Figures
Abstract
Background
Nigeria has a high proportion of the world’s underimmunised children. We estimated the inequities in childhood immunisation coverage associated with socioeconomic, geographic, maternal, child, and healthcare characteristics among children aged 12–23 months in Nigeria using a social determinants of health perspective.
Methods
We conducted a systematic review to identify the social determinants of childhood immunisation associated with inequities in vaccination coverage among low- and middle-income countries. Using the 2018 Nigeria Demographic and Health Survey (DHS), we conducted multiple logistic regression to estimate the association between basic childhood vaccination coverage (1-dose BCG, 3-dose DTP-HepB-Hib (diphtheria, tetanus, pertussis, hepatitis B and Haemophilus influenzae type B), 3-dose polio, and 1-dose measles) and socioeconomic, geographic, maternal, child, and healthcare characteristics in Nigeria.
Results
From the systematic review, we identified the key determinants of immunisation to be household wealth, religion, and ethnicity for socioeconomic characteristics; region and place of residence for geographic characteristics; maternal age at birth, maternal education, and household head status for maternal characteristics; sex of child and birth order for child characteristics; and antenatal care and birth setting for healthcare characteristics. Based of the 2018 Nigeria DHS analysis of 6,059 children aged 12–23 months, we estimated that basic vaccination coverage was 31% (95% CI: 29–33) among children aged 12–23 months, whilst 19% (95% CI:18–21) of them were zero-dose children who had received none of the basic vaccines. After controlling for background characteristics, there was a significant increase in the odds of basic vaccination by household wealth (AOR: 3.21 (2.06, 5.00), p < 0.001) for the wealthiest quintile compared to the poorest quintile, antenatal care of four or more antenatal care visits compared to no antenatal care (AOR: 2.87 (2.21, 3.72), p < 0.001), delivery in a health facility compared to home births (AOR 1.32 (1.08, 1.61), p = 0.006), relatively older maternal age of 35–49 years compared to 15–19 years (AOR: 2.25 (1.46, 3.49), p < 0.001), and maternal education of secondary or higher education compared to no formal education (AOR: 1.79 (1.39, 2.31), p < 0.001). Children of Fulani ethnicity in comparison to children of Igbo ethnicity had lower odds of receiving basic vaccinations (AOR: 0.51 (0.26, 0.97), p = 0.039).
Conclusions
Basic vaccination coverage is below target levels for all groups. Children from the poorest households, of Fulani ethnicity, who were born in home settings, and with young mothers with no formal education nor antenatal care, were associated with lower odds of basic vaccination in Nigeria. We recommend a proportionate universalism approach for addressing the immunisation barriers in the National Programme on Immunization of Nigeria.
Citation: Williams SV, Akande T, Abbas K (2024) Systematic review of social determinants of childhood immunisation in low- and middle-income countries and equity impact analysis of childhood vaccination coverage in Nigeria. PLoS ONE 19(3): e0297326. https://doi.org/10.1371/journal.pone.0297326
Editor: Harapan Harapan, Universitas Syiah Kuala, INDONESIA
Received: January 31, 2023; Accepted: December 22, 2023; Published: March 6, 2024
Copyright: © 2024 Williams et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: The 2018 Nigeria DHS data set is publicly available and accessible upon registration for legitimate research purposes on the DHS website at https://dhsprogram.com/methodology/survey/survey-display-528.cfm. To download DHS datasets, researchers must register as a DHS data user at https://dhsprogram.com/data/new-user-registration.cfm.
Funding: KA is supported by Save the Children, Vaccine Impact Modelling Consortium (INV-034281), and the Japan Agency for Medical Research and Development (JP223fa627004). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Competing interests: The authors have declared that no competing interests exist.
Abbreviations: AOR, Adjusted odds ratio; BCG, Bacille Calmette-Guérin vaccine; DHS, Demographic Health Survey; DTP, Diphtheria, tetanus and pertussis containing vaccine; DTP-HepB-Hib, Diphtheria, tetanus, pertussis, hepatitis B and Haemophilus influenzae type B; ECI, Erreygers concentration indices; EPI, Expanded Programme of Immunization; Gavi, Global Alliance for Vaccines and Immunisations; LGA, Local Government Area; LMIC, Low- and Middle-Income Countries; PRISMA, Preferred Reporting Items for Systematic Reviews and Meta-Analyses; SDG, Sustainable Development Goals; UNICEF, United Nations Children’s Fund; WHO, World Health Organisation; WUENIC, WHO and UNICEF estimates of national immunization coverage
Introduction
Nigeria is the most populous country in Africa with around 202 million people in 2020 and its population is predicted to double by 2050 [1]. It is a multi-ethnic country with 36 autonomous states and the Federal Capital Territory. Around 83 million people (40% of total population) live below the poverty line while an additional 53 million people (25% of total population) are vulnerable to falling below the poverty line [2]. Economic growth has been slow with challenges including ongoing conflict in parts of the country, inconsistent regulatory environment, poor power supply and infrastructure [2].
Vaccination is a highly cost-effective public health intervention and beyond the direct benefits to population health, vaccines provide additional economic and social benefits to individuals and society [3, 4]. Infectious diseases remain a leading cause of death among under-5-year-old children, and an additional 1.5 million deaths could be avoided every year with improvements in global vaccination coverage [5, 6]. Model-based estimates, not including COVID-19, project 51 million deaths to be prevented by vaccination during 2021–2030 [7]. There have been substantial improvements in vaccine introductions and vaccination coverage in low- and middle-income countries since the inception of Gavi, the Vaccine Alliance in 2000 [8]. However, the prevalence of zero-dose children, that is children aged 12–23 months who had not received any of the routine childhood vaccines, was 7.7% in low- and middle-income countries during 2010–2019 [9]. The importance of improving vaccination coverage was recognised in the Sustainable Development Goals (SDGs), with immunisation contributing to 14 of the 17 SDGs and includes reduction on poverty, hunger and improving social equity [10]. Vaccination coverage and equity are a strategic goal of the global Immunisation Agenda 2030, with the aim to reach equitable coverage at national and district levels by addressing immunisation barriers posed by location, age, socioeconomic status, and gender [11].
The Expanded Programme on Immunisation (EPI) was established by the World Health Organization (WHO) in 1974 to improve vaccination services globally [12], and Nigeria began nationwide implementation of EPI in 1979 which was later changed to the National Programme on Immunization [13]. Although the vaccines in the routine immunisation programme (S1 Table) for under 5-year-old children are available with no out-of-pocket charges [14], Nigeria has the most under-immunised children in the world with 4.5 million in 2018 [15]. The immunisation system challenges in Nigeria include weak institutions, service delivery, funding, infrastructure, poor coordination between the National Programme on Immunization and non-governmental organisations delivering vaccination services, and a lack of political commitment in some regions, with further challenges to immunisation services caused by the COVID-19 pandemic [14, 16–18]. There are fewer adequately skilled healthcare personnel in rural areas and northern states, and poor retention and frequent transfers of workers. Security is also an issue, with attacks on healthcare workers in recent years. Attitudes of communities and caregivers are important too, with a lack of knowledge about vaccination and mistrust of services hindering vaccination uptake [16, 19].
In the context of wider immunisation system challenges in Nigeria, we focused on factors associated with inequities in basic vaccination coverage through the social determinants of health model. This model framework has been explicitly linked to health equity by the WHO Commission on Social Determinants of Health [20] and considers the social, cultural, political, economic, commercial and environmental factors that shape the conditions in which people are born, grow, live, work and age, and these factors are determined by wealth, power and resources. In this study, we use the social determinants of health model framework, which encompasses the individual, parental, household, environment, and national policy levels that influence inequities in basic vaccination coverage among children in Nigeria (see Fig 1). We refer to vaccine inequity as unfair and avoidable or remediable differences in health among population groups defined socially, economically, demographically, or geographically [21]. This is related to but distinct from health inequality, which indicates the status of imbalances or differences in health among population groups without any moral judgement on whether the imbalances or differences are fair or not [22, 23].
Social determinants of health model framework encompassing the individual, parental, household, environment, and national policy levels and influencing inequities in basic vaccination coverage among children in Nigeria.
Our aim is to analyse the 2018 Nigeria Demographic and Health Survey (DHS) and estimate the inequities in basic vaccination coverage (1-dose BCG (Bacille Calmette-Guérin), 3-dose DTP-HepB-Hib (diphtheria, tetanus, pertussis (DTP), hepatitis B (HepB) and Haemophilus Influenzae type b (Hib)), 3-dose polio, and 1-dose measles vaccines) associated with socioeconomic, geographic, maternal, child, and healthcare characteristics among children aged 12–23 months in Nigeria. We conducted disaggregated equity impact analysis to reveal the inequities in basic vaccination coverage that are hidden at the aggregated national level, and understand the facilitators and barriers to vaccination through the social determinants of health framework.
Methods
Study design of demographic and health survey
We analysed the 2018 Nigeria DHS which was conducted between August to December 2018 [24]. The DHS are nationally representative household surveys focusing on population, health, and nutrition in LMICs [25]. The DHS sample is a two-stage stratified cluster sample with sampling weights applied to ensure that results are representative. There are four questionnaires: household questionnaire, woman’s questionnaire, man’s questionnaire, and biomarker questionnaire. The country is divided into clusters with 30 households selected from each cluster. The woman’s questionnaire was asked to women aged 15–49 years and provides the data for our study. All women aged 15–49 years in the sampled households were included and the survey was successfully conducted in 1,389 clusters after 11 clusters were dropped following deteriorating security in those areas during data collection. In addition, in the state of Borno, 11 of the 27 Local Government Areas (LGAs) in the state were dropped due to insecurity. Clusters selected from these dropped LGAs were replaced with clusters from the remaining LGAs and so may not be representative of the entire state [24]. The study population for our analysis was women aged 15–49 years with a child aged 12 to 23 months old. Of the 41,821 women interviewed, 33,924 women had a child aged 59 months or younger and immunisation data was collected for 6,059 living children aged between 12–23 months. We applied sampling weights to the survey dataset to adjust for disproportionate sampling and non-response, thereby ensuring that the sample was representative of the population.
Characteristics selection and systematic review
The WHO had analysed inequality in immunisation using the following characteristics determined from a literature review: child (gender, birth order), maternal (age at birth, education, ethnicity or caste), household (sex of household head, household economic status), geographic (rural or urban place of residence, subnational region) [26]. Using the WHO inequality work as a starting point, we conducted a systematic review to select the pertinent DHS variables for our equity analysis. We conducted a systematic review to analyse qualitative and quantitative peer-reviewed literature of studies focused on inequities in childhood immunisation in low- and middle-income countries (LMICs) to identify the social determinants of childhood immunisation. S1 Fig illustrates the process flow diagram of identification, screening, eligibility, and inclusion of articles for the systematic review, using the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) framework (S1 Checklist) [27]. We conducted our search using MEDLINE and additional studies were identified through hand-searches of reference lists for articles written in the English language, published between 01/01/2010 to 04/10/2021, for which the full text was available, and contained the following terms in English or American spellings: (Vaccination coverage or Immunisation coverage) AND (Determinant, characteristic, predictor) AND (Equity, equality, disparity, inequality, inequity). We did not search prior to 2010 as papers and the subsequently identified social determinants may be less relevant to the current context.
Vaccination coverage
In the 2018 Nigeria DHS, the information of whether a child has received a vaccination is gathered from the child’s vaccination card. If that is not available or if a vaccine has not been recorded, then the mother is asked which vaccines have been given to her child [24]. Our primary outcome and dependent variable of interest was basic vaccination coverage, that is the proportion of children receiving 1-dose BCG, 3-dose DTP-HepB-Hib, 3-dose polio, and 1-dose measles vaccines. DHS gives the vaccination status of “received” and “not received” for individual vaccines. Binary variables of “received all three doses” and “not received all three doses” were generated for the three dose vaccines. The basic vaccination variable was generated as a binary variable of “received all basic vaccinations” and “not received all basic vaccinations” by combining the variables for 1-dose BCG, 3-dose DTP-HepB-Hib, 3-dose polio, and 1-dose measles vaccines.
Equity analysis
We conducted simple logistic regression to estimate crude odds ratios and assess basic vaccination coverage disaggregated by socioeconomic, geographic, maternal, child, and healthcare characteristics as measured by the DHS and identified through the systematic review and the WHO inequality report on immunisation [26]. Due to the survey design, a p-value for all categories within a characteristic was determined using the Adjusted Wald’s test through the “test” function in Stata [28]. These p-values were used to assess the association between basic vaccination coverage and the characteristics [29] and if a p-value was <0.05 then the characteristic was included in the model. We checked for collinearity between variables and avoided multicollinearity in the development of a parsimonious model [29] using the “regress” in Stata and calculation of the variance inflation factor. However, no variables required removal from the model.
Interaction was tested using the “contrast” function in Stata. This gives F statistics which are adjusted for the survey design, with the p-value demonstrating the statistical significance of the interaction. As in the WHO report [26, 29], interactions were tested between mother’s education and household wealth, mother’s age and household wealth, mother’s age and education, and place of residence and household wealth. We conducted multivariable logistic regression to estimate adjusted odds ratios (AORs) for socioeconomic, geographic, maternal, child, and healthcare characteristics associated with basic vaccination coverage.
We analysed inequity further by estimating the Erreygers concentration indices for maternal education, antenatal care, and household wealth to assess if basic vaccination coverage and vaccination card usage had progressive, regressive, or equal distribution based on each of these characteristics. The concentration index value shows how much of a health measure is concentrated in an advantaged or disadvantaged group. Values range from +1 to -1, with a value of zero meaning there is no inequity and positive values indicating that a health measure is concentrated in the more advantaged groups [30].
Results
In the systematic review, we identified 160 publications, screened the title and abstract, assessed full articles for eligibility, and included 49 publications in our systematic review (see Table 1). In addition to the characteristics analysed by the WHO inequality report on immunisation [26], we identified that antenatal care and birth setting had evidence of association with vaccination coverage. We streamlined the social determinants of childhood immunisation to: household wealth, religion, and ethnicity for socioeconomic characteristics; region and place of residence for geographic characteristics; maternal age at birth, maternal education, and maternal household head status for maternal characteristics; sex of child and birth order for child characteristics; and antenatal care and birth setting for healthcare characteristics.
Vaccination coverage
Among the 6,059 children aged 12–23 months in the 2018 Nigeria DHS following the application of sample weights, 2,100 (35%) of them lived in urban areas. The coverage for the individual vaccines of BCG, DTP-HepB-Hib, polio, and measles was higher in urban areas compared to rural areas (Fig 2 and S2 Table). At the national level, the mean basic vaccination coverage was 31% (95% CI: 29–33) with coverage of single vaccinations ranging from 48% (46–50%) for the third dose of the polio vaccine to 73% (71–75%) for the first dose of the polio vaccine.
Vaccination coverage among children aged 12–23 months in Nigeria and disaggregated by urban and rural areas of residence. Vaccination card coverage is relatively higher in urban areas in comparison to rural areas, and is associated with higher vaccination coverage. Basic vaccination includes 1-dose BCG (Bacille Calmette-Guérin), 3-dose DTP-HepB-Hib (diphtheria, tetanus, pertussis, hepatitis B and Haemophilus influenzae type B), 3-dose polio, and 1-dose measles vaccines.
Vaccination cards were available for 49% (46–51%) of children, among which 57% (55–60%) had received all basic vaccinations. Among the 51% (49–54%) of children without vaccination cards, only 6.4% (5.3–7.7%) of them had received all basic vaccinations. Almost one fifth of children (19% (18–21%)) had not received any of the basic vaccinations and in rural areas almost a quarter had received none. For polio vaccinations, 26% (24–28%) of children had received none of the three doses and for DTP vaccinations, 35% (33–37%) of children had received none. There was a higher proportion of zero-dose children in rural areas compared to urban areas.
Equity analysis
Fig 3 shows the basic vaccination coverage among children aged 12–23 months in Nigeria disaggregated by socioeconomic (household wealth, religion, ethnicity), geographic (region, place of residence), maternal (maternal age at birth, maternal education, maternal household head status), child (sex of child, birth order), and healthcare (antenatal care, birth setting) characteristics. For socioeconomic characteristics, children living in wealthier households had higher basic vaccination coverage ranging from 17% (15–20%) to 49% (45–53%) from the poorest to the richest wealth quintiles. For religion, basic vaccination coverage was higher among children of the Catholic faith at 49% (43–54%) while most children (58%) were of Islamic faith with relatively lower coverage of 23% (21–25%). Regarding ethnicity, basic vaccination coverage ranged from 12% (9–16%) to 56% (51–61%) among children of Fulani and Igbo ethnicities respectively. For geographic characteristics, 65% of children lived in rural areas but basic vaccination coverage was higher for children in urban areas at 44% (41–47%) in comparison to 23% (21–25%) in rural areas. At the regional level, basic vaccination coverage among children ranged from 20% (17–23%) in the North West region to 57% (51–62%) in the South East region (Fig 4). For maternal characteristics, children of mothers aged 35–49 years had higher basic vaccination coverage at 34% (31–39%) in comparison to 16% (12–21%) for children of younger mothers aged 15–19 years. Basic vaccination coverage increased with higher levels of maternal education, with basic vaccination coverage among children of mothers with no education, primary education, and secondary education or higher at 15% (13–17%), 33% (28–38%), and 47% (45–50%) respectively. Children living in female-headed households had relatively higher basic vaccination coverage of 39% (35–44%) in comparison to 30% (28–32%) in male-headed households. For child characteristics, basic vaccination coverage was similar among female and male children at 31% (29–33%) and 31% (29–34%) respectively, while coverage decreased by birth order with 36% (32–40%) and 23% (20–26%) among first-born and sixth-born respectively. For healthcare characteristics, children of women who had a higher number of antenatal care visits during their pregnancy had higher basic vaccination coverage at 41% (39–44%) for four or more visits and 11% (8.7–13%) for no or unknown number of visits. More than half of all women gave birth at home, and basic vaccination coverage among these children was relatively lower at 20% (18–22%) in comparison to 47% (44–49%) among children born in a public or private clinical facility.
Basic vaccination coverage among children aged 12–23 months in Nigeria by socioeconomic (household wealth, religion, ethnicity), geographic (region, place of residence), maternal (maternal age at birth, maternal education, maternal household head status), child (sex of child, birth order), and healthcare (birth setting, antenatal care) characteristics.
Basic vaccination coverage among children aged 12–23 months in Nigeria at the regional level. (The figure is created by the authors using RStudio and naijR package using data from CIA World Factbook. The figure can be reproduced under CC BY 4.0 license).
Fig 5 shows the concentration curve for household wealth-related inequity in basic vaccination coverage, while Table 2 presents the inequities in vaccination card usage rates and vaccination coverage among children aged 12–23 months disaggregated by maternal education, antenatal care, and household wealth in Nigeria, based on Erreygers concentration indices. With respect to maternal education, antenatal care, and household wealth, each of these characteristics had a regressive pro-advantage distribution, with higher vaccination card usage rates and coverage among children from wealthier households, higher maternal education and more antenatal care.
Concentration curve for household wealth-related inequity in basic vaccination coverage among children aged 12–23 months in Nigeria.
Table 3 and Fig 6 presents the inequities in basic vaccination coverage in Nigeria among children aged 12–23 months associated with socioeconomic (household wealth, religion, ethnicity), geographic (region, place of residence), maternal (maternal age at birth, maternal education, maternal household head status), child (sex of child, birth order), and healthcare (antenatal care, birth setting) characteristics. After controlling for other background characteristics through multiple logistic regression, the adjusted odds ratios (AORs) were significant for the associations between basic vaccination coverage and household wealth, religion, ethnicity, maternal age at birth, maternal education, antenatal care, and birth setting. This model and the AORs include the interaction between household wealth and place of residence (see S3 Table for the strata specific AORs between place of residence and household wealth).
Inequities in basic vaccination coverage among children aged 12–23 months in Nigeria associated with socioeconomic (household wealth, religion, ethnicity), geographic (region, place of residence), maternal (maternal age at birth, maternal education, maternal household head status), child (sex of child, birth order), and healthcare (birth setting, antenatal care) characteristics.
Inequities in basic vaccination coverage (1-dose BCG, 3-dose DTP-HepB-Hib, 3-dose polio, and 1-dose measles) in Nigeria among children aged 12–23 months associated with socioeconomic (household wealth, religion, ethnicity), geographic (region, place of residence), maternal (maternal age at birth, maternal education, maternal household head status), child (sex of child, birth order), and healthcare (antenatal care, birth setting) characteristics. Crude and adjusted odds ratios were estimated using simple and multiple logistic regression respectively.
Children living in households of richest wealth quintiles had 221% higher odds (AOR: 3.21 (2.06, 5.00), p < 0.001) of receiving basic vaccinations in comparison to children of the poorest wealth quintiles. However, children living in rural areas in the richer quintile had 64% lower odds (AOR: 0.36 (0.24, 0.53), p < 0.001) and children in rural areas in the richest quintile 50% lower odds (AOR: 0.50 (0.35, 0.72), p <0.001) than children in urban areas. Children whose religion was classified as ‘other’ had 75% lower odds (AOR: 0.25 (0.10, 0.60), p < 0.002) of receiving basic vaccinations than children of Catholic faith. In comparison to children of Igbo ethnicity, children of Fulani ethnicity had 49% lower odds of receiving basic vaccinations (AOR: 0.51 (0.26, 0.97), p = 0.039). Children of mothers aged 35–49 years had 125% higher odds (AOR: 2.25 (1.46, 3.49), p < 0.001) of receiving basic vaccination than children of mothers aged 15–19 years. Children of mothers with secondary or higher education had 79% higher odds (AOR: 1.79 (1.39, 2.31), p < 0.001) of receiving basic vaccination in comparison to children of mothers with no formal education. Children of mothers who had four or more antenatal care visits had 187% higher odds (AOR: 2.87 (2.21, 3.72), p < 0.001) of receiving basic vaccinations than children of mothers who had no antenatal care. Children born in clinical facilities had 32% higher odds (AOR 1.32 (1.08, 1.61), p = 0.006) than children born in home settings of receiving basic vaccinations.
Discussion
We conducted a systematic review to identify the social determinants of childhood immunisation in low- and middle-income countries. We selected household wealth, religion, and ethnicity for socioeconomic characteristics; region and place of residence for geographic characteristics; maternal age at birth, maternal education, and maternal household head status for maternal characteristics; sex of child and birth order for child characteristics; and antenatal care and birth setting for healthcare characteristics. Based on the characteristics identified from the systematic review, we applied a social determinants framework to assess basic vaccination coverage (1-dose BCG, 3-dose DTP-HepB-Hib, 3-dose polio, and 1-dose measles) among children aged 12–23 months in Nigeria using the 2018 Nigeria DHS survey dataset.
The associations identified in this study between basic vaccination coverage and socioeconomic, geographic, maternal, child, and healthcare characteristics identified are supported by other studies. Basic vaccination coverage was associated with household wealth, and families in the richest quintile are more likely to live in urban areas with better access to functional private and public health facilities that provide immunisation services [24, 80]. Mothers in urban areas are more likely to use preventive healthcare services, including childhood immunisation, due to their proximity to healthcare facilities in urban settings and higher educational status in comparison to mothers in rural areas with higher travel costs [81–83]. Children in the richer households of rural areas had reduced odds of basic vaccination coverage in comparison to children in the poorest households of urban areas. Children of Fulani ethnicity had lower odds of basic vaccination compared to Igbo children, and there is evidence that awareness of immunisation is low amongst Fulani mothers [84, 85]. Further, Fulani ethnic groups reside in mostly rural settings and are nomadic, limiting their access to health services including immunisation services.
We found that basic vaccination coverage was associated with maternal education. Educated mothers have better awareness and knowledge on childhood immunisation and are more able to overcome cultural barriers to vaccination [86]. Maternal age was associated with basic vaccination coverage and older mothers may have more experience with antenatal clinics and have greater awareness of immunisation services from previous children [26]. They are also more likely to have financial access to immunisation services and live in urban settings with improved access to immunisation services.
Delivery in a health facility and antenatal care were associated with basic vaccination, and to give birth in a health facility indicates that mothers have overcome barriers to accessing health services, and mothers will also receive information on childhood immunisation from healthcare workers there. Hence, utilisation of health services by mothers leads to improved immunisation status of their children [87].
At the regional level, basic vaccination among children ranged from the lowest coverage in the North West region to nearly three times higher coverage in the South East region, although residents in Northern Nigeria are more likely to have immunisation services within 5 km [59]. The large degree of autonomy of different states and the impact of ongoing conflict in parts of the country, in addition to socio-cultural reasons, can explain in part the geographical disparity in immunisation services [14]. However, regional differences in coverage were not significant in the multivariable logistic regression model.
Despite vaccination being provided at no cost to individuals, coverage was still below target levels for even the most advantaged groups and therefore we recommend a proportionate universalism approach with actions proportionate to the level of disadvantage [88, 89]. There is some evidence of payment being required for vaccination, even in public health facilities, and this may threaten vaccination uptake [82]. Both the oversight of immunisation services and public awareness of vaccinations’ no cost status should be strengthened.
Higher coverage with more antenatal care indicates greater engagement with health services and thereby providing more opportunities for vaccine education. The integration of immunisation services to nutrition programmes and paediatric outpatient departments of primary healthcare centres has been shown to improve coverage and decrease drop-out rates in South Sudan [90]. Hence, we recommend efforts to engage with families during health care visits outside of routine immunisation services and to take advantage of these missed opportunities to reach under-immunised children [91].
Our estimates of vaccination coverage in Nigeria for 2018 were lower than national estimates based on administrative reporting from health service providers, though closer to WHO and UNICEF Estimates of National Immunization Coverage (WEUNIC) (see S4 Table) [92]. The coverage gaps have been shown to be systematically underestimated by administrative reporting in Nigeria [93]. In 80% of Nigerian states, the basic vaccination coverage was below the national target of 95% or higher coverage and below the Gavi target of 90% DTP3 coverage [94]. The below target coverage for first doses indicates challenges with access to immunisation services while the decrease in coverage for subsequent doses indicates drop-out due to insufficient knowledge on dose completion [9, 95, 96]. The COVID-19 pandemic has disrupted vaccination globally and coverage was lower than expected in Nigeria in 2020 [17, 18, 97], highlighting the urgent need for catch-up vaccination to close the immunity gaps and prevent vaccine-preventable disease outbreaks [98]. The role of conflict on these disparities is also important to understand. A literature review of conflict and vaccination inferred that conflict-affected countries had vaccination coverage below global levels and conflict affected vaccination services and human resources, including attacks on healthcare workers, which has happened in Nigeria [14, 70]. Our study inferences complement the findings in related studies in Nigeria and other countries.
The proportion of zero-dose children was high and raises the risk of vaccine-preventable disease outbreaks, with nearly 25% of children in rural areas not receiving a single dose of any of the basic vaccinations. Zero-dose children are also likely to lack access to health and welfare services and to suffer from multiple sources of deprivation [99, 100]. More than 50% of children do not have vaccination cards and nearly 60% of children do not have birth registrations [101] - improving uptake of vaccination cards and birth registrations would help in part to address the barriers for vaccine access for all children, including zero-dose children.
Our study has limitations, and we cannot estimate causal-effect relationships nor temporal inferences due to the cross-sectional study design of 2018 Nigeria DHS. Our study has similar biases that are associated with DHS surveys, including recall bias, measurement bias, and social desirability bias which tend to overestimate vaccination coverage. In particular, only 49% of children had a vaccination card and when a vaccination card was not available for a child, their mother was asked to recall their vaccinations, which may lead to an overestimation of coverage.
For future work, we recommend qualitative research to understand the barriers and enablers of childhood vaccination and their associations with socioeconomic, geographic, maternal, child, and healthcare characteristics which would be valuable to adapt vaccination programmes to improve coverage equitably in Nigeria.
Conclusions
We identified the inequities in basic vaccination coverage by socioeconomic, geographic, maternal, child, and healthcare characteristics among children aged 12–23 months in Nigeria using a social determinants of health perspective. In conclusion, we infer that inequities in basic vaccination were associated with lower coverage among children living in poorer households, belonging to Fulani ethnicity, born in home settings in Nigeria, with younger mothers at birth, with mothers with no formal education and with mothers who had no antenatal care visits. We recommend a proportionate universalism approach with targeted vaccination programmes proportionate to the level of disadvantage for addressing the immunisation barriers faced by these underserved subpopulations. This will improve coverage and reduce inequities in childhood immunisation associated with socioeconomic, geographic, maternal, child, and healthcare characteristics in Nigeria.
Supporting information
S1 Table. Routine vaccination schedule of under 1-year-old children in Nigeria.
https://doi.org/10.1371/journal.pone.0297326.s002
(DOCX)
S2 Table. Vaccination coverage and vaccination card usage rates in Nigeria.
https://doi.org/10.1371/journal.pone.0297326.s003
(DOCX)
S4 Table. Vaccine coverage.
Vaccine coverage estimates for Nigeria in 2018 based on DHS, WUENIC (WHO-UNICEF), administrative, and official country sources.
https://doi.org/10.1371/journal.pone.0297326.s005
(DOCX)
S1 Fig. PRISMA flowchart.
The Preferred Reporting Items for Systematic Reviews and Meta Analyses (PRISMA) flow diagram of articles’ identification, screening, eligibility, and inclusion in the systematic review is illustrated.
https://doi.org/10.1371/journal.pone.0297326.s006
(DOCX)
Acknowledgments
We thank the DHS Program for access to the 2018 Nigeria Demographic and Health Survey dataset.
References
- 1.
UNDP. World Population Prospects—Population Division—United Nations. 2019 [cited 1 Nov 2019]. Available: https://population.un.org/wpp/
- 2.
World Bank. Nigeria Overview: Development news, research, data | World Bank. 2020 [cited 21 Sep 2021]. Available: https://www.worldbank.org/en/country/nigeria/overview
- 3. Piot P, Larson HJ, O’Brien KL, N’kengasong J, Ng E, Sow S, et al. Immunization: vital progress, unfinished agenda. Nature. 2019;575: 119–129. pmid:31695203
- 4. Rodrigues CMC, Plotkin SA. Impact of vaccines; health, economic and social perspectives. Front Microbiol. 2020;11: 1526. pmid:32760367
- 5.
UNICEF. IGME: Levels and Trends in Child Mortality—UNICEF DATA. 2020 [cited 21 Sep 2021]. Available: https://data.unicef.org/resources/levels-and-trends-in-child-mortality/
- 6.
WHO. Immunization. 2019 [cited 21 Sep 2021]. Available: https://www.who.int/news-room/facts-in-pictures/detail/immunization
- 7. Carter A, Msemburi W, Sim SY, A.M. Gaythorpe K, Lindstrand A, Hutubessy RCW. Modeling the Impact of Vaccination for the Immunization Agenda 2030: Deaths Averted Due to Vaccination Against 14 Pathogens in 194 Countries from 2021–2030. SSRN Journal. 2021.
- 8.
Gavi. Facts and figures. 2021 [cited 21 Sep 2021]. Available: https://www.gavi.org/programmes-impact/our-impact/facts-and-figures
- 9. Cata-Preta BO, Santos TM, Mengistu T, Hogan DR, Barros AJD, Victora CG. Zero-dose children and the immunisation cascade: Understanding immunisation pathways in low and middle-income countries. Vaccine. 2021;39: 4564–4570. pmid:33744046
- 10. Decouttere C, De Boeck K, Vandaele N. Advancing sustainable development goals through immunization: a literature review. Global Health. 2021;17: 95. pmid:34446050
- 11.
WHO. Immunization Agenda 2030: A Global Strategy to Leave No One Behind. 2020 [cited 11 Jan 2021]. Available: https://www.who.int/teams/immunization-vaccines-and-biologicals/strategies/ia2030
- 12. Keja K, Chan C, Hayden G, Henderson RH. Expanded programme on immunization. World Health Stat Q. 1988;41: 59–63. pmid:3176515
- 13. Sorungbe AO. Expanded programme on immunization in Nigeria. Rev Infect Dis. 1989;11 Suppl 3: S509–11. pmid:2762695
- 14.
National Primary Health Care Development Agency. Comprehensive EPI Multi-Year Plan 2016–2020. Federal Ministry of Health, Nigeria; 2015.
- 15.
Gavi. Successfully transitioning Nigeria from Gavi support. 2018 [cited 21 Sep 2021]. Available: https://www.gavi.org/sites/default/files/board_meetings/2018/6_Jun/05%20-%20Successfully%20transitioning%20Nigeria%20from%20Gavi%20support.pdf
- 16.
WHO Africa. NERICC-Nigeria’s panacea to routine immunization and primary health care strengthening. | WHO | Regional Office for Africa. 2019 [cited 21 Sep 2021]. Available: https://www.afro.who.int/news/nericc-nigerias-panacea-routine-immunization-and-primary-health-care-strengthening
- 17. Causey K, Fullman N, Sorensen RJD, Galles NC, Zheng P, Aravkin A, et al. Estimating global and regional disruptions to routine childhood vaccine coverage during the COVID-19 pandemic in 2020: a modelling study. Lancet. 2021;398: 522–534. pmid:34273292
- 18. Fahriani M, Anwar S, Yufika A, Bakhtiar B, Wardani E, Winardi W, et al. Disruption of childhood vaccination during the COVID-19 pandemic in Indonesia. Narra J. 2021;1.
- 19. Oku A, Oyo-Ita A, Glenton C, Fretheim A, Eteng G, Ames H, et al. Factors affecting the implementation of childhood vaccination communication strategies in Nigeria: a qualitative study. BMC Public Health. 2017;17: 200. pmid:28202001
- 20. Marmot M, Friel S, Bell R, Houweling TAJ, Taylor S, Commission on Social Determinants of Health. Closing the gap in a generation: health equity through action on the social determinants of health. Lancet. 2008;372: 1661–1669. pmid:18994664
- 21.
WHO. Social determinants of health. 2021 [cited 18 Oct 2022]. Available: https://www.who.int/health-topics/social-determinants-of-health#tab=tab_3
- 22. Mulholland E, Smith L, Carneiro I, Becher H, Lehmann D. Equity and child-survival strategies. Bull World Health Organ. 2008;86: 399–407. pmid:18545743
- 23. Arcaya MC, Arcaya AL, Subramanian SV. Inequalities in health: definitions, concepts, and theories. Glob Health Action. 2015;8: 27106. pmid:26112142
- 24.
NPC/Nigeria, ICF. Nigeria Demographic and Health Survey 2018. National Population Commission Nigeria and ICF; 2019.
- 25.
Croft TN, Marshall AMJ, Allen CK. Guide to DHS Statistics. Rockville, Maryland, USA: ICF; 2018.
- 26.
WHO. WHO | Explorations of inequality: Childhood immunization. 2018 [cited 18 Sep 2019]. Available: https://apps.who.int/iris/handle/10665/272864
- 27. Moher D, Liberati A, Tetzlaff J, Altman DG, PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. PLoS Med. 2009;6: e1000097. pmid:19621072
- 28.
StataCorp. Stata: software for statistics and data science. College Station, Texas: StataCorp LP; 2019.
- 29.
Kirkwood BR, Sterne JAC. Essential Medical Statistics. 2nd ed. Wiley; 2003.
- 30.
WHO. Health Inequality Monitoring with a special focus on low- and middle-income countries. World Health Organization; 2013. Available: https://apps.who.int/iris/handle/10665/85345
- 31.
R Core Team. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2019.
- 32. Shenton LM, Wagner AL, Carlson BF, Mubarak MY, Boulton ML. Vaccination status of children aged 1–4 years in Afghanistan and associated factors, 2015. Vaccine. 2018;36: 5141–5149. pmid:30026033
- 33. Oliveira MFS de, Martinez EZ, Rocha JSY. Factors associated with vaccination coverage in children < 5 years in Angola. Rev Saude Publica. 2014;48: 906–915. pmid:26039393
- 34. Rahman A, Reza AAS, Bhuiyan BA, Alam N, Dasgupta SK, Mostari S, et al. Equity and determinants of routine child immunisation programme among tribal and non-tribal populations in rural Tangail subdistrict, Bangladesh: a cohort study. BMJ Open. 2018;8: e022634. pmid:30361402
- 35. Vyas P, Kim D, Adams A. Understanding spatial and contextual factors influencing intraregional differences in child vaccination coverage in Bangladesh. Asia Pac J Public Health. 2019;31: 51–60. pmid:30499306
- 36. Nda’chi Deffo R, Fomba Kamga B. Do the dynamics of vaccine programs improve the full immunization of children under the age of five in Cameroon? BMC Health Serv Res. 2020;20: 953. pmid:33059665
- 37. Ashbaugh HR, Hoff NA, Doshi RH, Alfonso VH, Gadoth A, Mukadi P, et al. Predictors of measles vaccination coverage among children 6–59 months of age in the Democratic Republic of the Congo. Vaccine. 2018;36: 587–593. pmid:29248265
- 38. Lakew Y, Bekele A, Biadgilign S. Factors influencing full immunization coverage among 12–23 months of age children in Ethiopia: evidence from the national demographic and health survey in 2011. BMC Public Health. 2015;15: 728. pmid:26224089
- 39. Geweniger A, Abbas KM. Childhood vaccination coverage and equity impact in Ethiopia by socioeconomic, geographic, maternal, and child characteristics. Vaccine. 2020;38: 3627–3638. pmid:32253099
- 40. Gram L, Soremekun S, ten Asbroek A, Manu A, O’Leary M, Hill Z, et al. Socio-economic determinants and inequities in coverage and timeliness of early childhood immunisation in rural Ghana. Trop Med Int Health. 2014;19: 802–811. pmid:24766425
- 41. Shrivastwa N, Gillespie BW, Kolenic GE, Lepkowski JM, Boulton ML. Predictors of vaccination in India for children aged 12–36 months. Vaccine. 2015;33 Suppl 4: D99–105. pmid:26615176
- 42. Devasenapathy N, Ghosh Jerath S, Sharma S, Allen E, Shankar AH, Zodpey S. Determinants of childhood immunisation coverage in urban poor settlements of Delhi, India: a cross-sectional study. BMJ Open. 2016;6: e013015. pmid:27566644
- 43. Khan J, Shil A, Prakash R. Exploring the spatial heterogeneity in different doses of vaccination coverage in India. PLoS ONE. 2018;13: e0207209. pmid:30485291
- 44. Francis MR, Nohynek H, Larson H, Balraj V, Mohan VR, Kang G, et al. Factors associated with routine childhood vaccine uptake and reasons for non-vaccination in India: 1998–2008. Vaccine. 2018;36: 6559–6566. pmid:28844636
- 45. Kannankeril Joseph VJ. Understanding inequalities in child immunization in India: a decomposition approach. J Biosoc Sci. 2021; 1–13. pmid:33722313
- 46. Srivastava S, Kumar P, Chauhan S, Banerjee A. Household expenditure for immunization among children in India: a two-part model approach. BMC Health Serv Res. 2021;21: 1001. pmid:34551769
- 47. Siramaneerat I, Agushybana F. Inequalities in immunization coverage in Indonesia: a multilevel analysis. Rural Remote Health. 2021;21: 6348. pmid:34432982
- 48. Van Malderen C, Ogali I, Khasakhala A, Muchiri SN, Sparks C, Van Oyen H, et al. Decomposing Kenyan socio-economic inequalities in skilled birth attendance and measles immunization. Int J Equity Health. 2013;12: 3. pmid:23294938
- 49. Masters NB, Wagner AL, Carlson BF, Muuo SW, Mutua MK, Boulton ML. Childhood vaccination in Kenya: socioeconomic determinants and disparities among the Somali ethnic community. Int J Public Health. 2019;64: 313–322. pmid:30535788
- 50. Allan S, Adetifa IMO, Abbas K. Inequities in childhood immunisation coverage associated with socioeconomic, geographic, maternal, child, and place of birth characteristics in Kenya. BMC Infect Dis. 2021;21: 553. pmid:34112096
- 51. Mutua MK, Mohamed SF, Iddi S, Muyingo S, Mwangi B, Kadengye D, et al. Do inequalities exist in the disadvantaged populations? Levels and trends of full and on-time vaccination coverage in two Nairobi urban informal settlements. Global Epidemiology. 2020;2: 100044. pmid:33363280
- 52. Sychareun V, Rowlands L, Vilay P, Durham J, Morgan A. The determinants of vaccination in a semi-rural area of Vientiane City, Lao People’s Democratic Republic: a qualitative study. Health Res Policy Syst. 2019;17: 2. pmid:30626379
- 53. Abebe DS, Nielsen VO, Finnvold JE. Regional inequality and vaccine uptake: a multilevel analysis of the 2007 Welfare Monitoring Survey in Malawi. BMC Public Health. 2012;12: 1075. pmid:23237082
- 54. Ntenda PAM, Chuang K-Y, Tiruneh FN, Chuang Y-C. Analysis of the effects of individual and community level factors on childhood immunization in Malawi. Vaccine. 2017;35: 1907–1917. pmid:28284678
- 55. Daca C, Sebastian MS, Arnaldo C, Schumann B. Socio-economic and demographic factors associated with reproductive and child health preventive care in Mozambique: a cross-sectional study. Int J Equity Health. 2020;19: 200. pmid:33168017
- 56. Patel PN, Hada M, Carlson BF, Boulton ML. Immunization status of children in Nepal and associated factors, 2016. Vaccine. 2021;39: 5831–5838. pmid:34456076
- 57. Antai D. Inequitable childhood immunization uptake in Nigeria: a multilevel analysis of individual and contextual determinants. BMC Infect Dis. 2009;9: 181. pmid:19930573
- 58. Antai D. Gender inequities, relationship power, and childhood immunization uptake in Nigeria: a population-based cross-sectional study. Int J Infect Dis. 2012;16: e136–45. pmid:22197748
- 59. Eboreime E, Abimbola S, Bozzani F. Access to Routine Immunization: A Comparative Analysis of Supply-Side Disparities between Northern and Southern Nigeria. PLoS ONE. 2015;10: e0144876. pmid:26692215
- 60. Ataguba JE, Ojo KO, Ichoku HE. Explaining socio-economic inequalities in immunization coverage in Nigeria. Health Policy Plan. 2016;31: 1212–1224. pmid:27208896
- 61. Uzochukwu BS, Okeke CC, Envuladu E, Mbachu C, Okwuosa C, Onwujekwe OE. Inequity in access to childhood immunization in Enugu urban, Southeast Nigeria. Niger J Clin Pract. 2017;20: 971–977. pmid:28891541
- 62. Uthman OA, Adedokun ST, Olukade T, Watson S, Adetokunboh O, Adeniran A, et al. Children who have received no routine polio vaccines in Nigeria: Who are they and where do they live? Hum Vaccin Immunother. 2017;13: 2111–2122. pmid:28665749
- 63. Obanewa OA, Newell ML. The role of place of residency in childhood immunisation coverage in Nigeria: analysis of data from three DHS rounds 2003–2013. BMC Public Health. 2020;20: 123. pmid:31996184
- 64. Siddiqui NT, Owais A, Agha A, Karim MS, Zaidi AKM. Ethnic disparities in routine immunization coverage: a reason for persistent poliovirus circulation in Karachi, Pakistan? Asia Pac J Public Health. 2014;26: 67–76. pmid:23420055
- 65. Canavan ME, Sipsma HL, Kassie GM, Bradley EH. Correlates of complete childhood vaccination in East African countries. PLoS ONE. 2014;9: e95709. pmid:24752178
- 66. Wariri O, Edem B, Nkereuwem E, Nkereuwem OO, Umeh G, Clark E, et al. Tracking coverage, dropout and multidimensional equity gaps in immunisation systems in West Africa, 2000–2017. BMJ Glob Health. 2019;4: e001713. pmid:31565416
- 67. Ndwandwe D, Uthman OA, Adamu AA, Sambala EZ, Wiyeh AB, Olukade T, et al. Decomposing the gap in missed opportunities for vaccination between poor and non-poor in sub-Saharan Africa: A Multicountry Analyses. Hum Vaccin Immunother. 2018;14: 2358–2364. pmid:29688133
- 68. Sambala EZ, Uthman OA, Adamu AA, Ndwandwe D, Wiyeh AB, Olukade T, et al. Mind the Gap: What explains the education-related inequality in missed opportunities for vaccination in sub-Saharan Africa? Compositional and structural characteristics. Hum Vaccin Immunother. 2018;14: 2365–2372. pmid:29630441
- 69. Ameyaw EK, Kareem YO, Ahinkorah BO, Seidu A-A, Yaya S. Decomposing the rural-urban gap in factors associated with childhood immunisation in sub-Saharan Africa: evidence from surveys in 23 countries. BMJ Glob Health. 2021;6. pmid:33452139
- 70. Grundy J, Biggs B-A. The impact of conflict on immunisation coverage in 16 countries. Int J Health Policy Manag. 2019;8: 211–221. pmid:31050966
- 71. Arsenault C, Harper S, Nandi A, Rodríguez JMM, Hansen PM, Johri M. An equity dashboard to monitor vaccination coverage. Bull World Health Organ. 2017;95: 128–134. pmid:28250513
- 72. Arsenault C, Johri M, Nandi A, Mendoza Rodríguez JM, Hansen PM, Harper S. Country-level predictors of vaccination coverage and inequalities in Gavi-supported countries. Vaccine. 2017;35: 2479–2488. pmid:28365251
- 73. Bosch-Capblanch X, Banerjee K, Burton A. Unvaccinated children in years of increasing coverage: how many and who are they? Evidence from 96 low- and middle-income countries. Trop Med Int Health. 2012;17: 697–710. pmid:22943300
- 74. Merten S, Martin Hilber A, Biaggi C, Secula F, Bosch-Capblanch X, Namgyal P, et al. Gender Determinants of Vaccination Status in Children: Evidence from a Meta-Ethnographic Systematic Review. PLoS ONE. 2015;10: e0135222. pmid:26317975
- 75. Hinman AR, McKinlay MA. Immunization Equity. Am J Prev Med. 2015;49: S399–405. pmid:26282089
- 76. Awoh AB, Plugge E. Immunisation coverage in rural-urban migrant children in low and middle-income countries (LMICs): a systematic review and meta-analysis. J Epidemiol Community Health. 2016;70: 305–311. pmid:26347277
- 77. Hosseinpoor AR, Bergen N, Schlotheuber A, Gacic-Dobo M, Hansen PM, Senouci K, et al. State of inequality in diphtheria-tetanus-pertussis immunisation coverage in low-income and middle-income countries: a multicountry study of household health surveys. Lancet Glob Health. 2016;4: e617–26. pmid:27497954
- 78. Hajizadeh M. Socioeconomic inequalities in child vaccination in low/middle-income countries: what accounts for the differences? J Epidemiol Community Health. 2018;72: 719–725. pmid:29581228
- 79. Hajizadeh M. Decomposing socioeconomic inequality in child vaccination in the Gambia, the Kyrgyz Republic and Namibia. Vaccine. 2019;37: 6609–6616. pmid:31558326
- 80. Adebowale A, Obembe T, Bamgboye E. Relationship between household wealth and childhood immunization in core-North Nigeria. Afr Health Sci. 2019;19: 1582–1593. pmid:31148987
- 81. Adenike O-B, Adejumoke J, Olufunmi O, Ridwan O. Maternal characteristics and immunization status of children in North Central of Nigeria. Pan Afr Med J. 2017;26: 159. pmid:28588745
- 82. Sibeudu FT, Uzochukwu BS, Onwujekwe OE. Rural-urban comparison of routine immunization utilization and its determinants in communities in Anambra States, Nigeria. SAGE Open Med. 2019;7: 2050312118823893. pmid:30719291
- 83. Okafor IP, Dolapo DC, Onigbogi MO, Iloabuchi IG. Rural-urban disparities in maternal immunization knowledge and childhood health-seeking behavior in Nigeria: a mixed method study. Afr Health Sci. 2014;14: 339–347. pmid:25320582
- 84. Dao MY, Brieger WR. Immunization for the migrant fulani: identifying an under-served population in southwestern Nigeria. Int Q Community Health Educ. 1994;15: 21–32. pmid:20841016
- 85. Afolabi RF, Salawu MM, Gbadebo BM, Salawu AT, Fagbamigbe AF, Adebowale AS. Ethnicity as a cultural factor influencing complete vaccination among children aged 12–23 months in Nigeria. Hum Vaccin Immunother. 2021;17: 2008–2017. pmid:33605835
- 86. Balogun SA, Yusuff HA, Yusuf KQ, Al-Shenqiti AM, Balogun MT, Tettey P. Maternal education and child immunization: the mediating roles of maternal literacy and socioeconomic status. Pan Afr Med J. 2017;26: 217. pmid:28690731
- 87. Adedokun ST, Uthman OA, Adekanmbi VT, Wiysonge CS. Incomplete childhood immunization in Nigeria: a multilevel analysis of individual and contextual factors. BMC Public Health. 2017;17: 236. pmid:28270125
- 88. Carey G, Crammond B, De Leeuw E. Towards health equity: a framework for the application of proportionate universalism. Int J Equity Health. 2015;14: 81. pmid:26369339
- 89. Marmot M, Bell R. Fair society, healthy lives. Public Health. 2012;126 Suppl 1: S4–10. pmid:22784581
- 90. Idris IO, Obwoya JG, Tapkigen J, Lamidi SA, Ochagu VA, Abbas K. Impact evaluation of immunisation service integration to nutrition programmes and paediatric outpatient departments of primary healthcare centres in Rumbek East and Rumbek Centre counties of South Sudan. Family Med Commun Hlth. 2021;9. pmid:34433617
- 91. Restrepo-Méndez MC, Barros AJD, Wong KLM, Johnson HL, Pariyo G, Wehrmeister FC, et al. Missed opportunities in full immunization coverage: findings from low- and lower-middle-income countries. Glob Health Action. 2016;9: 30963. pmid:27146444
- 92.
WHO, UNICEF. WUENIC (WHO/UNICEF Estimates of National Immunization Coverage) estimates—Vaccines monitoring system 2019 Global Summary Reference Time Series. 2019 [cited 11 Jun 2023]. Available: https://www.who.int/teams/immunization-vaccines-and-biologicals/immunization-analysis-and-insights/global-monitoring/immunization-coverage/who-unicef-estimates-of-national-immunization-coverage
- 93. Gunnala R, Ogbuanu IU, Adegoke OJ, Scobie HM, Uba BV, Wannemuehler KA, et al. Routine Vaccination Coverage in Northern Nigeria: Results from 40 District-Level Cluster Surveys, 2014–2015. PLoS ONE. 2016;11: e0167835. pmid:27936077
- 94.
Gavi. 2019 Annual Progress Report. 2020 [cited 21 Sep 2021]. Available: https://www.gavi.org/sites/default/files/programmes-impact/our-impact/apr/Gavi-Progress-Report-2019_1.pdf
- 95. Adedire EB, Ajayi I, Fawole OI, Ajumobi O, Kasasa S, Wasswa P, et al. Immunisation coverage and its determinants among children aged 12–23 months in Atakumosa-west district, Osun State Nigeria: a cross-sectional study. BMC Public Health. 2016;16: 905. pmid:27578303
- 96. Odusanya OO, Alufohai EF, Meurice FP, Ahonkhai VI. Determinants of vaccination coverage in rural Nigeria. BMC Public Health. 2008;8: 381. pmid:18986544
- 97. Tatar M, Shoorekchali JM, Faraji MR, Wilson FA. International COVID-19 vaccine inequality amid the pandemic: Perpetuating a global crisis? J Glob Health. 2021;11: 03086. pmid:34221356
- 98.
WHO. Leave No One Behind: Guidance for Planning and Implementing Catch-up Vaccination. 2020 [cited 1 Feb 2021]. Available: https://www.who.int/teams/immunization-vaccines-and-biologicals/essential-programme-on-immunization/implementation/catch-up-vaccination/
- 99.
WHO. Progress and Challenges with Achieving Universal Immunization Coverage. 2020 [cited 22 Dec 2022]. Available: https://www.who.int/publications/m/item/progress-and-challenges-with-achievinguniversal-immunization-coverage
- 100. Bhatia A, Krieger N, Beckfield J, Barros AJD, Victora C. Are inequities decreasing? Birth registration for children under five in low-income and middle-income countries, 1999–2016. BMJ Glob Health. 2019;4: e001926. pmid:31908868
- 101.
United Nations Children’s Fund,. Birth Registration for Every Child by 2030: Are we on track? UNICEF; 2019.