute in Abidjan, Ivory Coast; Sheilagh Smit, from National

Institute for Communicable Diseases in Johannesburg, South Africa; Li-

kang Xu (Centers for Disease Control and Prevention), for database

management and statistical assistance; and Balcha Masresha (World Health

Organization African Regional Office), for his guidance and support during

this investigation. The findings and conclusions in this report are those of

the authors and do not necessarily represent the official position of the

Centers for Disease Control and Prevention or the MOHS of Sierra Leone.

References

1. World Health Organization. WHA42.32. In: Handbook of resolutions

and decisions of the World Health Assembly and the Executive Board,

2nd ed. Vol III.(1985–1989). Geneva, Switzerland: WHO, 1990.

S268 d JID 2011:204 (Suppl 1) d Sugerman et al

at CD

C P

ublic Health Library &

Information C

enter on July 27, 2011jid.oxfordjournals.org

Dow

nloaded from

http://whqlibdoc.who.int/wha_eb_handbooks/9241652098_Vol3.

pdf. Accessed 20 November 2010.

2. United National Children’s Fund. Plan of action for implementing the

World declaration on the survival, protection, and development of

children in the 1990s. New York, NY: UNICEF, 1990. http://www.

unicef.org/wsc/plan.htm. Accessed 20 November 2010.

3. Centers for Disease Control and Prevention. Progress in global measles

control and mortality reduction, 2000–2006. MMWR Morb Mortal

Wkly Rep 2007; 56:1237–1241.

4. World Health Organization (WHO) African Regional Office. Plan of

action for measles mortality reduction in the African Region, 2001–

2005. Harare, Zimbabwe: WHO African Regional Office, 2000.

5. Centers for Disease Control and Prevention. Measles mortality

reduction-West Africa, 1996–2002. MMWR Morb Mortal Wkly Rep

2008; 55:28–30.

6. Bilous J, Eggers R, Gasse F, et al. A new global immunization vision and

strategy. Lancet 2006; 367:1464–6.

7. Masresha B, Fall A, Eshetu M, et al. Measles Mortality Reduction

and Pre-Elimination in the African Region, 2001–2009. J Infect Dis

2011. doi: 10.1093/infdis/JIR116.

8. United Nations Population Division. World population prospects: the

2008 revision. 2008. http://esa.un.org/unpp/. Accessed 18 March 2011.

9. Human Rights Watch: Sierra Leone Getting away with murder, mu-

tilation, rape. New testimony from Sierra Leone. 1999, 11(3A). http://

www.hrw.org/en/reports/1999/06/24/getting-away-murder-mutila-

tion-and-rape. Accessed 20 November 2010.

10. United Nations Human Development Index. http://hdr.undp.org/en/

statistics/. Accessed 20 November 2010.

11. United Nations Children’s Fund State of the World’s Children 2009.

Maternal and newborn health. http://www.unicef.org/sowc09/docs/

SOWC09-FullReport-EN.pdf. Accessed 20 November 2010.

12. Senessie C, Gage GN, von Elm E. Delays in childhood immunization in

a conflict area: a study from Sierra Leone during civil war. Confl Health

2007; 9:14.

13. National Measles-Malaria Campaign Report, 2006: Sierra Leone

Ministry of Health and Sanitation. https://www.fosalone.org/doc/

FinalM-MCampaign.pdf. Accessed 20 November 2010.

14. World Health Organization (WHO). WHO vaccine-preventable dis-

eases monitoring system 2010 global summary. http://apps.who.int/

immunization_monitoring/en/globalsummary/country-

profileresult.cfm. Accessed 20 November 2010.

15. Yellow fever and measles post-campaign immunization coverage sur-

vey in Sierra Leone, 12/29/2009–1/30/2010: World Health Organ-

ization, Statistics Sierra Leone, and EPI Sierra Leone.

16. Centers for Disease Control and Prevention. Progress toward measles

control—African Region, 2001–2008. MMWR Morb Mortal Wkly Rep

2009; 58:1036–1041.

17. World Health Organization African Regional Office. Measles sur-

veillance guidelines, Jan 2006. http://www.afro.who.int/index.-

php?option=com_content&view=article&id=2383:publications-

measles&catid=1974&Itemid=2734. Accessed 16 March 2011.

18. World Health Organization. Manual for the laboratory diagnosis

of measles and rubella virus infection, 2nd ed. http://www.

who.int/immunization_monitoring/LabManualFinal.pdf. Accessed 20

November 2010.

19. Kremer JR, Nkwembe E, Bola Oyefolu AO, et al. Measles virus strain

diversity, Nigeria and Democratic Republic of the Congo. Emerg Infect

Dis. 2010; 16:1724–1730.

20. McMorrow ML, Gebremedhin G, van den Heever J, et al.

Measles outbreak in South Africa, 2003–2005. S Afr Med J. 2009;

99:314–319.

21. Farrington CP. Estimation of vaccine effectiveness using the screening

method. Int J Epidemiol. 1993; 22:742–746.

22. Goodson JL, Perry RT, Mach O, et al. Measles outbreak in Tanzania,

2006–2007. Vaccine 2010; 28:5979–5985.

23. Sierra Leone standard demographic and health survey. 2008. http://

www.measuredhs.com/countries/metadata.cfm?surv_id5324&ctry_id5

208&SrvyTp5ctry&cn5Sierra%20Leone. Accessed 20 November 2010.

24. Rota PA, Featherstone DA, Bellini WJ. Molecular epidemiology of

measles virus. Curr Top Micribiol Immunol 2009; 330:129–150.

25. World Health Organization. Response to measles outbreaks in measles

mortality reduction strategies; 2009. http://whqlibdoc.who.int/hq/

2009/WHO_IVB_09.03_eng.pdf. Accessed 20 November 2011.

26. Kurubi J, Vince J, Ripa P, Tefuarani N, Riddell M, Duke T. Immune

response to measles vaccine in 6 month old infants in Papua New

Guinea. Trop Med Int Health 2009; 14:167–173.

27. Caceres VM, Strebel PM, Sutter RW. Factors determining prevalence of

maternal antibody to MV throughout infancy: a review. Clin Infect Dis

2000; 31:110–119.

28. Guyer B, McBean AM. The epidemiology and control of measles in

Yaounde, Cameroun, 1968–1975. Int J Epidemiol 1981; 10:263–269.

29. Cummings DA, Moss WJ, Long K, et al. Improved measles surveillance

in Cameroon reveals two major dynamic patterns of incidence. Int J

Infect Dis. 2006; 10:148–155.

30. Ferrari M, Grais R, Bharti N, et al. The dynamics of measles in sub-

Saharan Africa. Nature 2008; 451:679–84.

31. World Health Organization (WHO). Measles vaccines: WHO position

paper. Wkly Epidemiol Rec 2009; 84:349–360.

Sierra Leone Measles Outbreak, 2009–2010 d JID 2011:204 (Suppl 1) d S269

at CD

C P

ublic Health Library &

Information C

enter on July 27, 2011jid.oxfordjournals.org

Dow

nloaded from