Supplementary polio immunization activities and prior use of routine immunization services in non-polio-endemic sub-Saharan Africa
Stephane Helleringer a, Jemima A Frimpong a, Jalaa Abdelwahab b, Patrick Asuming c, Hamadassalia Touré b, John Koku Awoonor-Williams d, Thomas Abachie d & Flavia Guidetti b
a. Heilbrunn Department of Population and Family Health, Columbia University, 60 Haven Avenue B-2, New York, NY 10032, United States of America (USA).
b. United Nations Children’s Fund, New York, USA.
c. Department of Economics, Columbia University, New York, USA.
d. Ghana Health Service, Accra, Ghana.
Correspondence to Stephane Helleringer (e-mail: email@example.com).
(Submitted: 22 June 2011 – Revised version received: 23 January 2012 – Accepted: 23 January 2012 – Published online: 11 April 2012.)
Bulletin of the World Health Organization 2012;90:495-503. doi: 10.2471/BLT.11.092494
Since the late 1980s, use of supplementary immunization activities (SIAs) has been a key strategy of the Global Polio Eradication Initiative (GPEI). SIAs are mass vaccination campaigns that aim to administer additional doses of oral poliovirus vaccine (OPV) to each child aged < 5 years, regardless of their vaccination history. In doing so, SIAs attempt to remedy the limited ability of routine immunization services to reach at-risk children with the number of OPV doses required to generate immunity.1,2 In many countries, SIAs have largely contributed to the 99% global reduction in the incidence of paralytic poliomyelitis observed since the 1988 launch of the GPEI.2–4
Despite the central role of SIAs in eradication efforts, setbacks in the GPEI have been attributed to low-quality SIAs.5 Target dates for eradication have repeatedly been pushed back and, at present, transmission of wild poliovirus remains endemic in Afghanistan, Nigeria and Pakistan. Four countries where circulation of wild poliovirus had stopped (Angola, Chad, Democratic Republic of the Congo and South Sudan) have been labelled as having “re-established polio transmission” and several other countries previously considered to be “polio free” have reported cases of acute flaccid paralysis due to wild poliovirus strains originating from northern Nigeria.6,7 A wild poliovirus “importation belt” thus stretches from Senegal to the Horn of Africa. To achieve eradication, the 2010–2012 GPEI strategic plan sets strict targets of > 90% coverage for each SIA conducted in the importation belt. Even in such highly immunized populations, however, outbreaks may still occur if much lower coverage is achieved for particular subpopulations.8 In particular, the influence of SIAs on population-level immunity against polio may be lowered if children who do not access routine immunization services (and are thus less likely to be immune to polio and other vaccine-preventable diseases) also participate less frequently in SIAs.
Very limited data on patterns of SIA participation are available that consider past use of routine immunization services. In a study of the 1997 Madagascar SIA, Andrianarivelo and colleagues9 reported significantly increased SIA-associated immunity among children who had not used routine immunization services or had missed routine OPV doses. Currently collected data on SIA coverage do not include an assessment of the immunization history of children who were not vaccinated during SIAs. The effectiveness of polio SIAs at supplementing routine immunization services in non-polio-endemic sub-Saharan African countries is thus not known. In this article, we test the hypothesis that children who did not use routine immunization services before an SIA were less likely to participate in that SIA, compared with children who were users of routine services. We also measured SIA participation among users of routine immunization services who were compliant with the routine OPV immunization schedule, compared with users who were non-compliant.
Data collection and study groups
We used three data sources: Demographic and Health Surveys (DHSs), Multiple Indicator Cluster Surveys (MICSs) and the 2010 Mobile Technology for Community Health (MoTeCH) survey (Appendix A, available at: http://www.columbia.edu/~sh2813/appendix-02292012sh.pdf). The first two sources are nationally representative household-based surveys conducted, on average, every 3–6 years in several sub-Saharan countries. The MoTeCH survey is a household-based survey conducted among women residing in the Kassena-Nankana East and West districts in Ghana’s Upper East Region. In all surveys, data on participation in SIAs and use of routine immunization services were collected in a similar manner. Mothers were asked to provide vaccination information for their surviving children < 5 years old.10–12 They were first asked whether their child had ever had a health card. Health cards are small booklets, usually given to mothers or guardians at the time of delivery or during the first vaccination visit, in which health workers record receipt of various antigens recommended through the World Health Organization’s (WHO’s) Expanded Programme on Immunization. For children whose health card was available at the time of the survey, interviewers transcribed the date of each vaccination recorded in the card. Interviewers then asked mothers to specify types of undocumented vaccination, if any, these children received. For children whose health card was not available at the time of the survey or who had never had a health card, interviewers asked mothers to specify every vaccination these children received but vaccination dates were not requested.
Because vaccinations received during polio SIAs are not recorded in children’s health cards by health workers and volunteers, OPV doses documented in health cards represent doses obtained through routine immunization services. We thus used health-card data to measure children’s prior use of routine immunization services in two ways. First, we used ownership of a health card to distinguish children who had ever used routine immunization services (hereafter, “users”) from children who had never used routine immunization services (hereafter “non-users”). Second, among users, we distinguished children who were compliant with routine OPV immunization from children who were not compliant by examining the age at which each OPV dose was received. Most countries in sub-Saharan Africa use a standard schedule for OPV: the first OPV dose is administered at 6 weeks of age; the second, at 10 weeks; and the third, at 14 weeks. Thus, we classified children as compliant if, at the time of the SIA, their health card reflected receipt of each required OPV dose. For example, a child who was 20 weeks old at the time of an SIA and had the third OPV dose documented in their health card would be classified as compliant, whereas a child who was 11 weeks old at the time of an SIA and had only the first OPV dose documented in their health card would be classified as non-compliant.
In many of the MICSs and DHSs and in the MoTeCH survey, mothers are asked about their children’s participation in recent polio SIAs. In some surveys, mothers are asked only whether their children participated in any SIA in recent years. In other surveys, mothers are asked whether their children participated in a specific SIA. Surveys were included in this study only if they included assessment of participation in a specific SIA for which the date of implementation was available. We obtained dates of SIAs directly from the survey questionnaire or indirectly from the WHO calendar of SIAs (available at: http://apps.who.int/immunization_monitoring/en/globalsummary/siacalendar/padvancedsia.cfm) To limit recall bias, we further excluded SIA data if collection of survey data began > 12 months after an SIA. We also excluded subnational SIAs because it was impossible to determine which of the children included in survey data sets were targeted.
All analyses excluded children whose day of birth was unavailable or who were born after the SIA of interest was held. Analyses of SIA participation among compliant and non-compliant users excluded children whose health card was not reviewed by the interviewer, was incomplete or had an invalid sequence of receipt dates for routine OPV doses (e.g. the date of the second dose was more recent than the date of the third dose).
Primary analyses used logistic regression models to measure the associations between SIA participation and prior routine immunization use and between SIA participation and routine immunization compliance. Such models included SIA participation as the (dichotomous) dependent variable and controlled for child age and sex, mother age and education level and household characteristics (i.e. religion and ethnicity of the household head, wealth quintile and urban/rural residence). We also included a set of regional fixed effects. Standard errors were adjusted for the clustering of observations within enumeration areas and households. We report adjusted frequencies of SIA participation derived from the logistic regression models, by routine immunization service use and routine OPV immunization compliance. These frequencies were computed using the margin command in Stata, version 12 (StataCorp, College Station, United States of America), after setting other covariates at their mean value.
We conducted two robustness tests of the logistic regression models used in our primary analyses. The first test re-estimated the models after inclusion of all children for whom the month but not day of birth was available. In this test, only children who were aged > 4 months at the time of the SIA and, thus, were supposed to have completed the routine OPV schedule were included. The second test re-estimated the models after reclassification of children who first used routine immunization services after the SIA of interest as non-users.
In a secondary investigation, we compared the organizational attributes, human resources and budgetary allocations for three SIAs conducted in Benin, to explore why some SIAs are more successful than others at reaching undervaccinated children. Benin was selected for this investigation because (i) it is the only country for which we had survey data on participation in 3 SIAs, (ii) SIA implementation records were available to the study team and (iii) SIA participation among non-users of routine services during SIAs in 2005 and 2006 was significantly less than that during an SIA in 2000 (61–64% in 2005–2006 versus 91% in 2000, see below).
Characteristics of SIAs and children
We reviewed data from 119 surveys conducted between 1988 and 2010. Data from 21 SIAs (Fig. 1) met inclusion criteria. These primarily included SIAs conducted in the wild poliovirus importation belt, as well as one in Lesotho and two in Namibia. One SIA was conducted in 1999, three in 2000, four in 2004, nine in 2005, three in 2006 and one in 2010.
Fig. 1. Flowchart of data set selection for evaluation of polio supplementary immunization activities (SIAs) participation in non-polio-endemic sub-Saharan African countries
DHS, Demographic and Health Survey; MICS, Multiple Indicator Cluster Survey; OPV, oral poliovirus vaccine.
a 1995 and 2002 Eritrea DHS, 1992 Guinea DHS, 2000–2001 Mauritania DHS and 2003 South Africa DHS.
b All surveys from the DHS-II and DHS-III rounds (i.e. DHS surveys conducted between 1988 and 1997), as well as 2004 Cameroon DHS, 2005 Cape Verde DHS, 2000 Comoros MICS, 2005 Congo (Brazzaville) DHS, 2005 Ethiopia DHS, 2000 Gabon DHS, 2000 Guinea-Bissau MICS, 2008 Kenya DHS, 2009 Lesotho DHS, 2009 Liberia DHS, 2008 Madagascar DHS, 2004 and 2010 Malawi DHSs, 2007 Mauritania MICS, 2003 Mozambique DHS, 2005 Rwanda DHS, 2007 Rwanda interim DHS, 2000 Senegal MICS, 2006 Somalia MICS, 1998 South Africa DHS, 2006 Uganda DHS, 2005 and 2010 United Republic of Tanzania DHSs, 2007 Zambia DHS and 2005–2006 Zimbabwe DHS.
c 2003 Burkina-Faso DHS, 2003–2004 Madagascar DHS, 2006 Mali DHS, 2000 Rwanda DHS and 2000 Zambia MICS.
d 2008 Sierra Leone DHS and 2006–2007 Swaziland DHS.
e 2005 Burundi MICS, 2000 and 2006 Cameroon MICSs, 2000 and 2006 Central African Republic MICSs, 2000 Côte d’Ivoire MICS, 2000 Equatorial Guinea MICS, 2000 Ethiopia DHS, 2000 and 2006 Gambia MICSs, 2000 Kenya MICS, 2000 Lesotho MICS, 2000 Madagascar MICS, 2000 Malawi DHS, 2000 Niger MICS, 2000 Rwanda DHS, 2006 Sao Tome and Principe MICS, 2000 Sierra Leone MICS, 2000 Swaziland MICS, 2000 Togo MICS and 2001–2002 Zambia DHS.
f 2000–2001 Uganda DHS and 1999 United Republic of Tanzania DHS.
g 1999, 2000 and 2003 Lesotho measles SIAs; 2002–2003 Guinea measles SIA; 2003 Guinea yellow fever SIA; 2004 and 2005 Niger measles SIAs; 2005 Benin measles SIA; 2005 Côte d’Ivoire measles SIA; 2000 Gambia measles SIA; 2001 Gambia meningitis SIA; 2005 Guinea-Bissau vitamin A supplementation activity; and 2005 Togo vitamin A supplementation activity.
h 1999 Benin polio SIA; May 2005 Burkina Faso polio SIA; 1998 and 1999 Burundi polio SIAs; Feb–May 2005 Côte d’Ivoire polio SIA; 2001 Ghana polio SIA; 2002 Guinea polio SIA; 2001 Kenya polio SIA; 1997, 1998 and 1999 Mali polio SIAs; 1999, 2004 and 2005 Namibia polio SIAs; 2004 Niger polio SIA; 2002 Senegal polio SIA; and Feb–Mar 2005 Togo polio SIA.
i 2002 Ghana subnational polio SIA and 2002 Kenya subnational polio SIA.
The proportion of children with a known date of birth varied greatly across countries (Table 1). Among children with a known birthday, between 74.5% (during the 2000 Benin SIA) and 93.6% (during the 2004 Lesotho SIA) were alive at the time of the SIA. Between 94.3% and 99.8% of respondents answered the specific SIA questions. Prior use of routine immunization services varied significantly across countries: during the 2004 Lesotho SIA, only 1.3% of sampled children were non-users of routine immunization services, whereas during the 2000 Mali SIA, non-users comprised 29.2% of children.
Table 1. Data on surveys and surveyed children aged < 5 years used to evaluate participation in polio supplementary immunization activities (SIAs) in 15 non-polio-endemic sub-Saharan African countries
Full results of logistic regression analyses of the probability of SIA participation are reported in Appendix B (available at: http://www.columbia.edu/~sh2813/appendix-02292012sh.pdf). SIA participation ranged from 70.2% (during the 2004 Lesotho SIA) to 96.1% (during the 1999 Burundi SIA). In most SIAs, participation was lower among infants than among children 1–4 years old. SIA participation increased with age and educational level of the mother or guardian. In 8 of 17 SIAs for which data on household wealth were available, SIA participation was highest among wealthier households. In 7 SIAs, participation was associated with residential location: 2 SIAs (the 1999 Burundi SIA and the 2005 Sierra Leone SIA) had greater participation in rural areas and 5 SIAs (the 2000 Mali SIA, the 2000 Benin SIA, the 2005 Burkina-Faso SIA, the 2005 Gambia SIA and the 2006 Namibia SIA) had greater participation in urban areas. There were regional differences in participation in all SIAs but differences associated with ethnicity were less common. Religious differences in SIA participation were observed in 6 SIAs, during which participation was lower among people with traditionalist beliefs than among Christians and Muslims.
Prior use of routine services
In adjusted logistic regression analyses (Fig. 2), user participation was > 85% for 12 SIAs but non-user participation was > 85% in only 5 SIAs. In 18 of 21 SIAs, participation was significantly higher (P < 0.01 in 16 SIAs, P < 0.05 in 2 SIAs and P < 0.1 in 1 SIA), among routine immunization service users (Fig. 2). In robustness analyses, however (Appendix C and Appendix D, both available at: http://www.columbia.edu/~sh2813/appendix-02292012sh.pdf), participation was higher among routine immunization service users than among non-users in all but 1 SIA, which occurred during 2000 in Benin, discussed below. These differences in SIA participation by prior use of routine immunization services were sometimes very large. For example, during the 2010 Ghana SIA in the Kassena-Nankana districts, adjusted SIA participation was 91.5% among routine immunization service users but only 32.7% among non-users (P < 0.01).
Fig. 2. Participation in polio supplementary immunization activities (SIAs) in non-polio-endemic sub-Saharan African countries, by use or non-use of routine immunization (RI) servicesa
OPV compliance among users
Among routine immunization service users, the proportion of compliant children varied significantly across countries (Appendix E, available at: http://www.columbia.edu/~sh2813/appendix-02292012sh.pdf). Fewer than 60% of users had received all required routine OPV doses for their age before the 1999 Burundi SIA, the 2000 Mali SIA, the 2004 and 2005 Sierra Leone SIAs and both 2005 Niger SIAs. On the other hand, > 80% of users were compliant with the routine vaccination schedule before the 2004 Lesotho SIA and the 2006 Namibia SIA (Appendix E). SIA participation among compliant users was significantly higher than that among non-compliant ones in 14 of 21 SIAs analysed (Fig. 3). The largest difference was observed during the 2004 Guinea SIA, in which 68.8% of non-compliant routine immunization users participated, compared with 85.4% of compliant users (P < 0.01).
Fig. 3. Participation in polio supplementary immunization activities (SIAs) in non-polio-endemic sub-Saharan African countries among users of routine immunization (RI) services, by compliance with the routine oral poliovirus vaccine (OPV) schedulea
The Benin case study
Although participation in the 2000 Benin SIA was high (> 90%) among both routine immunization service users and non-users, SIAs conducted in 2005 and 2006 had high participation among users but much lower participation among non-users (approximately 60%; Fig. 2). Investigation of the SIAs’ budgetary allocations revealed that the percentage of the budget allocated to community mobilization declined sharply, from 19.8% in 2000 to 10.1% in 2005 and 11.1% in 2006 (Table 2).
Table 2. Characteristics of polio supplementary immunization activities (SIAs) conducted in Benin between 2000 and 2006
In this study, we used data from the MICS, the DHS and a recent survey we conducted in two districts of Ghana’s Upper East Region to document patterns of participation in polio SIAs in sub-Saharan African countries where polio is not endemic. We found that a large percentage of undervaccinated children benefit from vaccination opportunities offered during SIAs every year but that SIAs only imperfectly remedy the limited reach of routine immunization services. In the 21 SIAs we analysed, reported SIA participation among routine immunization users was often significantly higher than that among non-users. Compliant users were also often more likely than non-compliant users to participate in SIAs, but these differences were of much smaller magnitude than those between users and non-users. Of 3 SIAs in Benin, the one with the highest participation among non-users had the greatest percentage of the total SIA budget invested in community mobilization.14 During the 2010 Ghana SIA, some of the possible reasons for low SIA participation among non-users of routine immunization services included inappropriate marking of houses in the targeted areas, incomplete training of volunteers, lack of local maps of the targeted areas among teams and suboptimal supervision.15
Our study has several potential limitations. First, analyses were limited to 21 of thousands of SIAs conducted since the launch of the GPEI and excluded SIAs conducted in countries where polio transmission is endemic or considered to be re-established. Also, most data were for SIAs conducted before 2006. Although analyses of the 2010 Ghana SIA suggest that large differences in SIA participation between routine immunization service users and non-users may have persisted in recent years, data from the MoTeCH survey are not nationally representative and are derived from a limited sample size. Second, data were limited to children for whom a valid birth date was reported and were thus possibly affected by sample selection bias. However, robustness analyses involving children for whom the month but not day of birth was known (Appendix C) yielded results very similar to those for children whose birth date was known (Fig. 1 and Fig. 2). Third, SIA participation was determined on the basis of maternal recall and self-report rather than on the basis of more objective methods (e.g. finger marking5). Although we attempted to minimize recall bias by excluding SIA data if the associated survey was conducted > 12 months after the SIA, a desire to state socially acceptable responses to survey questions might have tempted some mothers to exaggerate the extent to which their children participated in SIAs. Fourth, the criterion used to distinguish routine immunization users from non-users is a potential source of information bias. If SIAs stimulate interest in immunization among undervaccinated children, non-users who participate in an SIA might subsequently begin accessing routine immunization services, which could result in their misclassification as routine immunization service users at the time of the SIA. The results in Appendix D, however, indicate that this source of bias is unlikely to have explained the observed patterns. Fifth, our data have limitations common to retrospective studies of vaccination status (e.g. they exclude children who died or moved before the survey).16 Finally, our exploration of the factors that may explain low SIA coverage among non-users of routine immunization services was limited. It was based solely on the comparison of three SIAs conducted in one country (Benin); used only data from SIA budgets and planning documents, rather than data tracking the implementation of SIAs at the local (i.e. district) level17; and did not incorporate elements (e.g. rumours and fatigue) characterizing the demand for SIAs and immunization among local populations.
Our study nonetheless has important implications for polio eradication. First, our findings provide insights into factors explaining the recurrent importation of wild poliovirus in previously polio-free sub-Saharan countries since 2002. Specifically, differences in SIA coverage between routine immunization service users and non-users may have maintained local pockets of susceptibility to polio importation. Second, our analyses suggest that SIA monitoring in the GPEI should include an assessment of the vaccination history of children “missed” by vaccination teams during SIAs. Current monitoring practices do not include such assessment and thus do not permit identification of possible pockets of individuals susceptible to infection. Whereas the 2010 Ghana SIA met the GPEI’s quality criterion of > 90% participation in the two Kassena-Nankana districts, we found very low coverage among non-users of routine immunization services, who are most likely to be undervaccinated. Finally, our analyses have implications for strategies to improve SIA quality in the GPEI. At present, quality assessments are focused on estimating the proportion of children who were not reached during an SIA and on determining why they were not reached (e.g. refusal and conflict-related inaccessibility). Such data are descriptive and do not permit identification of the SIA characteristics (e.g. poor microplanning, lack of supervision and insufficient or ineffective community mobilization) that explain poor SIA coverage among populations at greatest risk of experiencing polio outbreaks.17 To sustain high levels of immunity against polio and achieve eradication, an ambitious agenda of operational research on the characteristics of undervaccinated children (e.g. location and socioeconomic characteristics) and the organizational determinants of SIA participation is thus urgently needed. Findings from this research will help guide SIA quality improvement strategies and help develop new interventions to promote participation in immunization activities among children who are not reached by both routine immunization services and SIAs.
We thank Jacques Hassane, James Phillips, Almamy Malick Kanté and Francis Yeji.
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