Vaccine 29 (2011) 34193423

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Measles susceptibility in children in Karachi, Pak

Sana She sifShahidaa Department ob Department o

a r t i c l

Article history:Received 29 OReceived in reAccepted 24 FAvailable onlin

Keywords:MeaslesPakistanVaccinationSeroprevalenc

ntabln ofme nat504ntiboilies3% osingrepo

thenies are

1. Introduction

Measles elimination is one of the critical elements in achievingthe Millennium Development Goal of reducing the child mortalityby two thirregion, Pakiby 2010 [1,the measlesincidence oassociated min the EMRPakistan whcases per th

In ordercoverage ofcontrol is tomeasles vacgle dose ofEPI programdose was oleft unvaccitial occurre

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measles vaccine supplementary immunization activity (SIA) wasconducted in 20072008 [9]. This campaign was reported to be thelargest measles vaccine campaign in history and reportedly morethan 66 million children aged 9 months to 13years (97% of the

0264-410X/$ doi:10.1016/j.ds by the year 2015. Being a member of WHO EMROstan adopted a resolution in 1997 to eliminate measles2]. To eliminate measles, regional goal was to reduceassociated mortality by 90% by 2010 and to reduce thef measles to 1 case per million [3]. Although measlesortality has been reduced by 90% from 2000 to 2007

O region [4], measles outbreaks continue to occur inere the incidence of measles in 2007 was reported as 2ousand children less than 5years of age [5].to effectively control measles, routine measles vaccine>90% is required [6]. Another key element of measlesensure that every child receives at least two doses of

cine, preferably after 1 year of age [7]. Until 2007, a sin-measles vaccine was being used in Pakistans National

at 9 months of age, and the coverage of this singlenly 60% [8]. Therefore, up to 2 million children werenated against measles every year. Realizing the poten-nce of major measles outbreaks, a nationwide one year

ding author at: Department of Paediatrics and Child, Health, Aga Khandium Road, PO Box 3500, Karachi 74800, Pakistan.864955; fax: +92 21 34934294.ress: asad.ali@aku.edu (A. Ali).

target population) were vaccinated [9].Despite this extensive supplemental immunization campaign,

measles outbreaks have continued to occur in Pakistan. It is there-fore important to determine the effectiveness of this measles SIAby determiningwhat proportion of children is still seronegative formeasles and hence susceptible to the disease. If a signicant pro-portion of children are found to be susceptible, then a strong casefor a repeat and more effective SIA against measles can be made.

2. Methodology

This study was done in Karachi, the largest metropolitan cityof Pakistan located in the Sindh province at the coast of ArabianSea. Karachi comprises of 18 towns [10] and approximately 7750clusters. Children between the ages of 1259 months were eligi-ble for this study if they were living in Karachi for the past threemonths. Sampling frame was a complete line listing of 90 ran-domly selected clusters of Karachi which have the representationfrom all the towns of Karachi. Following the EPI 607 multi stagecluster sampling technique [11], 60 clusters were selected, and atleast 7 children from each cluster were randomly selected from thegiven sampling frame. Data collectors checked for an eligible childin the randomly selected house hold. If an eligible child was notavailable at home after three attempts or if the house was locked,

see front matter 2011 Elsevier Ltd. All rights reserved.vaccine.2011.02.087ikha, Asad Ali a,, Anita K.M. Zaidia, Ajmal Aghab, AQureshia, Iqbal Azamb

f Paediatrics and Child Health, Aga Khan University, Karachi, Pakistanf Community Health Sciences, Aga Khan University, Karachi, Pakistan

e i n f o

ctober 2010vised form 19 January 2011ebruary 2011e 9 March 2011

e

a b s t r a c t

Measles, despite being vaccine prevecountries.We estimated the proportiotan city of Pakistan, one year after thof 20072008. Oral uid specimens ofwere collected to detect measles IgG aThe proportion of children whose famwere 78% and 12% respectively. Onlythrough the SIA. Among the reportednity against measles while among theof measles immunity. Urgent strengvaccination campaigns against measl/ locate /vacc ine

istan

Khowajaa, Salim Allanaa,

e is still a major public health problem in many developingeasles susceptible children in Karachi, the largestmetropoli-

ionwide measles supplementary immunization activity (SIA)randomly selected children from Karachi, aged 1259monthsdies. Measles antibodies were detected in only 55% children.reported receiving a single or two doses of measles vaccinef parents reported that their child received measles vaccinele dose measles vaccine recipients, 58% had serologic immu-rted two dose measles vaccine recipients, 64% had evidence

ng of routine immunization services and high quality massrecommended to achieve measles elimination in Pakistan.

2011 Elsevier Ltd. All rights reserved.

3420 S. Sheikh et al. / Vaccine 29 (2011) 34193423

Total Households approached

N=758

Householdto parci

then the neof householare shownwas presenthe caretakgather inforcation statuof measlesif providednutritional

Oral u(Malvern Mwas collectwas rubbedlower jawsuid samplat the Agasis. We testusing Microford, Middlof measlesagainst measpecicity o93% and 98

3. Sample

Accordin13years of apaign of 20dose of meathe childrenerror of esteffect of 2 tsample sizesample size

4. Statistic

Data weversion 3 aWeighted a

Table 1Baseline clinical and socio-demographic characteristics of study subjects.

Variables Frequency (%)n=504

mont

rs ed

s edu

economic statusb Low 211 (42)Middle 154 (31)High 135 (27)

y of 1st dose measles vaccine No 110 (22)Yes 394(78)Card veried 143 (36)Verbal 251 (64)

y of 2nd dose measles vaccine No 442 (88)Yes 62 (12)Card veried 34 (55)Verbal 28 (45)

y of vaccine through SIA No 488(97)Yes 16 (3)

easles infectionc No 467 (93)Yes 37 (7)

ngd (weight for height) No 437(87)Yes 67 (13)

ngd (height for age) No 307 (61)Yes 197(39)

weightd (weight for age) No 353(70)Yes 151(30)

rmation about a motherand fathers education was missing.rmation of 4 participants were missing. This variable was constructed byusehold items like telephone/mobile, television, refrigerator, air condi-otor cycle, car, washing machine, VCR/DVD player and generator/UPS.Not eligible=8Eligible=750

Household excluded

Locked or eligible child not available=85

Household included=665

consented pate=504

Household not consented to

parcipate=170

Fig. 1. Flow chart of participants.

xt randomly selected house was approached. Numberds approached and number of participant at each stagein Fig. 1. If an eligible child was found and caretakert, then written informed consent was obtained fromer. After consent, a questionnaire was administered tomation of socio-demographic characteristics and edu-s of parents, childs vaccination status and past historyinfection. Childs immunization cards were reviewedand height and weight of each child was recorded forassessment.id was collected by Oracol oral collection devicesedicalDevelopments, Worcester, UK) [12,13]. Sampleed following manufacturers protocol. Oracol devicefor one minute on the base of gums of both upper andinside and out like a toothbrush [12]. The collected oralewas transported in icepacks to the research laboratoryKhan University and stored at 28 C [14] for analy-ed oral uid specimens for antibodies to measles virusimmune IgG capture EIA kit (Microimmune, Brent-

esex, UK) [15]. The accuracy of salivary measurementsIgG antibody as a marker of immunologic protectionsles has been previously validated [14]. Sensitivity and

Age in

Sex

Mothe

Father

Socio-

Histor

Histor

Histor

Past m

Wasti

Stunti

Under

a Infob Info

using hotioner, mf EIA test for measles IgG detection using oral uid is% respectively compared to the serum [16].

size

g to ofcial estimates, 97% children 9 months toge of age receivedmeasles vaccine during the SIA cam-072008. Since the seroconversion rate after a singlesles vaccine is 85%, we expected that 82% (9785%) ofwill have measles IgG. Keeping the 5% bound on the

imation for a 95% condence interval, applying designo adjust for cluster sampling [17] and after inating theby 10% to account for non-responders, our estimatedwas 499.

al analysis

re double entered, checked and validated in Epi datand analyzed by SAS version 9.1 and SPSS version 17.nalysis was done to adjust for cluster sampling [18].

c Diagnosticlopapular rashpresent.

d Using Z sc

Categoricaltinuous varmultiple lowith presenconfounder

5. Results

A total o1259 monbaseline chsubjects watribution ochildren re15 monthshs 1224 126 (25)>2436 128 (25)>3648 143 (28)>4859 106 (21)Mean (SD) 34.7 (13)

Female 251 (50)Male 253 (50)

ucationa No formal education 150 (30)10 years 202 (40)1114 years 132(26)14 years 19 (4)

cationa No formal education 109 (22)10 years 216 (43)1114 years 147 (29)14 years 30 (6)criteria was age of child >5 months and history of fever and macu-or history of cough, coryza or conjunctivitis or peeling of skin was

ore of

S. Sheikh et al. / Vaccine 29 (2011) 34193423 3421

Table 2Factors associated with presence of measles serologic immunity in oral uid among children in Karachi (n=504).

Variables Measles antibodies present Measles antibodies absent Crude OR (95% CI) Adjusted OR (95% CI)Frequency (%) Frequency (%)

OverallHistory of 1sNo (n=109)Card veriedVerbal (n=2History of 2nNo (n=442)Card veriedVerbal (n=2WastingYes (n=67)No (n=437)Mothers eduNo formal (n10years (n1114years>14years (nFathers educNo formal (n10years (n1114years>14years (nAge in month1224 (n=1>2436 (n=>3648 (n=>4859 (n=

Saliva sathe 504 studies against mreported thit was conof second ddren and va34 (55%) suby SIA wasfectionwasp(68%)werein 67 (13%)weight.

Presencewith increavaccinationmeasles vacagainst memeasles vacVerbal reponot associattwo doses omeasles serHowever, thtwo doses.ciation withwas found i

6. Discussi

Our studful nationwchildren inKlence was c82%, whicherage of 97vaccinatedit is highly

d actablial eimatamp. Anoted onen inlikecha

exes,gh-inedge276 (55) 228 (45)t dose measles vaccine

47(43) 62(57)(n=140) 92(66) 48(34)

53) 137(54) 116(46)d dose measles vaccine

236 (53) 206 (47)(n=34) 26(76) 8(24)

8) 14(50) 14(50)

32(48) 35(52)243(56) 194(44)

cation=150) 75 (50) 75(50)=202) 107(53) 95(47)(n=132) 78(59) 54(41)=19) 13(68) 6(32)ation=109) 62(57) 47(43)=216) 111(51) 105(49)(n=147) 82(56) 65(44)=30) 20(6) 10(33)s26) 52 (41) 74 (59)128) 60 (47) 68 (53)143) 89 (62) 54 (38)

106) 74 (70) 32 (30)

mples for serological analysis were available for all ofy subjects. Overall, 276 (55%) childrenhad IgG antibod-easles in their saliva. Caretakers of 394 (78%) children

e receipt of at least a single dose ofmeasles vaccine, andrmed by vaccination card in 143 (36%) subjects. Historyose of measles vaccine was reported by 62 (12%) chil-ccination card documenting the same was provided bybjects. Non routine/extra dose of measles vaccine givenreported by 16 (3%) subjects. History ofpastmeaslesin-resentin37(7%)children. Among these 37 children, 25

found to have serologic immunity.Wastingwas present, 197 (39%) were stunted and 151 (30%) were under-

of serologic immunity against measles was associated

receivean injein ofccial estshowcpaignsestimaonly inchildreareasuniquecompland hiknowlsing age of the child, and with the history of measles. Children with card veried information of single dosecination were more likely to have serologic immunityasles compared to children who had not received thecine (adjusted odds ratio [OR] 2.67, 95% CI 1.395.10).rt alone of receipt of one dose of measles vaccine wased with measles seropositivity. Card-veried receipt off measles vaccine was also associated with increasedopositivity (76%) with adjusted OR of 1.85 (0.64, 5.32).ere were only 34 children with card-veried receipt ofVerbal report of receipt of two doses showed no asso-seropositivity. No difference in presence of immunity

f child was well-nourished or wasted (Table 2).

on

y showed that after one year of a reportedly success-ide measles vaccine SIA, only 55% of 1259 monthsarachiwereprotected againstmeasles. This seropreva-onsiderably less than the expected seroprevalence ofwas calculated by using reported measles vaccine cov-% in the SIA [19]. The proportion of children reportedlythrough the SIA was surprisingly only 3%. We feel thatunlikely that parents would be unaware if their child

of lack of amessaging

We usedserology. Timmunity lspecicity othis non inserologic imprograms feffectivenenization act

Routinereported byThis was hi(PDHS) esti50.7% childin Sindh prour sampleto the agebe that in thcombined ewas limited

Amongvaccine his1 12.56 (1.44,4.53) 2.67 (1.39,5.10)1.58 (0.98,2.54) 1.64 (0.97,2.79)

1 12.94 (1.29, 6.73) 1.85 (0.64, 5.32)0.85 (0.37, 1.96) 0.71 (0.27, 1.88)

1 1(0.81, 2.18) 1.46 (0.82, 2.61)

1 11.13 (0.74, 1.73) 1.18 (0.65,2.15)1.43 (0.90,2.28) 1.52 (0.68,3.41)2.42 (0.75,7.77) 2.17 (0.48,9.66)

1 10.79 (0.50,1.24) 0.61 (0.34,1.10)0.94 (0.57,1.55) 0.58 (0.27,1.27)1.42 (0.62,3.24) 0.69 (0.24,1.94)

1 11.24 (0.76,2.01) 1.34 (0.78,2.28)2.34 (1.44,3.78) 2.84 (1.62,5.00)3.25 (1.88,5.61) 3.82 (2.15,6.77)

non-routine additional dose of measles vaccine as it ise vaccine. There can be several reasons for this disparitystimates and our results. A likely reason is that of-es at the district or province level were exaggerated toaign success, ashasbeen reported forpolio vaccine cam-ther reason could be that 97% coverage was the overallgure from the whole country and our study was donecity. Effortsmayhave beenmore focused on vaccinatingunder-served areas than to vaccinate children in urbanKarachi. Large metropolises such as Karachi presentllenges for vaccinators because of high-rise apartmentsecurity fears, and higher rates of refusals from middlecome households. However, most parents reported noabout the measles SIA campaign. This may be because

ggressive advertisement campaigns, publicity or massthrough electronic or print media.oral uid collected by using a swab to detect measles

his method is now widely used to assess populationevels against measles and has a sensitivity of 93% andf 98%, compared to serum antibody [16,2729]. Withvasive, easy to use technique, evaluation of measlesmunity should be incorporated in measles elimination

or highly endemic countries as a tool to measure thess of both routine and supplementary measles immu-ivities.vaccination with a single dose of measles vaccine was78% of the caretakers of study subjects in our study.

gher than the Pakistan Demographic and Health Surveymate of measles vaccine coverage, which reports thatren of 1223 months were vaccinated against measlesovince [8]. One reason for more vaccinated children inwas the broader age group (1259 months) comparedgroup in PDHS (1223 months). Another reason coulde PDHS data, the proportion of vaccinated children is astimate of Sindh urban and rural areas while our studyto urban areas only.

the single dose measles vaccine recipients in our data,tory of only 36% children could be conrmed by card

3422 S. Sheikh et al. / Vaccine 29 (2011) 34193423

and remaining children had no documentation of measles vaccinealthough caretakers recalled their child as receiving the vaccine.Our results showed that card retention was associated with thepresence of serologic immunity and verbal report alone of childsvaccinationDifferent stvaccine receSome studisource of inverbal infor[21].Our stuof vaccinati

Caretakesecond dosvaccine wawas been gand rubellamajority, sounexpecteddemonstratresulted in0.64, 5.32).of childrenwcine. Althoutwodoses osible explanbefore 9momaternallycine failuremaintenanc

Maternaimmunity.[25]. No tre

Presencewho were wing was conmalnutritioies after vameasles vachildren, annourishedc[26]. Malnoable to meaMalnourishformeaslesmortality.

Our studreport of cation of ourinformationvisited fewkeeping wamation. Hodoesnot assdo correlatpation refupopulationmeasles imthe poor lamothers we

In conclumeasles vadetectableproportionceptible anurgent stre

level high-quality measles vaccination campaign is required. Alsomonitoringandevaluationof vaccination campaignsbyassessmentof measles serologic immunity on national scale should be doneregularly and vaccination strategies should be rened on basis of

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cinesp://ww07.10]letta Hunizinatiwas not associated with the presence of immunity.udies have assessed the reliability of verbal report ofipt versus verication by card or otherwritten records.es suggested that verbal information can be a reliableformation for vaccine surveys [20]. Others showed thatmation gives incorrect estimates of vaccine recipientsdy shows that verbal reportwasanunreliablepredictoron status in children residing in Karachi.rs of only 12% of the children reported receiving thee of measles vaccine. Second routine dose of measless included in Pakistans EPI in 2009 but second doseiven at private sectors in combination with mumps(MMR). As MMR vaccine is not accessible to the vastthis low proportion of second dose recipients is not

. Among card veried two-dose vaccine recipients, 76%ed serological immunity; however small sample sizewide condence intervals (adjusted OR 1.85, 95% C.I.Of note, measles antibody could not be detected in 24%ith card conrmed receipt of twodosesofmeasles vac-

gh the sample sizewas small (only 34 children receivedfmeasles vaccine veried by card documentation), pos-ations for vaccine failure are rst dose of vaccine givennths of age [22]with the potential for interference fromacquired antibody [23]. Other known reasons for vac-are improper administration or improper cold chaine of vaccine [24].l education showed an increasing trend with measlesThis nding was consistent with other studies as wellnd was observed for fathers education.of serologic immunity was not different in childrenell nourished compared to wasted children. This nd-sistent with the existing literature which suggests thatn does not affect the development of measles antibod-ccination [26]. There have been misconceptions aboutccine causing immune-suppression in malnourishedd this sometimes leads to reluctanceof vaccinatingmal-hildrenagainstmeaslesbyhealthproviders andparentsurished children therefore become even more vulner-sles infection, which is most severe in this population.ed children should therefore be a high priority groupvaccination in order to decreasemeaslesmorbidity and

y had some limitations. We had to rely on the verbalretakers regarding vaccination status for a large propor-study children. We were not able to verify this verbalfrom local EPI centers or any otherwritten records.WeEPI centers to get vaccination information but records inconsistent and we failed to nd the required infor-wever, our data show that verbal report of vaccinationociatewithmeasles immunity, but card veried reportse with immunity. Another limitation was the partici-sal rate of almost 26% which could have biased studyselection and resulted in an under or over-estimate ofmunity in population. The major reason for refusal wasw and order situation in the city, due to which manyre reluctant to interact with strangers.sion, our study showed that even after one year ofmass

ccination campaign, only 55% children in Karachi hadmeasles serologic immunity. This shows that a largeof the under 5-year population in Karachi is still sus-d future measles outbreaks are likely. In addition tongthening of routine immunization, immediate mass

serologmeasleunprec

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elimmunity estimates to effectively control and eliminatem this country, specially as Pakistan recovers from theted oods of 2010.

ing

ikh is supported by training grant D43TW007585 fromInternational Center, National Institutes of Health

project was funded by support from the GAVI Alliancem to Aga Khan University.

gements

gratefully acknowledge the support of Huma KhawarAVI Alliance CSO Program, Altaf Bosan (National EPInd Tayyab Nisa for their help in this project.

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Measles susceptibility in children in Karachi, PakistanIntroductionMethodologySample sizeStatistical analysisResultsDiscussionGrant fundingAcknowledgementsReferences