Human papillomavirus vaccination uptake and determinant factors among adolescent schoolgirls in sub-Saharan Africa: A systematic review and meta-analysis

ABSTRACT

Despite the ongoing global vaccination campaign aimed at preventing human papillomavirus (HPV) related health issues, the uptake of the HPV vaccine remains unacceptably low in developing regions, particularly in sub-Saharan Africa (SSA). Therefore, this systematic review and meta-analysis aimed at determining the pooled prevalence and associated factors of HPV vaccine uptake among adolescent school girls in SSA. Electronic bio-medical databases were explored. Pooled prevalence, publication bias, meta-regression, sub-group, and sensitivity analysis were performed. The estimated pooled prevalence of HPV vaccine uptake was 28.53% [95% CI: (5.25, 51.81)]. Having good knowledge and a positive attitude was significantly associated with HPV vaccine uptake in SSA. Subgroup analysis revealed the highest uptake was 62.52% from Kenya and the lowest was 3.77% in Nigeria. The HPV vaccine uptake is low. It underscores the need for community education, school-based immunization, and education programs that promote the uptake of the vaccine to increase coverage.

KEYWORDS:

• Uptake
• human papilloma virus vaccine
• adolescent
• sub-Saharan Africa
• systematic review
• meta-analysis

Introduction

Human papillomavirus (HPV) is one of the most common sexually transmitted infections in the world. HPV infection can lead to the development of cervical cancer.¹ HPV has more than 130 serotypes as low and high risk: high-risk serotypes (HPV 16, 18) can cause cancers such as cervical cancer, though the low-risks cause benign warts.² There is a risk for all women that HPV infection may become chronic and pre-cancerous lesions progress to invasive cervical cancer.¹

Cervical cancer is the fourth most common cancer in women and globally about 7.5% of cancer-related deaths among women are attributed to it.^1,3 In 2020, estimated 604,000 women were diagnosed with cervical cancer and about 342,000 deaths from the disease across the world, while low- and middle-income countries account for more than 90% of the deaths.^4,5 In sub-Saharan Africa (SSA), cervical cancer is the second leading cause of female cancer which accounts for 22.5% of all cancer cases. Moreover, about 117,316 females were diagnosed annually with the disease.⁶ Cervical cancer most predominantly affects young, uneducated females living in less developed countries where access to information about the disease, screening, and treatment is inadequate.⁵

The introduction of HPV vaccination has been considered a significant breakthrough in the prevention of cervical cancer and other HPV-related diseases.⁷ The vaccine protects against HPV type 16 and 18 (high-risk strains), which are known to cause at least 70% of the cervical cancers. Unlike high-income countries, less than 30% of low- and middle-income countries have implemented the HPV vaccination program, with only about 3% of the teenagers being vaccinated against HPV and around 44% of the women being screened for cervical cancer.⁸

HPV vaccines, like Gardasil and Cervarix, have been successful in reducing HPV-related diseases, especially among young women who receive the vaccine before becoming sexually active.⁹ These vaccines provide long-lasting immunity and high efficacy rates in preventing HPV-related diseases, as well as the potential to reduce health-care costs. They have also shown efficacy in preventing genital warts and certain pre-cancerous lesions. However, there are some potential cons, including the need for multiple doses and potential side effects. Before approval, the vaccines underwent clinical trials involving various populations, including males and females between the ages of 9–26 years old. The level of protection provided by the vaccines varies depending on the specific vaccine and the strain of HPV targeted.^10,11

Sixty-four countries have launched national immunization programs for the HPV vaccine to achieve the 2030 Sustainable Development Goal (SDG) of vaccinating 90% of the girls by age 15. Studies have shown an 83% reduction in HPV 16 and 18 infections after 8 years of vaccine administration for girls aged 13–19.¹² A single dose of the vaccine can prevent 70% of the cervical cancers, similar to two or three doses. The vaccine is most effective when administered before exposure to HPV, so the WHO recommends vaccinating girls between the ages of 9 and 14.^5,13 The practical vaccination age in Africa varies. The recommended age range for HPV vaccination in Africa is typically between 9 and 13 years old, considering factors such as cultural differences, religious beliefs, perceptions, and behavior. Vaccinating girls within this age range before they become sexually active reduces the risk of HPV infection. Vaccinating girls within this age range before they become sexually active reduces the risk of HPV infection. In many African cultures, vaccinating young girls is seen as a way to protect their health and well-being, while also aligning with religious teachings about abstinence and purity. Based on the research findings, parents in sub-Saharan Africa were supportive of vaccinating their daughters if the vaccine was framed as a preventative measure for cervical cancer.¹⁴

While the HPV vaccine has been available for about 15 years, the coverage remains as low as 20% in SSA countries compared to 80% in Scotland.¹⁵ The reasons behind the low vaccine uptake were numerous and complex, including a lack of awareness about the vaccine, limited access to health-care facilities, and insufficient availability of the vaccine. Furthermore, cultural and social beliefs also played a crucial role in the low uptake of the vaccine

The uptake of the HPV vaccine is a critical factor in addressing the burden of cervical cancer. Therefore, it is vital to have evidence from SSA, one of the regions with the highest burden of HPV infection, and align with the global strategy for eliminating cervical cancer. This systematic review and meta-analysis aimed to determine the pooled estimates of HPV vaccine uptake and its determinants among adolescent school girls in sub-Saharan Africa. These findings could aid in designing evidence-based interventions and measures aimed at improving the availability and accessibility of the vaccine in low-resource settings (i.e. SSA region). Furthermore, policymakers, health-care providers, and researchers in sub-Saharan Africa can use these findings to make evidence-based decisions and put in place interventions that help improve the uptake level of the vaccine.

Review Question:

What is the pooled uptake level of HPV vaccine and associated factors among adolescent school girls in sub-Saharan Africa?

Methods

Reporting

This systematic review and meta-analysis followed the Preferred Reporting Items for Systematic Review and Meta-Analysis for Protocols (PRISMA-P) 2020¹⁶ (Figure 1) and the Meta-analysis of Observational Studies in Epidemiology (MOOSE) guideline.¹⁷ The results were reported based on the PRISMA statement, and the article screening and selection process was demonstrated through a PRISMA-P flow diagram. The updated PRISMA checklist guideline was used for reporting HPV vaccine uptake among adolescent school girls in sub-Saharan Africa (Supplementary File 1). This review is registered with the International Prospective Register of Systematic Reviews (PROSPERO) (registration number: CRD42023443554).

Figure 1. PRISMA flow diagram of screened and the selection process of studies on pooled prevalence of HPV vaccine uptake and determinant factors among adolescent school girls in sub-Saharan Africa, 2023.

Search strategy

We performed a complete search of electronic databases, such as PubMed/MEDLINE, EMBASE, Science Direct, Web of Science, and Google Scholar, to find relevant articles on the topic of interest. Articles written in English were searched for in this review. References from retrieved articles were also used to manually search for additional relevant articles if they were missed. The search strings or terms stemmed from the following keywords: uptake, practice, utilization, papillomavirus vaccines, vaccines, human papillomavirus vaccine, adolescents, schoolgirls, young women, and sub-Saharan Africa. In the advanced search databases, the search strategy was built based on the above-mentioned terms using Medical Subject Headings (MeSH)“ and “All fields” by linking “AND” and “OR” Boolean operator terms, as appropriate. The search strategy is reported in Supplementary File 2.

Data extraction and quality assessment

The Endnote citation manager (Version X8, for Windows, Thomson Reuters, and Philadelphia, PA, USA) was used to import the retrieved studies and then duplicates were removed. Two independent (YSA and GAK) reviewers screened all the articles for eligibility criteria. Reviewers began by screening abstracts and titles, followed by full-text screening. The quality of the articles was assessed using the Newcastle-Ottawa Quality Assessment Scale (adapted for cross-sectional studies).¹⁸ Disagreements were resolved by a (TMK) third investigator. The articles were critically appraised by the following criteria from the tool: Representativeness of the sample (1 score maximum), sample size (1 score maximum), non-respondent (1 score maximum), ascertainment of exposure (2 score maximum), comparability of outcome based on study design (2 score maximum), outcome assessment (2 score maximum), and statistical analysis (1 score maximum). All the included studies assessed through the tool with a score of ≥5 were included in this systematic review and meta-analysis. After the quality rating, no study was dismissed as illustrated in the supplementary file (Supplementary File 3). Two investigators used a standardized extraction format prepared in Microsoft Excel. The Excel spreadsheet included the name of the first author and year of publication, country, total sample size, and the uptake of the human papilloma vaccine.

Eligibility criteria (inclusion and exclusion criteria)

All studies conducted in sub-Saharan Africa on the prevalence of HPV vaccine uptake among adolescent school girls were included. Moreover, cross-sectional studies published in English and conducted across all SSA countries on adolescent school girls were included in this systematic review and meta-analysis. Qualitative studies, review papers, case series, case reports, conference proceedings, abstracts, and studies that did not report the outcome of interest are excluded.

Statistical analysis

Data was extracted in Microsoft Excel format and analyzed using STATA software version 16.0 (Stata Corp LLC, Texas, USA). We used forest plots to report the estimated pooled prevalence of each study with their confidence interval (CI) to provide a visual summary of the data. Effect sizes were expressed as a proportion with 95% CI around the summary estimate. The data were first presented using a narrative synthesis of the included studies. A summary table was prepared to describe the characteristics (author, year, country, study design, sample size, uptake of HPV vaccine) of the included studies. We assumed no, low, medium, and high heterogeneity across studies if the I² values were 0%, 25%, 50%, and 75%, respectively. A meta-analysis using a random effects model was performed to analyze the pooled prevalence with 95% confidence intervals (CI) since significant heterogeneity was detected between studies. The heterogeneity of each outcome measure was assessed using both X² and I² statistics to determine dispersion. Meta-regression analysis was performed to investigate the source of heterogeneity. A Funnel plot and Egger’s regression test were conducted to assess publication bias. In addition, sensitivity and subgroup analysis were performed to ensure consistency of the pooled results. Statistical significance was considered at p < .05.

Outcome measurement

The outcome of the current study is the pooled prevalence of HPV vaccine uptake among adolescent school girls in sub-Saharan Africa. The proportion of adolescent girls who had received at least one dose of the HPV vaccine was considered to be the uptake of the HPV vaccine.¹⁵ Moreover, this systematic review and meta-analysis aimed to calculate the pooled effect for associated factors using the odds ratio.

Results

Search results

Initially, a total of 188 articles were identified through searches of different databases. Of the identified studies, 51 were removed due to duplication. Eighty-six studies were excluded after reviewing their abstracts and titles. The full texts of the remaining 51 articles were sought for retrieval, of which 14 were removed and the remaining (n = 37) included full assessment based on the eligibility criteria. We again excluded (n = 21) articles, which are not conducted in sub-Saharan Africa. Finally, the review included 16 studies conducted between 2012 and 2023. (Figure 1) illustrates the process.

Characteristics of the included studies

From a total of 16 studies included in the final analysis, we found that five of the studies were from Nigeria.^19–23 Eight (four each) of the studies were from Ethiopia^24–27 and Uganda,^28–31 while two were from Kenya.^32,33 One study reported was from Cameroon³⁴ (Table 1).

Table 1. Included study characteristics to estimate the pooled prevalence of HPV vaccine uptake and determinant factors in sub-Saharan Africa, 2023.

Authors	Publication year	Country (Region)	Design	Sample Size	Uptake of HPV(%)
Aruho et al.^Citation25	2022	Uganda	CS	250	22
Ayissi et al.^Citation31	2012	Cameroon	CS	553	34.2
Beyen et al.^Citation21	2022	Ethiopia	CS	422	44.4
Bitariho et al.^Citation26	2023	Uganda	CS	524	8.6
Ezeanochie et al.^Citation16	2020	Nigeria	CS	215	1
Kassa et al.^Citation22	2021	Ethiopia	CS	591	66.5
Lakneh et al.^Citation23	2022	Ethiopia	CS	633	45.3
Mabeya et al.^Citation29	2018	Kenya	CS	2994	93.8
Mohammed et al.^Citation18	2019	Nigeria	CS	245	3.7
Nabirye et al^Citation27	2020	Uganda	CS	407	14
Ndikom et al.^Citation19	2017	Nigeria	CS	296	4.1
Odongo et al.^Citation28	2023	Uganda	CS	197	35
Ogunlaja et al.^Citation20	2018	Nigeria	CS	307	6.5
Vermabdere et al.^Citation30	2014	Kenya	CS	254	31.1
Terefe et al.^Citation24	2022	Ethiopia	CS	568	42
Zubairu et al.^Citation17	2022	Nigeria	CS	410	4.4

Overall pooled prevalence estimates of HPV uptake

The Human papilloma vaccine uptake among adolescent girls was identified in 16 studies, from a total of 8866 school girls, 4,470 school girls received the HPV. Based on the random-effects model, the pooled prevalence estimate of HPV uptake among adolescent girls was 28.53% [95% CI: (5.25, 51.81)] as shown in (Figure 2).

Figure 2. Forest plot depicting the pooled prevalence of HPV vaccine uptake among adolescent school girls in sub-Saharan Africa, 2023.

Determinants of HPV uptake among adolescent girls

To identify factors associated with human papillomavirus vaccine uptake among adolescent girls in sub-Saharan Africa, variables such as good knowledge about the HPV vaccine, positive attitude about HPV vaccine, hearing about HPV vaccine, availability of awareness creation about HPV vaccine importance, and parental educational status were extracted from the included studies. Finally, two variables were identified as independent predictors of HPV vaccine uptake among adolescent girls in SSA: good knowledge about the HPV vaccine and positive attitude about HPV vaccine. The pooled odds ratio (OR) was used to estimate the association between these variables and the uptake of the HPV vaccine, and a statistically significant association between the HPV vaccine uptake and predictor variables was declared at two-sided p < .05 with 95% CI.

To start with, the odds of HPV vaccine uptake were 2.98 times (OR = 2.98, 95% CI = 1.51, 5.88) higher in those adolescent girls who had good knowledge about the vaccine than their counterparts (Figure 3).

Figure 3. The pooled odd ratio of the association between good knowledge about HPV vaccine and HPV vaccine uptake among adolescent school girls in sub-Saharan Africa, 2023.

Adolescent girls with a positive attitude were 2.72 times (OR = 2.72, 95% CI = 2.15, 5.88) more likely to receive the HPV vaccine as compared to their counterparts with a negative attitude (Figure 4).

Figure 4. The pooled odd ratio of the association between positive attitude about HPV vaccine and HPV vaccine uptake among adolescent school girls in sub-Saharan Africa, 2023.

Subgroup analysis

We conducted the subgroup analysis of the uptake of HPV among adolescent school girls by country. The subgroup analysis by country revealed the highest uptake of HPV was 62.52% [95% CI: (1.07, 123.96)] which was from Kenya. This was followed by Ethiopia 49.58% [95% CI: (37.87, 61.28)] and Central African countries 4.11% [95% CI: (1.27, 6.95)]. A lower prevalence of 3.77% [95% CI: (1.82, 5.73)] was reported in Nigeria (Figure 5).

Figure 5. Forest plot depicting sub-group analysis by country for the pooled prevalence of HPV vaccine uptake among adolescent school girls in sub-Saharan Africa, 2023.

Meta-regression

Meta-regression was used to identify factors associated with the pooled prevalence of human papilloma vaccine uptake among adolescent schoolgirls. For the meta-regression, publication year and sample size were considered. The analysis revealed a significant correlation between the pooled prevalence of human papillomavirus vaccine uptake among adolescent girls and sample size (p < .001) but no significant correlation with the Publication year (p < .001) (Table 2).

Table 2. Meta-regression to identify the source of heterogeneity for the estimated pooled prevalence of human papilloma vaccine uptake and determinant factors among adolescent school girls in sub-Saharan Africa, 2023.

Uptake of HPV	Coefficient	[95% CI]	p value
Publication Year	0.5430568	−2.711414–3.797528	p = .724
Sample size	0.0294026	0.0137917–0.450134	p < .001

Publication bias assessment

Publication bias was assessed through diagrammatic presentation and statistically tested using Egger’s test. The test showed that there is no evidence of a small study effect or publication bias with a p-value of 0.563. A funnel plot (Figure 6) was constructed from study estimates, with a 95% confidence limit against the standard error of the prevalence. The asymmetry of funnel plot visual inspection showed evidence of publication bias in the pooled prevalence estimate of HPV vaccine uptake.

Figure 6. Funnel plot depicting publication bias of studies reporting on the pooled prevalence of HPV vaccine uptake among adolescent school girls in sub-Saharan Africa, 2023.

Sensitivity analysis

By excluding each study individually, a leave-out-one sensitivity analysis was used to determine the effect of a single study on the pooled prevalence of human papilloma vaccine uptake among adolescent school girls in sub-Saharan Africa. According to our findings, no single study had a significant impact on the pooled prevalence of human papilloma vaccine uptake among adolescent school girls in sub-Saharan Africa (Figure 7).

Figure 7. Sensitivity analysis on the studies included in the pooled prevalence of HPV vaccine uptake among adolescent school girls in sub-Saharan Africa, 2023.

Discussion

Cervical cancer is a major health issue in several sub-Saharan African countries, yet it has not received significant attention. To tackle this problem, increasing access to the HPV vaccine and improving its uptake rate are crucial strategies. This systematic review and meta-analysis present a critical overview of the regional uptake of the HPV vaccine, using data from 16 observational studies involving 4,470 adolescent school girls in sub-Saharan Africa.

The findings of the current review showed an overall pooled estimated HPV vaccine uptake of 28.53% [95% CI: (5.25, 51.81)] among schoolgirl adolescents in sub-Saharan Africa. This is in line with the Tanzanian National Health survey report 49%³⁵ and previous systematic review and meta-analysis in high- and low-income countries, which was 41.5%.³⁶ However, this was lower than studies conducted in Scotland, the USA,^15,36 and Australia,³⁷ where the uptake was 94.4%, 62.8%, and 83%, respectively. The variation in findings could be due to the limited accessibility and availability of the vaccine in SSA countries, as compared to developed countries where all eligible girls have access to HPV vaccination as a routine service. The other possible reasons for the low uptake of the vaccine in sub-Saharan Africa could be the fear of side effects, inadequate awareness, and misconceptions about the HPV vaccine.

In the subgroup analysis, the uptake of the HPV vaccine varied significantly across the subnational region of SSA. Based on this subgroup analysis the highest uptake was from Kenya 62.52% and the lowest was from Nigeria 3.77%. A possible explanation for the difference could be due to Kenya, where the HPV vaccine has been in use since 2006³⁸ which is earlier than most of the SSA countries. Another possible reason might be the implementation of school-based vaccination, and the other possible explanation might be the number of studies included in the analysis in which Kenya was represented by only two studies.

In this systematic review and meta-analysis, we also found that good knowledge about the HPV vaccine and positive attitudes about the HPV vaccine were identified as risk factors of HPV vaccine uptake among adolescent school girls in SSA. To start with, good knowledge about the HPV vaccine was significantly associated with the uptake of the HPV vaccine. The pooled odds of taking the HPV vaccine were approximately three times higher among adolescent girls with good knowledge about the HPV vaccine than adolescent girls with poor knowledge about the vaccine. This finding was congruent with studies from China,³⁹ the USA,⁴⁰ and Brazil.⁴¹ This can be explained to ensure the success of any health intervention, possessing knowledge is of utmost importance. It is crucial to inform adolescents about the benefits of receiving the HPV vaccine, as it would increase their likelihood of getting vaccinated.⁴² Furthermore, participants' behavior is expected to change upon learning about the HPV vaccine and hearing about it triggered them to read and learn more about the vaccine.

A positive attitude about the HPV vaccine was also associated with a higher uptake of the HPV vaccine. This finding is supported by studies conducted from a systematic review and meta-analysis study affirms the current finding.⁴³ This can be attributed to the influence of adolescents’ attitudes on their motivation and initiative to engage in healthy behaviors or maintain a healthy lifestyle, where positive attitudes foster better performance and the implementation of preventive measures. Furthermore, one possible reason for the high uptake of HPV vaccination among adolescents is that their attitudes and beliefs about the effectiveness, safety, and convenience of vaccination play a significant role as immediate causes.²⁴

An effective vaccination program and high vaccination coverage not only protect those vaccinated but also have significant cross-protection and herd effects among boys and older women.¹² To meet disease reduction goals in the population, countries need to review their immunization program objectives, the factors associated with an effective vaccination strategy, and key aspects of field implementation of vaccines.⁴⁴ Policy-level commitments to eliminate cervical cancer have already been made after the launch of the 2030 WHO strategy. Vaccination strategies require committed infrastructure for vaccine delivery and administration, subsidy of the services, and vaccine coverage monitoring and evaluation.⁴⁴ Providing appropriate health education is an intervention to improve field-level HPV vaccine uptake among adolescents, promoting mandatory vaccination policies and financial inducements.⁴⁵ Regarding the method of delivery, class-based instruction in educational settings and multi-component provider interventions, such as an education session, repeated contacts, personalized feedback, and incentives, as well as parent interventions, such as sharing information and educational materials like pamphlets and audio-visual materials, all led to an increase in the uptake of HPV.⁴⁵

The current meta-analysis has several strengths. It provides a comprehensive overview of HPV uptake levels among school-age adolescent girls in sub-Saharan countries and follows the PRISMA guidelines recommended recently. We conducted a rigorous search of the literature using multiple databases and identified eligible studies. Although the meta-analytic techniques used in this study were robust, the findings should be interpreted with caution due to study limitations. Firstly, we observed significant heterogeneity in HPV uptake across countries. However, this heterogeneity may be attributed to factors such as the year of publication and sample size. Furthermore, only six countries were included in the investigation, which limits the representativeness of the results.

Conclusion

Overall, the pooled uptake level of HPV vaccine among sub-Saharan African adolescent schoolgirls is low. Having good knowledge and a positive attitude were found to be risk factors for HPV vaccine uptake. Though the burden of cervical cancer in sub-Saharan Africa is high, the coverage of HPV vaccine is very low, highlighting the need for continued efforts to reduce cervical cancer through HPV vaccine as primary prevention. At the same time, inequalities in the distribution of the HPV vaccine remain significant, with the HPV vaccine uptake generally low in sub-Saharan African countries. It is crucial to vaccinate adolescent school girls through different delivery strategies to increase coverage, as it can have an impact on achieving 2030 SDG goals. Moreover, active campaign to improve the uptake of the HPV vaccine among adolescent school girls in SSA is needed as it can have an impact on achieving 2030 SDG goals.

Authors’ contribution

YSA, TMK, and BLS; conceived and designed the study, methodology, data analysis and interpretation, and writing original draft. KUM, ZAA, HAA, and AHS; established the search strategy, extracted the data, and assessed the quality of included studies. Writing review and editing: TMT, ALL, BFK, BMF, YSA, GAK, and TMK. All the authors read and approved the manuscript.

Acknowledgments

We are indebted to all the researchers whose studies were included in this study.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Data availability statement

All associated data and supporting information are included in this systematic review and meta-analysis.

Supplementary material

Supplemental data for this article can be accessed on the publisher’s website at https://doi.org/10.1080/21645515.2024.2326295

Additional information

Funding

This study did not receive any specific grant from any organization in either the public or commercial sector.