Strategies to increase the demand for childhood vaccination in low- and middle-income countries: a systematic review and meta-analysis

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Systematic reviews

Strategies to increase the demand for childhood vaccination in low-
and middle-income countries: a systematic review and meta-analysis
Mira Johri,a Myriam Cielo Pérez,b Catherine Arsenault,c Jitendar K Sharma,d Nitika Pant Pai,e Smriti Pahwaf &
Marie-Pierre Sylvestrea

    Objective To investigate which strategies to increase demand for vaccination are effective in increasing child vaccine coverage in low- and
    middle-income countries.
    Methods We searched MEDLINE, EMBASE, Cochrane library, POPLINE, ECONLIT, CINAHL, LILACS, BDSP, Web of Science and Scopus databases
    for relevant studies, published in English, French, German, Hindi, Portuguese and Spanish up to 25 March 2014. We included studies of
    interventions intended to increase demand for routine childhood vaccination. Studies were eligible if conducted in low- and middle-income
    countries and employing a randomized controlled trial, non-randomized controlled trial, controlled before-and-after or interrupted time
    series design. We estimated risk of bias using Cochrane collaboration guidelines and performed random-effects meta-analysis.
    Findings We identified 11 studies comprising four randomized controlled trials, six cluster randomized controlled trials and one controlled
    before-and-after study published in English between 1996 and 2013. Participants were generally parents of young children exposed to an
    eligible intervention. Six studies demonstrated low risk of bias and five studies had moderate to high risk of bias. We conducted a pooled
    analysis considering all 11 studies, with data from 11 512 participants. Demand-side interventions were associated with significantly higher
    receipt of vaccines, relative risk (RR): 1.30, (95% confidence interval, CI: 1.17–1.44). Subgroup analyses also demonstrated significant effects
    of seven education and knowledge translation studies, RR: 1.40 (95% CI: 1.20–1.63) and of four studies which used incentives, RR: 1.28
    (95% CI: 1.12–1.45).
    Conclusion Demand-side interventions lead to significant gains in child vaccination coverage in low- and middle-income countries.
    Educational approaches and use of incentives were both effective strategies.

                                                                                    articles published up to 2009.9 In the interim, several new stud-
Introduction                                                                        ies of potentially higher quality have been published.
Almost 40 years after the launch of the World Health Organiza-                           We carried out a systematic review and meta-analysis to
tion’s (WHO’s) Expanded Programme on Immunization, one                              evaluate whether demand-side interventions increase uptake
in five children worldwide still does not have access to basic                      of routine childhood vaccination in low- and middle-income
vaccines.1,2 In May 2012, the World Health Assembly approved                        countries. Our objectives were to ascertain the effect of de-
the Global Vaccine Action Plan to ensure that the full ben-                         mand-side interventions on vaccine coverage and to identify
efits of immunization are extended to people in every region,                       which strategies are effective. We focused on demand-side
country and community.1 Midway through the Global Vaccine                           interventions, since these strategies can more easily reach
Action Plan’s decade of vaccines (2011–2020)1, disparities in                       underserved populations and reduce inequities in immuniza-
vaccine coverage within and between countries persist,3 and                         tion coverage.
the search for effective strategies to reach underserved popula-
tions has gained urgency.                                                           Methods
      Interventions to improve vaccination outcomes are com-
                                                                                    Protocol and registration
monly grouped into those targeting health services delivery
or supply (e.g. improving human resources training, logistics,                      The review protocol was registered in the PROSPERO database
cold chain maintenance and vaccine storage, effective financing,                    (CRD42013005783; available at: http://www.crd.york.ac.uk/
monitoring and evaluation and supportive supervision) and                           PROSPERO/display_record.asp?ID=CRD42013005783). The
those that stimulate demand for vaccines (e.g. monetary or food                     full report, available from the authors, includes both a narra-
incentives, knowledge transfer or communication campaigns).                         tive synthesis and a meta-analysis as outlined in the protocol.
Certain demand-side interventions have been associated with
                                                                                    Eligibility criteria
improved vaccine coverage of children in low- and middle-
income countries in previous systematic reviews.4–9 However,                        We defined six criteria for inclusion of studies in the review
limitations in study quality and design precluded quantitative                      and meta-analysis: (i) based on guidelines developed by
synthesis in these reviews. The most recent review considered                       the Cochrane Effective Practice and Organisation of Care

a
  Centre de Recherche du Centre Hospitalier de l’Université de Montréal (CRCHUM), Tour Saint-Antoine, Porte S03-458, 850 rue St-Denis, Montréal, Québec, H2X 0A9,
  Canada.
b
  Département d’administration de la santé, Université de Montréal, Montréal, Canada.
c
  Department of Epidemiology, Biostatistics and Occupational Health, McGill University, Montréal, Canada.
d
  National Health Systems Resource Centre (NHSRC), Ministry of Health and Family Welfare, New Delhi, India.
e
  Department of Medicine, McGill University, Montréal, Canada.
f
  Pratham Education Foundation (ASER Centre), New Delhi, India.
Correspondence to Mira Johri (email: mira.johri@umontreal.ca).
(Submitted: 8 September 2014 – Revised version received: 5 December 2014 – Accepted: 23 January 2015 – Published online: 23 March 2015 )

Bull World Health Organ 2015;93:339–346C | doi: http://dx.doi.org/10.2471/BLT.14.146951                                                                        339
Systematic reviews
 Childhood vaccination in low- and middle-income countries                                                                          Mira Johri et al.

(EPOC) group, randomized controlled            author translated the strategy and terms
                                                                                                  with more precise estimates. Study-
trial, non-randomized controlled trial,        for the databases in other languages.
                                                                                                  specific estimates of variance were
controlled before-after or interrupted         Identified records were uploaded into
                                                                                                  obtained by deriving standard errors
time series study designs were eligible;10     EndNote (Thomson Reuters, Philadel-
                                                                                                  from the confidence intervals reported
(ii) the study location was a low- and         phia, United States of America) and
                                                                                                  by the studies. For cluster randomized
middle-income country as defined by            duplicates eliminated. Two authors
                                                                                                  controlled trials, we used the standard
the World Bank;11 (iii) the study was          screened titles and abstracts indepen-
                                                                                                  errors with adjustment for clustering,
published in a peer-reviewed scientific        dently and eliminated studies that failed
                                                                                                  which allowed us to use both clustered
journal, because in previous reviews           to meet eligibility criteria. Full texts of
                                                                                                  and non-clustered randomized controls
that considered the grey literature, the       remaining studies were retrieved. Two
                                                                                                  trials in the same meta-analyses. In
quality of these studies was found to          authors independently screened full
                                                                                                  addition to conducting meta-analysis
be low; 4–7 (iv) the participants were         text articles against study inclusion
                                                                                                  on all included studies, we performed
generally parents and caregivers of            criteria and compared results; another
                                                                                                  meta-analysis on five pre-specified sub-
children younger than two years, living        author validated all decisions.
                                                                                                  groups: (i) studies including the third
in communities where interventions
                                               Data extraction                                    dose of diphtheria-tetanus-pertussis
to increase demand for routine child-
                                                                                                  (DTP3); (ii) studies using knowledge
hood vaccination had been carried out;         From each study, two authors indepen-
                                                                                                  transfer interventions; (iii) studies us-
(v) eligible interventions were defined        dently extracted data on study design,
                                                                                                  ing incentives, (iv) studies whose risk
broadly as any intervention that might         aims, location, population, intervention,
                                                                                                  of bias was assessed to be moderate-
increase demand for routine child-             follow-up period and outcomes, using
                                                                                                  to-high; and (v) studies whose risk of
hood vaccination, such as incentives           a pre-defined template (available from
                                                                                                  bias was assessed to be low. We also
of money or food, knowledge transfer           corresponding author). We adopted the
                                                                                                  estimated three meta-regression models
initiatives, or communication cam-             original study definitions of comparator
                                                                                                  adjusting separately for: (i) baseline
paigns (studies that included strategies       or control groups. We pilot tested the
                                                                                                  vaccination coverage (the proportion
targeting vaccine supply in addition           template on a subset of studies. In ad-
                                                                                                  of children aged 12–23 months receiv-
to demand were eligible); and (vi) the         dition to vaccine outcomes, information
                                                                                                  ing DTP3 in the study area or country);
study outcomes included quantitative           on equity and economic outcomes were
                                                                                                  (ii) intervention type; and (iii) study
estimates of routine childhood vaccina-        extracted. Together, three authors cross-
                                                                                                  quality. Heterogeneity was assessed us-
tion coverage.                                 checked and verified these data. Study
                                                                                                  ing Cochrane’s Q-test and I2 statistics.12
                                               authors were contacted for clarification
Information sources                                                                               Potential publication bias was assessed
                                               if data were missing or unclear.
                                                                                                  using funnel plots. Analyses were per-
We searched the MEDLINE (via
                                               Risk of bias                                       formed using the metafor package13 for
Pubmed), EMBASE, Cochrane library,
                                                                                                  meta-analyses in R (R Foundation for
POPLINE, ECONLIT, CINAHL, LI-                  We used Cochrane collaboration criteria
                                                                                                  Statistical Computing, Vienna, Austria)
LACS (Latin America and the Caribbean          to assess risk of bias.12 As these criteria
                                                                                                  and the heterogi package 14 for Stata
Center on Health Sciences Information),        were developed to assess randomized
                                                                                                  (version 13.1, StataCorp LP, College
BDSP (French public health database),          controlled trials, we supplemented
                                                                                                  Station, USA).
Web of Science and Scopus databases            them to accommodate additional study
using appropriate terms and descrip-           designs. To address issues specific to
tors. Searches were limited to articles        cluster randomized controlled trials, we           Results
concerning human data that were writ-          systematically considered recruitment
                                                                                                  Study selection
ten in English, French, German, Hindi,         bias, unit of analysis bias and sample
Portuguese or Spanish. The search began        size as part of the “other” category.12 To         Search of the databases yielded 1705
on 1 September 2008 and was last up-           accommodate non-randomized designs,                citations. We also identified 59 records
dated on 25 March 2014. All published          we used the Cochrane EPOC group’s                  through previous systematic reviews,
studies included in previous systematic        additional criteria and scoring for non-           article bibliographies and subject-matter
reviews4–9 were also considered. We con-       randomized controlled trials, controlled           experts. After removal of 643 duplicate
sulted experts and reviewed article refer-     before-and-after and interrupted time-             records, there were 1121 records for title
ence lists for additional articles.            series studies.10 For each included study,         and abstract screening. Of these, 1073
                                               two authors independently assessed                 did not meet eligibility criteria and were
Search and selection
                                               risk of bias and compared results, and             excluded. The full text of the remaining
One of the authors and an academic             another author validated all decisions.            48 articles was retrieved for detailed
librarian defined the MEDLINE search                                                              review (available from corresponding
                                               Statistical analysis
strategy (available from corresponding                                                            author). It lists the 37 articles excluded af-
author). Search terms were combina-            The principal measure was the rela-                ter full-text evaluation and the principal
tions of “interventions”, “programs”,          tive risk (RR) of vaccination among                reasons for their exclusion. A total of 11
“approaches”, “subsidies”, “knowledge          children in intervention versus control            studies15–25 comprising four randomized
translation”, “vouchers”, “vaccination”,       groups. We performed a meta-analysis               controlled trials, six cluster randomized
“immunization”, “vaccines”, “child”,           by estimating random effect models                 controlled trials and one controlled
“infant”, “newborn”, “kid”, and “low-          with inverse variance weighting. This              before-and-after study were included in
and middle-income countries”. The              method gives greater weight to studies             the review (Fig. 1 and Table 1).

340                                                            Bull World Health Organ 2015;93:339–346C| doi: http://dx.doi.org/10.2471/BLT.14.146951
Systematic reviews
Mira Johri et al.                                                                                     Childhood vaccination in low- and middle-income countries

Study characteristics                                   Fig. 1. Interventions to increase the demand for childhood vaccination: selection of
Study inclusion                                                 studies
The 11 studies were published in Eng-
lish between 1996 and 2013; eight were                   1705 records identified through database searching:
from lower-middle income countries15–22                   • 368 in Medline (56 with keywords)
and three were from low-income coun-                      • 95 in CINAHL
                                                          • 390 in PUBMED                                                             59 additional records identified through
tries. 23–25 Study locations included                     • 99 in LILACS                                                              other sources:
south Asia (n = 7), 15–20,23 sub-Saharan                  • 202 in ECONLIT                                                             • 18 from experts
Africa (n = 3),22,24,25 and central America               • 304 in POPLINE                                                             • 20 from previous reviews
(n = 1).21                                                • 111 EMBASE                                                                 • 21 from reference lists
                                                          • 53 in BDSP
Participants                                              • 83 in Cochrane Library
                                                                                                                                      1073 excluded after screening
Data were collected from 11 512 par-                                                                                                  titles and abstracts:
ticipants yielding outcomes for 11 512                                                                                                 • not an intervention study
children. As many interventions were                                                         1764 records screened                     • not a primary study
directed to communities or populations                                                                                                 • not in a low- or middle-income country
                                                                                                                                       • not about routine childhood
rather than to individuals, the number of                                                                                                immunization
individuals reached by the interventions                                            1121 records after duplicates removed              • not a demand-side intervention
was considerably larger. Participants                                                                                                  • not an intervention to increase
were mothers, caregivers, households of                                                                                                  vaccination uptake
children who were within the target age-
                                                                                   48 full-text articles assessed for eligibility
group for immunization (n = 9),15–18,21–25                                                                                            37 full-text articles excluded:
or the general populations of target                                                                                                   • 10 supply-side interventions
communities (n = 2).19,20                                                                                                              • 8 no control group
                                                                                  11 studies included in the systematic                • 5 not about routine childhood
Interventions                                                                     review and meta-analysis:                              immunization
                                                                                   • 7 education or knowledge translation              • 5 immunization campaigns
Of the 11 studies, seven described educa-                                            interventions                                     • 3 not an intervention study
tion or knowledge translation interventi                                           • 4 incentive interventions                         • 2 study design does not satisfy EPOC
                                                                                                                                         criteria for admissibility
ons, 15–17,19,20,22,23 while four described
                                                                                                                                       • 2 duplicate
interventions using incentives.18,21,24,25                                                                                             • 1 no quantitative evidence on coverage
Of the latter, two considered monetary                                                                                                 • 1 outcome data unavailable
incentives,21,24 and two non-monetary
incentives.18,25 One study compared two                 EPOC: Effective Practice and Organisation of Care.
types of monetary incentives;24 thus, the               CINAHL: Cumulative Index to Nursing and Allied Health Literature
11 studies yielded data on 12 interven-                 PubMed: Public MEDLINE
                                                        LILACS: Latin-American and Caribbean Center on Health Sciences Information
tions. Four studies considered both                     ECONLIT: The American Economic Association’s electronic bibliography
demand and supply interventions to im-                  POPLINE: Free resource from the John Hopkins Bloomberg School of Public Health
prove vaccine coverage.16–18,21 For these               EMBASE: Elsevier’s biomedical database
studies, meta-analyses were based on                    BDSP : Banque de Données en Santé Publique
the estimated demand-side effect.16–18,21
Outcomes
                                                       age-appropriate vaccination.25 The tim-                               but only two provided stratified analyses
Nine studies undertook coverage sur-                   ing of outcome measures was variable.                                 related to subgroups of interest.17,20
veys to assess outcomes, 15,18–25 while                While some studies addressed on-time
                                                                                                                             Risk of bias
two used administrative data.16,17 For                 delivery, a majority focused on the
six studies, the main aim of the inter-                simpler assessment of presence or ab-                                 We assessed risk of bias for nine cri-
vention was to increase immunization                   sence of vaccinations within a specified                              teria. Our assessments ranged from
coverage,15–19,22 while for five studies,              period. This period was based on the                                  low risk of bias on all criteria in one
improving immunization coverage was                    age of the child at the time outcomes                                 study 18 to high risk of bias on five cri-
a secondary aim and data on immuni-                    were assessed and varied between stud-                                teria in one study. 25 For the purpose of
zation outcomes were included.20,21,23–25              ies: less than one year,15–17,20,25 less than                         subgroup analyses, we classified five
                                                       two years,19,22 less than three years,18,21 or                        studies with high risk of bias on one
Vaccination outcomes
                                                       less than five years.23,24                                            or more criteria as moderate-to-high
Four studies described full immuniza-                        One study recorded changes in im-                               risk of bias.20,21,23–25 The remaining six
tion as defined by the country’s immu-                 munization knowledge, attitudes and                                   studies were categorised as low risk of
nization schedule, all of which contain                beliefs19 and two estimated intervention                              bias. 15–19,22 Fig. 2 presents a summary
DTP3 as a subset. 18,22–24 Six studies                 costs and cost–effectiveness,18,19 as ad-                             of our assessment of the risk of bias
presented information on DTP3 vacci-                   ditional vaccination-related outcomes.                                (a detailed assessment for each study
nation.15–17,22–24 Three studies presented             All studies considered equity in the                                  and criterion, and figure summarizing
information on receipt of one or more                  choice of target populations by directing                             risk of bias assessments by criterion is
vaccine doses18,20,21 and one considered               interventions to areas of greater need,                               available from corresponding author)

Bull World Health Organ 2015;93:339–346C| doi: http://dx.doi.org/10.2471/BLT.14.146951                                                                                            341
Systematic reviews
 Childhood vaccination in low- and middle-income countries                                                                                        Mira Johri et al.

 Fig. 2. Interventions to increase the demand for childhood vaccination: summary of the risk of study bias

                                           Andersson Banerjee     Briere     Brugha     Morris     Owais     Pandey Robertson         Roy      Usman      Usman
                                             2009     2010        2012        1996      2004       2011       2007    2013           2008       2009       2011

         Random sequence generation
                     (selection bias)

               Allocation concealment
                        (selection bias)

                             Blinding
 (performance bias and detection bias)

             Incomplete outcome data
                       (attrition bias)

                 Adequately protected
                against contamination

                   Selective reporting
                      (reporting bias)

                               Baseline
                  charateristics similar

                   Baseline outcome
                measurements similar

                             Other bias

                                              High risk of bias       Unclear risk of bias       Low risk of bias

High risk of bias occurred most fre-                     receipt of vaccines (RR: 1.30; 95% CI:
                                                                                                                Subgroup analyses
quently for the category “other bias”                    1.17–1.44), but there was consider-
(five studies), while unclear risk of                    able heterogeneity (I2 = 88.96; 95% CI:                The overall effect of educational or
bias was most frequent for the category                  82.94– 92.16). Unweighted results were                 knowledge translation interventions was
“selective reporting” (nine studies).                    similar to weighted results (RR: 1.34;                 greater than for incentives RR: 1.40 (95%
Risk of bias was related to intervention                 95% CI: 1.21−1.50). To reduce diversity                CI: 1.20–1.63) versus RR: 1.28 (95% CI:
type: three of the four studies that used                associated with outcomes measured,                     1.12–1.45), respectively (available from
incentives had moderate-to-high risk                     we considered only the nine studies                    corresponding author). The pooled
of bias.21,24,25                                         reporting data for DTP3 or full vac-                   analysis considering studies with a low
                                                         cination (information available from                   risk of bias yielded a higher estimate
Receipt of vaccine
                                                         corresponding authors). These results                  of overall effect than that for studies
RR estimates, 95% confidence intervals                   were similar to those for all studies (RR:             with moderate-to-high risk of bias,
(CI) and weights for each individual                     1.32; 95% CI: 1.15–1.51; I2 = 86.31; 95%               RR: 1.53 (95% CI: 1.28−1.82) and RR:
study are shown in Fig. 3. For each study,               CI: 75.31–91.11).                                      1.15 (95% CI: 1.02–1.30), respectively
the crude proportion of participants                                                                            (available from corresponding author).
                                                         Bias across studies
with and without vaccination is shown                                                                           Heterogeneity was lower for educational
separately for intervention and control                  To explore potential sources of heteroge-              or knowledge translation interven-
groups. For one study, Morris et al.,21                  neity, we plotted the observed outcome                 tions: I2 = 80.48, (95% CI: 53.90–88.88)
data necessary for meta-analysis were                    against the standard error for all meta-               than for incentives I2 = 89.40, (95% CI:
not available in the text or from the                    analyses and meta-regressions. Visual                  76.83–93.73). Heterogeneity was also
study author and were taken from a                       inspection of funnel plots revealed no                 lower for studies with low risk of bias:
published article.26                                     evidence of asymmetry (available from                  I2 = 79.16, (95% CI: 42.92−88.82) versus
    In the pooled analysis consider-                     corresponding author); however, due to                 studies with moderate-to-high risk of
ing all 12 interventions assessed in the                 the small number of studies the test has               bias: I2 = 90.26, (95% CI: 81.40–93.86).
11 studies (Fig. 3), interventions were                  low power and we cannot exclude the                    Meta-regression revealed no important
associated with significantly higher                     possibility of publication bias.                       differences in results by baseline cover-

342                                                                          Bull World Health Organ 2015;93:339–346C| doi: http://dx.doi.org/10.2471/BLT.14.146951
Systematic reviews
Mira Johri et al.                                                                                 Childhood vaccination in low- and middle-income countries

 Fig. 3. Interventions to increase the demand for childhood vaccination: meta-analysis of 11 studies

                                                          Children vaccinated/total
   Author(s) and year                                     Intervention     Control    Weights %        RR (95% CI)                          RR (95% CI)
   Brugha and Kevany, 1996                                   171/200       137/219         9.21        1.40 (1.23–1.59)
   Morris et al., 2004                                          -             -           10.38        1.07 (1.01–1.13)
   Pandey et al., 2007                                       107/149        36/79          9.57        1.57 (1.41–1.75)
   Roy et al., 2008                                           64/126        60/104         6.78        0.88 (0.69–1.12)
   Andersson et al., 2009                                    283/535       103/422         3.94        2.17 (1.43–3.29)
   Usman et al., 2009 – received education only              242/375       205/375         9.36        1.18 (1.05–1.33)
   Banerjee et al., 2010 – intervention B vs A               148/382        68/379         6.55        2.16 (1.68–2.78)
   Owais et al., 2011                                        129/179        92/178         6.22        1.39 (1.06–1.82)
   Usman et al., 2011                                        228/376       149/378         8.04        1.50 (1.25–1.80)
   Briere et al., 2012                                      1062/1607      382/723        10.10        1.25 (1.16–1.35)
   Robertson et al., 2013 – unconditional cash transfer      393/517       253/360         9.92        1.08 (0.99–1.18)
   Robertson et al., 2013 – conditional cash transfer        317/417       253/360         9.92        1.08 (0.99–1.18)

   Total                                                                                 100.00         1.30 (1.17–144)

                                                                                                                                        0.61 1 1.65           4.48
                                                                                                                              Favours control Favours intervention
 CI: confidence interval; RR: relative risk.
 Note: Weights are from random-effects analysis.

age level. Results for meta-regressions                   challenges confronted the studies re-                     by international agencies to assess im-
by intervention type and study quality                    viewed: (i) increases in demand cannot                    munization coverage and was included
were consistent with the corresponding                    be effective if supply-side constraints                   in nine of the 11 papers reviewed.3 All
meta-analyses.                                            limit provision of vaccines;21,25 (ii) if                 analyses consistently showed that de-
                                                          coverage rates are already very high,                     mand-side interventions are beneficial
                                                          there is limited scope to demonstrate                     in improving coverage. However, due
Discussion                                                improvement;24,25 and (iii) vaccination                   to diversity in outcomes and the small
This meta-analysis demonstrates that                      rates can be affected by changes in ser-                  number of studies, we cannot evaluate
demand-side interventions lead to an                      vice delivery occurring independently of                  the effect of interventions for specific
increase in child vaccination coverage in                 the study. Among the studies reviewed,                    vaccines.
diverse low- and middle-income settings                   only one study did not show a gain as-                         Fourth, health gains depend not
and among communities with lagging                        sociated with the intervention: in this                   only on increased vaccine coverage
health and social indicators. Immuni-                     study, all experimental groups experi-                    but also on appropriate timing of vac-
zation programmes have often focused                      enced substantial but similar gains in                    cination. With one exception,25 studies
on strengthening vaccine supply. Our                      vaccination coverage.23 Another study                     offered little information on when doses
results show that policymakers who seek                   noted a likely background trend with                      were delivered.
to increase access to vaccines through                    a differential impact on experimental                          Fifth, despite contacting the au-
the routine immunization system should                    groups.25 Unfortunately, neither of these                 thors, we were not able to retrieve data
also consider demand-side strategies.                     studies collected data on health system                   for all studies and had to use approxi-
     Educational or knowledge transla-                    trends that might affect immunization                     mate values for one study 21 based on
tion interventions were more effective                    delivery. Studies addressing vaccine and                  another publication.26
on average than interventions based on                    non-vaccine outcomes, including three                          Sixth, our analysis excluded inter-
incentives; however, both strategies were                 of the four incentive based studies21,24,25               ventions that focused exclusively on im-
effective. The highest estimates of effect                may have faced challenges related to                      proving vaccine supply. However, from a
and lowest heterogeneity were found                       broad study scope or a lack of vaccine-                   policy point of view, how demand-side
among studies with low risk of bias. Risk                 specific expertise in study planning. In                  interventions interact with supply side
of bias was related to intervention type,                 addition, two studies of financial incen-                 constraints is also important. With one
with three of the four incentives studies                 tives21,24 were large-scale interventions                 exception,18 immunization system per-
having moderate-to-high risk of bias.                     and faced substantial implementation                      formance was not explicitly assessed by
     Our analysis has six important                       challenges.                                               these studies.
limitations. First, vaccination cover-                         Second, the systematic review and                         Our results indicate that future
age is shaped by interrelated supply                      meta-analysis included only 11 stud-                      research on demand-side interven-
and demand factors. Many studies,                         ies. This limited our ability to explore                  tions to increase vaccine coverage
particularly those tackling vaccine and                   potential sources of heterogeneity quan-                  should (i) standardize measurement
non-vaccine outcomes,20,21,23–25 did not                  titatively and to exclude possible biases                 of outcomes; (ii) include vaccination
give due consideration to the role of                     related to publication and study size.                    experts during the study design phase;
the health system in delivering vaccines                       Third, studies measured different                    and (iii) collect data on health system
during the study design phase leading to                  vaccines over different time periods. Re-                 characteristics that may affect vaccine
increased risk of bias. Three supply-side                 ceipt of DTP3 is the measure preferred                    delivery.

Bull World Health Organ 2015;93:339–346C| doi: http://dx.doi.org/10.2471/BLT.14.146951                                                                           343
Systematic reviews
 Childhood vaccination in low- and middle-income countries                                                                          Mira Johri et al.

                                               coverage related to financial constraints,         interventions can be delivered effectively
Conclusion                                     opportunity costs, knowledge and                   at scale and in the long term. ■
Demand-side interventions are effective        prioritization. Future research should
in improving the uptake of childhood           seek to refine our understanding of                Acknowledgements
vaccines delivered through routine             which approaches are most effective in             We thank Diego Bassani, Hospital for
immunization services in low- and              specific contexts. Studies investigating           Sick Kids, Toronto, Canada.
middle-income countries. Our results           the value of knowledge translation and
are more definitive than those of previ-       incentives-based interventions offered             Funding: The Canadian Institutes for
ous systematic reviews which employed          in combination are also required. Stud-            Health Research (299960) and the
narrative synthesis techniques.4–9             ies that simultaneously consider sup-              Bill & Melinda Gates Foundation
    Demand-side strategies to improve          ply- and demand-side interventions                 (OPP1067851) funded this study.
vaccination coverage are important             – and enable us to evaluate their relative
because they are inherently equity-            effectiveness – are of particular interest.        Competing interests: None declared.
oriented and address specific barriers to      Finally, studies should consider whether

                                                                                                                                        ‫ملخص‬
                                 :‫اسرتاتيجيات زيادة الطلب عىل متنيع األطفال يف البلدان املنخفضة الدخل واملتوسطة الدخل‬
                                                                                           ‫مراجعة منهجية وحتليل تلوي‬
‫ منشورة باللغة اإلنجليزية‬،‫ودراسة واحدة مضبطة ملا قبل وملا بعد‬         ‫الغرض استقصاء لتحديد االسرتاتيجيات الفعالة يف زيادة الطلب‬
‫ كان املشاركون يف األغلب آبا ًء لصغار‬.2013‫ و‬1996 ‫ما بني‬               ‫عىل التغطية بخدمات متنيع األطفال يف البلدان املنخفضة الدخل‬
‫ أظهرت ست دراسات مستوى‬.‫األطفال املعرضني لتدخل مؤهل‬                                                              .‫واملتوسطة الدخل‬
‫ وكان لدى مخس دراسات مستوى‬،‫منخفض من اختطار التحيز‬                     EMBASE‫ و‬MEDLINE ‫الطريقة بحثنا يف قواعد معطيات‬
             ً ‫ أجرينا حتلي‬.‫متوسط إىل مرتفع من اختطار التحيز‬
‫ال جتميعي ًا مع‬                                                       ‫ و‬ECONLIT‫ و‬POPLINE‫ و‬Cochrane ‫ومكتبة‬
‫ مع بيانات من‬،‫األخذ يف االعتبار مجيع الدراسات اإلحدى عرش‬              Scopus‫ وويب العلوم و‬BDSP‫ و‬LILACS‫ و‬CINAHL
‫ ارتبطت التدخالت من جانب الطلب بارتفاع‬.‫ مشارك ًا‬11512                 ‫ منشورة باللغة اإلنجليزية والفرنسية‬،‫عن دراسات ذات صلة‬
‫؛ (بنسبة‬1.30 :‫ االختطار النسبي‬،‫تلقي اللقاحات بشكل ملحوظ‬               .2014 ‫ مارس‬25 ‫ حتى‬،‫واألسبانية والربتغالية واألملانية واهلندية‬
‫كام أظهرت حتليالت‬.)1.44 ‫ إىل‬1.17 :95% ‫أرجحية مقدارها‬                  ‫ضممنا دراسات التدخل التي هتدف إىل زيادة الطلب عىل متنيع‬
‫املجموعات الفرعية آثار ًا ملحوظة لسبع دراسات ترمجة تعليمية‬            ‫ تصبح الدراسات مؤهلة يف حالة إجرائها‬.‫األطفال الروتيني‬
:95% ‫ (بنسبة أرجحية مقدارها‬1.40 :‫ االختطار النسبي‬،‫ومعرفية‬             ‫ وإذا اعتمدت‬،‫يف البلدان املنخفضة الدخل واملتوسطة الدخل‬
‫ االختطار‬،‫) وألربع دراسات استخدمت احلوافز‬1.63 ‫ إىل‬1.20                ‫ أو جتربة غري معشاة مضبطة‬،‫عىل جتربة معشاة مضبطة بالشواهد‬
.)1.45 ‫ إىل‬1.12 :95% ‫ (بنسبة أرجحية مقدارها‬1.28 :‫النسبي‬               ‫ أو تصميم سالسل‬،‫ أو جتربة مضبطة ملا قبل وملا بعد‬،‫بالشواهد‬
‫االستنتاج أدت التدخالت من جانب الطلب إىل مكاسب ملحوظة‬                 ‫ قمنا بتقدير اختطار التحيز باستخدام الدالئل‬.‫متقطعة‬ِّ    ‫زمنية‬
‫يف جمال التغطية بخدمات متنيع األطفال يف البلدان املنخفضة الدخل‬                ً ‫ وأجرينا حتلي‬،Cochrane ‫اإلرشادية التعاونية ملكتبة‬
                                                                      ‫ال تلوي ًا‬
‫ كانت كل من األساليب التعليمية واستخدام‬.‫واملتوسطة الدخل‬                                                           .‫لآلثار العشوائية‬
                                     .‫احلوافز اسرتاتيجيات فعالة‬       ‫ دراسة تتألف من أربع جتارب معشاة مضبطة‬11 ‫النتائج توصلنا إىل‬
                                                                      ،‫ وست جتارب عنقودية معشاة مضبطة بالشواهد‬،‫بالشواهد‬

摘要
在中低收入水平的国家提高儿童接种疫苗需求的策略 : 系统评价和荟萃分析
目的 旨在调查何种增加疫苗接种需求的策略能够有效 倚风险 , 并且进行了随机荟萃分析。
提高中低收入水平国家中儿童接种疫苗的覆盖率。                  结果 我们在 1996 年和 2013 年期间鉴定了 11 项英文
方法 我们搜索了美国联机医学文献分析和检索系统 版研究 , 其中包括四项随机对照试验、六项整群随机
(MEDLINE)、荷兰医学文摘数据库 (EMBASE)、考克兰 对照试验和一项前后对照研究。参与者一般为接受合
(Cochrane) 图书库、人口信息数据库 (POPLINE)、经济 格干预的幼儿的父母。六项研究的偏倚风险较低 , 而
学文献资料库 (ECONLIT)、护理学数据库 (CINAHL)、 五项研究具有中高级偏倚风险。我们针对从 11 512 名
拉丁美洲和加勒比健康科学文献库 (LILACS)、公共卫 参与者处获得数据的 11 项研究全面开展汇整分析。需
生数据库 (BDSP)、科学网 (Web of Science) 以及斯高帕 求方面的干预措施会大大提高疫苗接种率 , 相对风险
斯 (Scopus) 数据库 , 旨在查找以英语、法语、西班牙语、 (RR) 为 :1.30,(95% 置信区间 ,CI:1.17–1.44)。小群组分
葡萄牙语、德语和印地语出版的相关研究资料 , 这项 析也论证了七项教育和知识翻译研究的重要作用 ,RR
工作的时间将一直持续到 2014 年 3 月 25 日。我们囊 为 :1.40 (95% CI:1.20–1.63), 以及四项采用激励措施的
括了意在提高常规儿童接种疫苗需求的干预研究。如 研究的重要作用 ,RR 为 :1.28 (95% CI: 1.12–1.45)。
果研究是在中低收入水平的国家开展 , 并且开展时采 结论 需求方面的干预措施能够大大提高中低收入水平
用的方法为随机对照试验、非随机对照试验、前后对 的国家中儿童接种疫苗覆盖率的成果。教育方法和使
照或间断时间序列设计 , 则该研究符合条件。我们通 用激励措施都是有效的策略。
过科克伦协作网 (Cochrane collaboration) 指南评估了偏

344                                                            Bull World Health Organ 2015;93:339–346C| doi: http://dx.doi.org/10.2471/BLT.14.146951
Systematic reviews
Mira Johri et al.                                                                          Childhood vaccination in low- and middle-income countries

Résumé
Stratégies pour accroître la demande de vaccination des enfants dans les pays à revenu faible et intermédiaire : examen
systématique et méta-analyse
Objectif Déterminer, parmi les stratégies visant à accroître la demande           une étude contrôlée avant et après, qui ont été publiées en anglais
de vaccination, celles qui sont efficaces pour augmenter la couverture            entre 1996 et 2013. Les participants étaient généralement les parents
vaccinale des enfants dans les pays à revenu faible et intermédiaire.             de jeunes enfants exposés à une intervention éligible. Six études
Méthodes Nous avons recherché, dans les bases de données                          montraient un faible risque de biais et cinq études avaient un risque
MEDLINE, EMBASE, de la bibliothèque Cochrane, POPLINE, ECONLIT,                   de biais moyen à élevé. Nous avons réalisé une analyse combinée en
CINAHL, LILACS, BDSP, Web of Science et Scopus, des études à ce                   tenant compte des 11 études, avec des données provenant de 11 512
sujet, publiées en allemand, en anglais, en espagnol, en français, en             participants. Les interventions axées sur la demande étaient associées
hindi, et en portugais, jusqu’au 25 mars 2014. Nous avons inclus les              à une administration de vaccins sensiblement plus élevée, risque relatif
études relatives à des interventions visant à accroître la demande de             (RR) : 1,30; intervalle de confiance de 95%, IC : 1,17-1,44). L’analyse de
vaccination systématique des enfants. Les études étaient recevables si            sous-groupes a également montré des effets importants pour sept
elles avaient été menées dans des pays à revenu faible et intermédiaire           études décrivant des interventions d’éducation ou d’application des
et si elles étaient de type essai contrôlé randomisé, essai contrôlé non          connaissances, RR : 1,40 (IC de 95% : 1,20–1,63) et pour quatre études
randomisé, contrôle avant et après ou étude de séries temporelles                 décrivant le recours à des incitations, RR : 1,28 (IC de 95% : 1,12-1,45).
interrompues. Nous avons estimé le risque de biais suivant les directives         Conclusion Les interventions axées sur la demande entraînent des
de la collaboration Cochrane et avons réalisé une méta-analyse à effets           avantages notables pour la vaccination des enfants dans les pays à
aléatoires.                                                                       revenu faible et intermédiaire. Les démarches éducatives ainsi que
Résultats Nous avons relevé 11 études, comprenant quatre essais                   le recours à des incitations étaient tous deux des stratégies efficaces.
contrôlés randomisés, six essais contrôlés randomisés en grappes et

Резюме
Стратегии повышения спроса на вакцинацию детей в странах с низким и средним уровнем доходов:
систематический обзор и метаанализ
Цель Определить, какие стратегии для увеличения спроса на                         контро лируемых исс ле довани я, шес ть к лас терных
вакцинацию оказываются эффективными и позволяют расширить                         рандомизированных контролируемых исследований и одно
охват вакцинацией детей в странах с низким и средним уровнем                      исследование, контролируемое перед началом и после
доходов.                                                                          окончания. Участники этих исследований — это в основном
Методы Был выполнен поиск исследований, опубликованных                            родители маленьких детей, в отношении которых применялась
на английском, французском, испанском, португальском,                             оправданная интервенция. Шесть исследований показали
немецком языках и хинди до 25 марта 2014 г., в базах данных                       низкий риск системной ошибки. Другие пять — умеренный и
MEDLINE, EMBASE, Кокрановской библиотеки, POPLINE, ECONLIT,                       высокий риск системной ошибки. Был проведен объединенный
CINAHL, LILACS, BDSP, Web of Science и Scopus. Поиск охватывал                    анализ с учетом всех 11 исследований, включающий данные 11
исследования интервенций, направленных на повышение спроса                        512 участников. Интервенции, направленные на повышение
на плановую вакцинацию детей. Отбирались исследования,                            спроса, были связаны со значительно более активным согласием
которые проводились в странах с низким и средним уровнем                          на вакцинацию. Относительный риск (ОР) составил 1,30 (95 %
доходов и включали рандомизированные контролируемые                               доверительный интервал, ДИ: 1,17–1,44). Анализ в подгруппах
испытания, нерандомизированные контролируемые испытания,                          также продемонстрировал значительный эффект в семи
испытания, контролируемые перед началом и после окончания,                        исследованиях, связанных с информированием и передачей
и испытания методом прерванного временного ряда. Оценка                           знаний, ОР: 1,40 (95 % ДИ: 1,20–1,63), и в четырех исследованиях,
риска системной ошибки осуществлялась согласно руководящим                        в которых использовались льготы, ОР: 1,28 (95 % ДИ: 1,12–1,45).
принципам организации «Кокрановское сотрудничество».                              Вывод Интервенции, направленные на повышение спроса
Кроме того, был проведен метаанализ по модели со случайными                       на вакцинацию, приводят к значительному расширению
эффектами.                                                                        охвата вакцинацией детей в странах с низким и средним
Результаты Были выявлены 11 исследований, опубликованных                          уровнем доходов. Свою эффективность показали как стратегии
на английском языке в 1996–2013 гг.: четыре рандомизированных                     информирования, так и использование льгот.

Resumen
Estrategias para incrementar la demanda de vacunación infantil en países de ingresos bajos y medios: una revisión sistemática
y un metanálisis
Objetivo Investigar qué estrategias para incrementar la demanda                   marzo de 2014. Se incluyeron estudios de intervenciones con el objetivo
de vacunación son efectivas en el incremento de la cobertura de                   de incrementar la demanda de vacunación infantil sistemática. Los
vacunación infantil en países de ingresos bajos y medios.                         estudios fueron elegibles si se realizaron en países de ingresos bajos y
Métodos Se realizaron búsquedas en las bases de datos de MEDLINE,                 medios y utilizaron un diseño de ensayo controlado aleatorizado, ensayo
EMBASE, Cochrane Library, POPLINE, ECONLIT, CINAHL, LILACS, BDSP,                 controlado no aleatorizado, controlado antes y después o de series
Web of Science y Scopus para encontrar estudios pertinentes, publicados           temporales interrumpidas. Se estimó un riesgo de sesgo mediante las
en alemán, español, francés, hindi, inglés y portugués hasta el 25 de             directrices de colaboración de Cochrane y se realizaron metanálisis de

Bull World Health Organ 2015;93:339–346C| doi: http://dx.doi.org/10.2471/BLT.14.146951                                                                  345
Systematic reviews
     Childhood vaccination in low- and middle-income countries                                                                                                  Mira Johri et al.

efectos aleatorios.                                                                         se relacionaron con una recepción de las vacunas significativamente
Resultados Se identificaron 11 estudios que abarcan cuatro ensayos                          superior, riesgo relativo (RR): 1,30, (intervalo de confianza, IC, del
controlados aleatorizados, seis ensayos controlados aleatorizados por                       95%: 1,17–1,44). Los análisis de los subgrupos también demostraron
conglomerados y un estudio controlado antes y después, publicados                           efectos importantes de siete estudios de educación y traslación de
en inglés entre 1996 y 2013. En general, los participantes fueron                           conocimientos, RR: 1,40 (IC del 95%: 1,20–1,63) y de cuatro estudios
padres de niños pequeños expuestos a una intervención elegible.                             que utilizaron incentivos, RR: 1,28 (IC del 95%: 1,12–1,45).
Seis estudios demostraron un bajo riesgo de sesgo y cinco estudios                          Conclusión Las intervenciones que afectan a la demanda llevan a
presentaron un riesgo de sesgo entre moderado y elevado. Se realizó                         mejoras significativas en la cobertura de vacunación infantil en países de
un análisis agrupado teniendo en cuenta los 11 estudios, con datos                          ingresos bajos y medios. Los enfoques educativos y el uso de incentivos
de 11,512 participantes. Las intervenciones que afectan a la demanda                        fueron estrategias efectivas.

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       knowledge of vaccines impact infant immunization rates? A community-
       based randomized-controlled trial in Karachi, Pakistan. BMC Public Health.
       2011;11(1):239. doi: http://dx.doi.org/10.1186/1471-2458-11-239 PMID:
       21496343

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Table 1. Studies included in systematic review and meta-analysis of strategies to increase the demand for childhood vaccination in low- and middle-income countries

                                                                                         Study and year          Site              Study design             Participants                                    Intervention                                   Control                Vaccination Outcomes
                                                                                                                                                                                                                                                                                                               Mira Johri et al.

                                                                                         Robertson et al.,       Zimbabwe, rural   Cluster randomized       30 areas were matched on socioeconomic          Unconditional cash transfer: every household No incentives            Proportion of children
                                                                                         201324                  areas             controlled trial         characteristics and randomized to three         collected US$ 18 plus US$ 4 per child (up to a                        less than 5 years with
                                                                                                                                                            groups (10 UCT: 10 CCT: 10 control).            maximum of three children) from designated                            up-to-date vaccinations
                                                                                                                                                            Households were eligible to participate if      pay points every 2 months.                                            (measles; BCG; polio;
                                                                                                                                                            they lived in a study area and met need-        Conditional cash transfer: households                                 and diphtheria–
                                                                                                                                                            based criteria. Vaccination outcomes consider   received the same amount, but were                                    tetanus–pertussis)
                                                                                                                                                            children aged 0–4 years in participating        monitored for compliance with several
                                                                                                                                                            households (934 in the intervention arms        conditions. Among others, children less than
                                                                                                                                                            (517 UCT; 417 CCT) and 360 controls).           5 years had to be vaccinated on time.
                                                                                         Briere et al., 201225   Kenya, largely    Controlled before-and-   Comparison between two adjacent districts.      During routine immunization visits, caregivers Routine                Children 2–13 months
                                                                                                                 rural             after study              Children aged 2–13 months were eligible;        with a child aged < 12 months were offered     immunization only      with up-to-date
                                                                                                                                                            1607 children in the intervention arm and       free hygiene kits (sodium hypochlorite                                immunization coverage
                                                                                                                                                            723 children in the control arm.                solution for household water treatment,                               (3 doses of pentavalent
                                                                                                                                                                                                            soap, pictorial educational materials) and                            vaccine at 6, 10 and
                                                                                                                                                                                                            education about water treatment and hand                              14 weeks and 1 dose
                                                                                                                                                                                                            hygiene.                                                              of measles vaccine at
                                                                                                                                                                                                                                                                                  9 months)
                                                                                         Owais et al., 201115    Pakistan, urban   Randomized controlled All mothers in five selected communities           Short, home-based information sessions         General health         At four months after
                                                                                                                 and peri-urban    trial                 with a child ≤ 6 weeks old were eligible to        on importance of vaccines for low-             promotion              enrolment, children
                                                                                                                 communities                             participate; 179 children in the intervention      literacy communities delivered by CHWs         messages (including    were defined as fully
                                                                                                                 near Karachi                            arm and 178 in the control arm.                    in 5 minutes. Pictorial cards conveyed         information on         immunized if they

Bull World Health Organ 2015;93:339–346C| doi: http://dx.doi.org/10.2471/BLT.14.146951
                                                                                                                                                                                                            three messages: vaccines save children’s       vaccines) delivered    completed all three
                                                                                                                                                                                                            lives; location of vaccination centres; and    by CHWs in 10–15       doses of DTP3/Hepatitis
                                                                                                                                                                                                            importance of retaining cards.                 minutes                B; otherwise non-
                                                                                                                                                                                                                                                                                  immunized
                                                                                         Usman et al., 201117    Pakistan, rural   Randomized controlled All children visiting six selected EPI centres    Group 1: A redesigned immunization card in      Mothers underwent      DTP3 completed
                                                                                                                 area near         trial                 for DTP1 were eligible, if mothers had lived in   a plastic jacket, with a hanging string.        routine EPI centre     (received both DTP2 and
                                                                                                                 Karachi                                 the area for at least 6 months. Mother–child      Group 2: 2–3 minutes conversation with          visits and received    DTP3) versus DTP3 not
                                                                                                                                                         pairs were randomly allocated to 1 of 4 study     mother during DPT1 visit to motivate and        neither intervention   completed
                                                                                                                                                         groups; 1 128 participants in the intervention    convey the potential adverse impact of
                                                                                                                                                         arms (Group 1: 378; 2: 376; 3: 374) and 378 in    incomplete immunization on the child’s
                                                                                                                                                         the control arm.                                  health.
                                                                                                                                                                                                           Group 3: Received both interventions.
                                                                                         Banerjee et al.,        India             Cluster randomized       Within each of 134 randomly selected           Intervention A: A mobile team conducted         No intervention; had   Children under
                                                                                         201018                                    controlled trial         villages, 30 households with a child 0–5 years monthly immunization camps in villages at       access to standard     3 years who
                                                                                                                                                            of age were randomly selected. Children        fixed dates and times to improve services.      services               received ≥ 1 vaccine
                                                                                                                                                            were included if they belonged to a selected In each village, a social worker performed                               dose or were fully
                                                                                                                                                            household and would be aged 1–3 years at       outreach, linkage and educated mothers                                 immunized;presence
                                                                                                                                                            the end of study (main sample) or were aged about immunization.                                                       of BCG scar, number of
                                                                                                                                                            0–6 months at baseline (baseline cohort).      Intervention B: Intervention A plus 1 kg of                            immunizations, costs
                                                                                                                                                            761 children received interventions (A: 379;   raw lentils per immunization and a set of                              and cost-effectiveness
                                                                                                                                                            B: 382); 860 children served as controls.      metal plates for a child’s full immunization.
                                                                                                                                                                                                                                                                                                                Childhood vaccination in low- and middle-income countries
                                                                                                                                                                                                                                                                                                                                                                            Systematic reviews

       346A
                                                                                                                                                                                                                                                                                            (continues. . .)
(. . .continued)

       346B
                                                                                         Study and year          Site              Study design             Participants                                    Intervention                                     Control                Vaccination Outcomes
                                                                                         Andersson et al.,       Pakistan, Lasbela Cluster randomized       32 EAs were randomly selected.18 EAs            The intervention involved three structured       Access to standard     Proportions of children
                                                                                         200919                  district          controlled trial         (3166 children < 5 years) in intervention       discussions separately with male and female      immunization           12–23 months receiving
                                                                                                                                                            group. 14 EAs (2475 children < 5 years) in      groups in each village. Discussions shared       services; both         DTP3 and measles
                                                                                                                                                            control group. Vaccination outcomes reflect     findings about local vaccine uptake; focused     groups received        vaccine;
                                                                                                                                                                                                                                                                                                                                                                             Systematic reviews

                                                                                                                                                            a random sample of children aged 12–23          on the costs and benefits of childhood           a district-wide        knowledge, attitudes
                                                                                                                                                            months in each cluster (intervention: 535       vaccination; and focused on local action         health promotion       and norms about
                                                                                                                                                            children; control: 422 children).               plans. Participants spread the dialogue in       programme on           vaccination; costs and
                                                                                                                                                                                                            their communities.                               household hygiene      cost-effectiveness
                                                                                         Usman et al., 200916    Pakistan, urban   Randomized controlled All children visiting five selected EPI centres    Group 1: A redesigned immunization card in       Mothers underwent      DTP3 completed
                                                                                                                 area in Karachi   trial                 for DTP1 were eligible to participate, if          a plastic jacket, with a hanging string. Group   routine EPI centre     (received both DTP2 and
                                                                                                                                                         mothers had lived in the area for at least         2: 2–3 minutes conversation with mother          visits and received    DTP3) versus DTP3 not
                                                                                                                                                         6 months. Mother–child pairs were randomly         during DPT1 visit to motivate and convey         neither intervention   completed
                                                                                                                                                         allocated to 1 of 4 study groups; 1125             the potential adverse impact of incomplete
                                                                                                                                                         participants in the intervention arms (Group       immunization on the child’s health.
                                                                                                                                                         1: 375; 2: 375; 3: 375) and 375 in the control     Group 3: Received both interventions.
                                                                                                                                                         arm.
                                                                                                                                                                                                                                                                                                                 Childhood vaccination in low- and middle-income countries

                                                                                         Roy et al., 200823      Bangladesh,       Randomized controlled 1275 poor women in 17 districts eligible           The standard programme provided income           Comparison group       Percentages of children
                                                                                                                 rural             trial                 for the rural maintenance programme                support, employment and skill training. The      received only          0–60 months receiving
                                                                                                                                                         were divided into three groups. Vaccination        intervention group received basic nutrition      standard programme;    (by dose) DTP, measles,
                                                                                                                                                         outcomes concerned 340 children 0–60               and health education (including child            control group          BCG, OPV that were
                                                                                                                                                         months (intervention: 126, control: 104,           immunization).                                   received neither       partially vaccinated or
                                                                                                                                                         comparison group 110).                                                                              programme nor          fully vaccinated
                                                                                                                                                                                                                                                             education
                                                                                         Pandey et al., 200720   India, Uttar      Cluster randomized       From 21 districts, 105 villages were randomly   Campaigns to inform poor rural populations       Access to standard     Children less than 1 year
                                                                                                                 Pradesh           controlled trial         selected. 10 households per village (5 low      about entitled health and education services     services               old receiving ≥ 1 vaccine
                                                                                                                                                            caste, 5 middle-to-high caste) with at least    were conducted in two rounds in each                                    dose
                                                                                                                                                            one child going to public primary school        village. Each round comprised two to three
                                                                                                                                                            were invited to join the baseline survey.       1 hour meetings consisting of an audiotaped
                                                                                                                                                            Vaccine outcomes relate to 337 households       presentation, question period and leaflet
                                                                                                                                                            (intervention 149; control 79) with a child     distribution. Participants were re-interviewed
                                                                                                                                                            less than 1 year                                after 12 months.
                                                                                         Morris et al., 200421   Honduras          Cluster randomized       70 municipalities with the highest rates of     Group 1 received vouchers worth £2.53 per        Access to standard     Proportion of children
                                                                                                                                   controlled trial         malnutrition were selected and randomly         month for each pregnant woman or child           services               93 days to 3 years
                                                                                                                                                            assigned to one of four study groups in         younger than 3 years, up to a maximum of                                who received DTP1;
                                                                                                                                                            the ratio 2:1:2:2. Approximately 470 000        two. Payments required compliance with                                  proportion of children
                                                                                                                                                            people received one or both interventions.      child preventive health care.                                           1 year old who received
                                                                                                                                                            Vaccination analyses for DTP1 compared 810      Group 2 improved health services via better                             measles vaccine
                                                                                                                                                            children in Group 1 to 878 controls.            planning, training and small repairs and
                                                                                                                                                                                                            purchases.
                                                                                                                                                                                                            Group 3 received both packages.
                                                                                                                                                                                                                                                                                              (continues. . .)

Bull World Health Organ 2015;93:339–346C| doi: http://dx.doi.org/10.2471/BLT.14.146951
                                                                                                                                                                                                                                                                                                                  Mira Johri et al.
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