A systematic review on the effect of the COVID-19 pandemic on childhood immunisation programmes of West African countries

the COVID-19 virus. Conclusion: While the changes were greater than 50% and lasted longer in some countries, they were brief and short-lived in others, emphasising that the COVID-19 pandemic's effect in each country differed.


INTRODUCTION
The expanded programme on immunisation (EPI) was birthed on the heels of the success of the smallpox vaccination programme. 1and integrated into routine maternal and childhood services, offering mobile and facility-based immunisation services.3][4][5] Furthermore, the EPI allowed the domestication of the vaccines provided in the scheme based on local and prevailing epidemiologic factors, which has led to the introduction of the Hepatitis, Yellow fever, Meningococcal and Pneumococcal vaccines. 6,7The EPI also allowed for the conduct of National immunisation days (NIDs), Supplemental immunisation activities (SIAs) and catch-up immunisation campaigns to supplement routine immunisation services. 8,91][12] DPT vaccination is routinely used to estimate vaccine utilisation, coverage and access. 13,14DPT1 vaccine coverage indicates entry points into the EPI programme, while DPT3 measures the programme's ability to retain the children.DPT dropout rates of > 10% denote poor utilisation of vaccine services. 15ccines have become one of the most cost-effective public health interventions. 16Over 116 million children are vaccinated annually (86% of all children born), and the use of vaccines has expanded to cover over 20 diseases and is being used to control epidemics or pandemics. 17frican regional DPT3 coverage was 52% in 2010, which increased to 76% by 2015, with 34% of African countries achieving greater than 90% national coverage 18 , and by 2019, global DPT3 coverage averaged 81.6 % 19 .Similarly, African regional MCV1 coverage increased from 53% in 2000 to 74% in 2015, with Twelve African countries (26%) achieving more than 90% national coverage.BCG vaccines currently have the highest coverage, and the Oral Polio vaccine has the lowest coverage, according to a study among 25 sub-Saharan countries 20 .
However, vaccine access globally is still inequitable, adversely affecting marginalised and poor populations.Over 13 million children are currently classed as "zerodose children" because they have not had a single dose of a potentially life-saving vaccine 16 , 75% of whom live in 14 Low to Middle-income countries(LMICs). 19nother 30 million children in these areas also do not receive the full complement of vaccination even when available 16 .Due to the poor distribution or access to vaccines, diseases that may have been on a downward trend have been resurgent.For example, vaccine-derived poliovirus is becoming a problem in many African countries. 21, and the incidence of measles has doubled in the last three years (2019-2021). 213][24] Furthermore, 13.5 million children missed doses of their vaccines in thirteen of the world's poorest countries 25,26 amidst reports of fresh outbreaks of the wild poliovirus in Afghanistan and Pakistan. 27Vaccine shipment was reduced by 80%, and lockdown regulations disrupted the production of vaccines. 28,293][24] For example, the WHO initially recommended suspending immunisations in the first few months of the COVID-19 pandemic because it feared the virus would spread during routine immunisations. 30[33][34] Given the fragility of health systems in West Africa and the struggle to achieve good childhood immunisation coverage, the risk of severe disruption to childhood immunisation programmes due to the COVID-19 pandemic exists.This review aims to quantify the COVID-19 pandemic's effects on West African immunisation programmes and conceptually synthesise why the pandemic had such an effect.

METHODS
The study was a systematic review without meta-analysis(SwiM) of all peer-reviewed longitudinal, descriptive, observational, prospective and retrospective studies on childhood immunisation programmes in West Africa published between January 2020 and May 2022.
The COVID-19 pandemic had its most disruptive impact on healthcare in 2020, and this period was selected to enable the review to capture as many reports/studies on the subject as possible, taking into account the varying length of time for peer review and publishing.
The protocol for this study was based on the Preferred Reporting Items for Systematic Reviews and Metaanalysis Protocols-PRISMA-P. 35A preliminary search was conducted using the PubMed database to validate the premise and availability of peer-reviewed articles covering the subject.Subsequently, a defined search strategy was designed(Figure 1).

Inclusion criteria
All peer-reviewed longitudinal, descriptive, observational, prospective, and retrospective studies published between 2020 and May 2022 that studied or described the effects of the COVID-19 pandemic on childhood immunization programmes in West Africa were deemed eligible.
Also included were studies that described or studied the effects of the COVID-19 pandemic on vaccination coverage and the utilisation of these services directly via vaccination numbers and trends by comparing pre and post-COVID-19 values and allowing for analysis of vaccine coverage and factors affecting coverage.
The review also included all modelling studies that used pre-COVID-19 data to estimate the impacts of the COVID-19 pandemic on immunisation programmes.In addition, Qualitative studies that explored the effect of the COVID-19 pandemic on the experiences of caregivers or parents accessing childhood vaccination services and healthcare workers providing childhood vaccination services were included.
An article was deemed to have studied the correct population (Childhood immunisation programmes in West Africa) and included in the review if it showed results on at least one of the BCG, Measles, Polio, Diphtheriapertussis, Pentavalent, Meningococcal or Yellow Fever vaccines in at least one West African country.For this review, only the results from the West African country were included for analysis.There were no language restrictions, and studies not in English were run through the Google translator AI (Google Translate) and then analysed.

Exclusion criteria
This study excluded systematic reviews, modelling studies that excluded pre-COVID-19 vaccination data, and papers that did not estimate the impact of the COVID-19 pandemic on childhood vaccine coverage.

Information sources and search strategy
OCO and VAO conducted a literature search in the PubMed, Embase, Scopus, and Web of Science databases and filtered it to allow only papers published between January 2020 and May 2022.The search strategy explored alternate search words for the main question items and used British and American spellings where necessary.Truncation and quotes were used to broaden the search parameters.Boolean commands "AND" and "OR" were used to combine search groups ( ).

Study records/screening
Search results from the respective databases were saved, downloaded, and imported into the Rayyan (www.rayyan.ai)web-based data management software. 36ticles were deduplicated in Rayyan and manually reviewed by OCO and VAO.Titles and abstracts were screened based on the inclusion criteria.After that, a full-text screening of the remaining articles on Rayyan was performed.Agreement on article inclusion between OCO and VAO was required before being included for further analysis.The included articles had their references screened to determine if any relevant citations were suitable for inclusion.

Data management
Following full-text screening and review, relevant data were extracted using a form created in Excel by one reviewer-OCO.For quantitative data, the data extracted included author, title, year of publication, study design, study population, length of study, inclusion criteria met by the paper, study aim, vaccine and vaccine characteristics studied, and data collection mode.The form also extracted the included studies' results, statistical methods, conclusions, and recommendations.For Qualitative data, the data extracted included author, title, year of publication, study population, length of study, study aim, vaccine and vaccine characteristics studied, data collection mode (KIs, FGD), major themes that emerged from the paper, conclusions, and recommendations by the article.Data analysis was based on the framework of Phillips et al. on factors determining vaccine coverage and contributing to inequalities in vaccine access (Figure 2). 37For quantitative studies, proportions and differences in vaccination numbers were extracted from the studies and analysed by country.In contrast, qualitative studies were analysed along thematic lines identified by the authors.All forms of studies were analysed following the conceptual framework for vaccination coverage (Figure 2).

Quality assessment
Quality for quantitative studies was assessed at the study design level to determine the presence or absence of bias during data collection, reporting, and management, including missing data handling, appropriate use of relevant statistical tests and methods, and data interpretation.Quality assessment for the qualitative studies was carried out using the four criteria described by Lincoln et al. 38,39 These criteria include credibility, dependability, confirmability, and transferability.
These quality assessment criteria were used because they allowed for a more flexible quality assessment in the dynamic context of the COVID-19 Pandemic.search of the references in the selected articles did not reveal any paper relevant to this review (Figure 3).

Study characteristics
The review included six quantitative studies on vaccination coverage trends before and during the COVID-19 pandemic [40][41][42][43][44][45] , one qualitative study on the utilisation of immunisation services during the COVID-19 pandemic 46 , and one mixed methodquantitative and qualitative study-on vaccination coverage and the utilisation of immunisation services. 47ata from eight of 17 West African countries were included in this review: Ghana. 42,47, Guinea 42 , Liberia 44,45 , Mali 45 , Niger 40 , Nigeria 42,45,46 , Senegal 42,43 , Sierra Leona. 41,45antitative Studies The tables below summarise quantitative data extracted along individual vaccine lines from the eligible studies.Copyright © The Author(s).This is an Open Access article under the CC BY license. 169

Qualitative studies
Two qualitative studies were included in this study. 62,63 d were analysed along thematic lines based on Phillips et al.'s framework for the determinants of vaccination coverage 55

Quality analysis
At the study design level, all quantitative studies relied on data collected via registries of data reports from various national registries.Only two studies 44,45 Explicitly stated how missing data were managed.One study 47 Mentioned missing data but did not state how this was handled.Other studies were silent about missing data.
Sample sizes were not explicitly stated for all studies.However, one study 41

Table 8 Quality analysis
Both qualitative studies showed some quality as the papers used appropriate research processes/procedures to answer the questions.However, while Bimpong 47 detailed the sampling procedure and process, Ahmed 46 did not provide any information about the sampling process or procedure, so the representability of his sample could not be determined.Furthermore, neither study was explicit on the methodology or framework used for their chosen approaches, nor were their methods fully justified.Bimpong provided some information about the qualitative process to replicate their study if necessary and utilised quotes to aid descriptions and findings compared to Ahmed. 46

DISCUSSION
The impact of the COVID-19 pandemic on West African countries' immunisation programmes can be described along three major themes (Figure 4).The most significant changes in vaccination volumes (>50%) occurred in April 2020 across the eight countries in this review.However, these changes in April may not have been solely due to the direct effects of the COVID-19 pandemic because this period coincided with the WHO directive recommending the suspension of mass immunisation programmes and the reduction of routine immunisation programmes due to concerns about the transmission of the Covid-19 virus. 30However, the continued changes to immunisation coverage noted in this review may be attributed directly to the pandemic alongside other factors like the strength of the health system before COVID-19 and the successes of the childhood immunisation programme before the pandemic.All of these contributed to the varying impact of the COVID-19 pandemic on childhood immunisation programmes in West African countries by impacting critical components of the vaccination cycle and determinants of vaccination coverage. 37,49untries with high pre-pandemic vaccination coverage, like Ghana, Senegal and Liberia, experienced minimal (<20%) and short-lived changes to vaccination volumes during the COVID-19 pandemic.However, measles outbreaks were still common in these countries, pointing to local contextual factors that may have pre-existed and Copyright © The Author(s).This is an Open Access article under the CC BY license.
1][52][53] Countries like Niger and Sierra Leone reported high vaccine coverage before the COVID-19 pandemic but witnessed reductions in immunisation during the COVID-19 pandemic lasting longer than August 2020.
However, these pre-pandemic gains may have been lost during the COVID-19 pandemic due to pre-existing high levels of insecurity, political unrest, poor vaccine storage and distribution, and a lack of a sustainable health system resilience plan combined with the effects of the COVID-19 pandemic.Other countries in this review-Nigeria, Mali, and Guinea-have poor pre-pandemic vaccine coverage and have demonstrated reduced vaccination coverage throughout the COVID-19 pandemic.The reported reductions in coverage were possibly due to the amplification of already existing inequalities in vaccine distribution and utilisation, pre-existing security challenges and political instability.
Five of the eight countries (Guinea, Mali, Nigeria, Niger, Sieera-Leone) in this review had significant reductions (>50%) in childhood vaccination coverage during the COVID-19 pandemic.When these reductions are viewed in light of the pre-existing challenges in these countries, the potential national and regional impacts on childhood health become enormous.While these disruptions' medium to long-term effects may not be known, the shortterm effects are currently being reported.The WHO says that a resurgence in vaccine-preventable diseases is rising in Africa. 54In 2022, between January and March, 17,500 cases (400% increase) of measles were reported from 20 African countries, eight more countries compared to the same period in 2021. 54e West African region contributed about 44% of measles cases (Nigeria 5,613, Cote d'Ivoire 1,075, Mali 946 contributing the most cases). 55Twenty African countries reported a variant of polio in 2020, which increased to Twenty-four in 2021. 54While all African countries except Malawi have been certified wild polio virus-free, the continent still has vaccine-derived poliovirus to contend with 54 Ten countries in West Africa have circulating vaccine-derived poliovirus infections.Only Togo and Ghana are polio-free in the region.The reduction of vaccinations caused by the COVID-19 pandemic is capable of causing the cross-border spread of vaccine-derived poliovirus, leading to a regional poliovirus crisis and worsening the poliovirus epidemics within West African Countries.
Hence, it is imperative that in the short term, catch-up immunisation programmes to provide the missed doses of vaccines be done in countries that experienced severe disruptions.These countries may also employ more National Immunisation days and Supplemental Immunisation activities to improve vaccine coverage.In the medium to long term, strengthening the facility readiness, improving community access, and increasing the intent to vaccinate while strengthening health system resilience should be pursued.Facility readiness, described as the ability of the existing health system to supply vaccines to meet demand, can be influenced by varying factors.An Important factor influencing facility readiness is the government's political will and the provision and management of funding.Copyright © The Author(s).This is an Open Access article under the CC BY license.
174 This review showed that programmes with a history of strong political and governmental support and good funding, e.g., Senegal, perform better than programmes with poor funding, poor political will, and government support, e.g., Guinea.Another factor directly affecting facility readiness and funding is the provision of adequate vaccine distribution, supply and storage. 57Distribution, supply, and storage are essential to prevent stock-outs and ensure that a facility continues offering vaccine services.Proper distribution and storage also ensure that the vaccine provided to children is high-quality.The availability of trained healthcare workers in adequate numbers is also pivotal to a facility's success in providing vaccine services.
The ability to bridge the facility's readiness to provide immunisation services and the intent to vaccinate depends on the community's access to these services.9][60] Contextualised bottom-up approaches like the community-driven comprehensive national immunisation programme in Senegal or the community engagement, social mobilisation and communication strategy of Liberia provide room for end-users ownership of the health system and improve community access to vaccines. 49,61plications for policy Health shocks like the COVID-19 pandemic are on the rise.Therefore, policies that strengthen the available health system are imperative to prevent these shocks' effects on the health system.Policies that improve facility readiness-improving community access to vaccines, storage and distribution of vaccines-and better government funding and support are essential to withstand the effects of health shocks.

Limitations of the review
A limitation of this review is that the currently available evidence is few and heterogeneous.Except for DPT3 and MCV vaccines, not all vaccines were studied for all countries, making estimating the pandemic's effect on childhood immunisation programmes within and between the countries along respective vaccine lines challenging.

CONCLUSION
The pandemic may have amplified pre-existing inequalities in vaccine access and system weakness, which hampered the provision of vaccination services during the pandemic.While the changes in the immunisation programmes were significant and lasted longer in some countries like Nigeria, Guinea, Mali, Sierra-leone and Niger, they were less substantial and short-lived in others

Figure 2
Figure 2Conceptual framework for vaccine coverage.37 Three hundred fifty-three (353) publications from four databases were retrieved.Retrieved results included 233, 8, 104 and 0 from PubMed, Scopus, Web of Science and Embase, respectively, on 22/02/2022.Eight results were retrieved from PubMed on 11/03/2022, while the other databases returned no additional results.The databases returned no other results at the last search session on 09/05/2022.Following deduplication, 259 studies were screened, and 230 publications were excluded due to a wrong publication type/irrelevant study.The full texts of 29 studies were retrieved and screened for inclusion.On full-text screening, twenty-one articles were excluded based on a wrong study population, study design or being a background article, e.g., editorials or letters to the editor.Eight studies were finally included in this review, and a

Figure 3
Figure 3 PRISMA flowchart of the systematic search process

Figure 4
Figure 4 Conceptualising the impact of the COVID-19 pandemic on childhood immunisation programmes in studied West African Countries.

Table 1
Summary of quantitative studies

Table 3
www.ghanamedj.orgVolume58 Number 2 June 2024Copyright © The Author(s).This is an Open Access article under the CC BY license.170

Table 1
Summary table of reductions in immunisation volumes in percentages from March 2020 -August 2021 showing national and subnational figures

Table 2 2019
48tional infant childhood immunisation coverage estimates in percentages before the pandemic.WHO-UNICEF estimates.48

Table 3
42utine DPT3 And MCV immunisation performance In West African countries during the pandemic.42

Table 4
45sruptions In BCG and PENTA3 vaccine coverage in West African countries during COVID-19.45 Copyright © The Author(s).This is an Open Access article under the CC BY license.

Table 6
41 )d healthcare and immunisations in Sierra Leone during the pandemic (Adapted from Buonsenso et al.41 )