Skip to main content
Advertisement
Browse Subject Areas
?

Click through the PLOS taxonomy to find articles in your field.

For more information about PLOS Subject Areas, click here.

  • Loading metrics

Human Papillomavirus Vaccination uptake and associated factors among schools girls aged between 9–14 years in Ethiopia: Performance Monitoring for Action (PMA-ET) 2023, multilevel analysis

  • Ermias Bekele Enyew ,

    Roles Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Software, Supervision, Validation, Visualization, Writing – original draft, Writing – review & editing

    ermiashi@gmail.com

    Affiliation Department of Health Informatics, School of Public Health, College of Medicine and Health Sciences, Wollo University, Dessie, Ethiopia

  • Mulugeta Desalegn Kasaye,

    Roles Conceptualization, Data curation, Investigation, Supervision, Validation, Writing – review & editing

    Affiliation Department of Health Informatics, School of Public Health, College of Medicine and Health Sciences, Wollo University, Dessie, Ethiopia

  • Shimels Derso Kebede,

    Roles Conceptualization, Investigation, Resources, Software, Validation, Writing – review & editing

    Affiliation Department of Health Informatics, School of Public Health, College of Medicine and Health Sciences, Wollo University, Dessie, Ethiopia

  • Mahider Shimelis Feyisa,

    Roles Investigation, Validation, Visualization, Writing – review & editing

    Affiliation Department of Medical Laboratory, College of Health Science, Debre Tabor University, Debre Tabor, Ethiopia

  • Naol Gonfa Serbessa,

    Roles Conceptualization, Data curation, Investigation, Supervision, Validation, Visualization, Writing – review & editing

    Affiliation Department of Health Informatics, College of Health Science, Mattu University, Mattu, Ethiopia

  • Tsion Mulat Tebeje,

    Roles Conceptualization, Data curation, Investigation, Resources, Supervision, Validation, Visualization, Writing – review & editing

    Affiliation School of Public Health, College of Health Sciences and Medicine, Dilla University, Dilla, Ethiopia

  • Abiyu Abadi Tareke

    Roles Investigation, Methodology, Supervision, Validation, Visualization, Writing – review & editing

    Affiliation Zonal-Level COVAX and Routine Immunization Technical Assistance (TA) at West Gondar zonal health department, Gondar, Ethiopia

Abstract

Background

Human papillomavirus (HPV) is one of the sexually transmitted diseases infections that causes cervical cancer, and it is the second-leading cause of infection-related cancer globally. HPV infection causes around 604,000 cervical cancer cases (342,000 deaths) globally each year. Therefore, this study aimed to assess Human Papillomavirus Vaccination uptake and associated factors among schools girls in Ethiopia.

Method

Performance Monitoring for Action Ethiopia (PMA Ethiopia) is a survey project designed to generate data on various reproductive, maternal, and newborn health (RMNH) indicators that can inform national and regional governments. The prevalence of HPV vaccine uptake with a 95% Confidence Interval (CI) was reported and presented in a forest plot for East Africa Countries using STATA version 14.1. Intra-class Correlation Coefficient (ICC), Likelihood Ratio (LR) test, Median Odds Ratio (MOR), and deviance (−2LLR) values were used for model comparison and fitness. Adjusted Odds Ratios (AOR) with a 95% Confidence Interval (CI) and p-value ≤0.05 in the multilevel logistic model were used to declare significant factors associated with HPV vaccine uptake.

Result

In Ethiopia, the prevalence of HPV vaccine uptake among schools girls was 30.82% (95% CI: 29.21, 32.45). In the multilevel logistic regression model, girls in age groups of 12–14 years were 2.44 [AOR = 2.44, 95% CI: 1.86–3.16] times more likely to take HPV vaccine as compared to girls aged 9–11 years. Similarly, girls who had received any health service and received sexual and reproductive health services had 7.75 [AOR = 7.75, 95% CI: 5.65–10.62], and 3.24 [AOR = 3.24, 95% CI: 2.33–4.51] were more likely to take HPV vaccine compared to their counterparts respectively.

Conclusion

The study findings indicate that the proportion of girls reporting receipt of the HPV vaccine in this nationally representative survey is an alarmingly low 30.8%. The following critical factors have influenced this rate: age, access to sexual and reproductive health services, general health service utilization, and regional health disparity.

Background

Human papillomavirus (HPV) is one of the sexually transmitted diseases infection that causes cervical cancer, and it is the second-leading cause of infection-related cancer globally [1,2]. There are numerous genotypes of HPV. HPV types 6 and 11 are responsible for 90% of genital warts, but HPV types 16 and 18 are classified as high-risk viruses, accounting for 70% of cervical cancer [3]. Persistent HPV infections with strains 16 and 18 cause 70% of cervical cancers and precancerous lesions [4]. Globally, HPV infection causes about 604,000 cases of cervical cancer annually, which leads to about 342,000 deaths. A significant amount of this burden falls on countries with low or middle incomes, where 90% of cases and 90% of deaths [5].

The frequency of cervical HPV infection varies around the world, but African women experience some of the highest rate [6]. Cervical cancer, caused by human papillomavirus (HPV), is the leading cause of cancer mortality among women in Sub-Saharan Africa (SSA) [7]. The estimated HPV prevalence in Sub-Saharan Africa is 24.4% [8]. A study conducted in Kenya revealed that HPV prevalence was high (42.3%), with approximately 46% of HPV-positive women carrying multiple kinds of infections. Another study conducted in Rwanda showed that HPV prevalence was 34%, being highest (54%) in women ≤19 years and decreasing to 20% at age ≥50 [9]. In a study done in some West African countries, the prevalence of HPV vaccine among women was 13.4% in Gambia [10], 33.2% in Benin [11], and 10.6 in Togo [12]. A small study in Gambella, Ethiopia, found that 48% of adolescent girls had received the HPV vaccine [13]. Similarly, in a study conducted in Bahirdar City among female preparatory school students, the proportion of human papillomavirus (HPV) vaccine uptake was 45.3% [14].

As of 2020, more than half of the WHO member countries have introduced HPV vaccination programs to meet the 2030 Sustainable Development Goal (SDG) elimination target of 90% [15]. The 2022 WHO position paper on HPV vaccinations urged that they be included in standard national immunization programs as a public health priority, including the goals related to immunization and their contribution to Primary Health Care (PHC) and Universal Health Coverage (UHC) [16,17]. Many countries, including Australia, the United Kingdom, and Canada, have developed public health programs for HPV vaccination, with school-based programs achieving high coverage in the target populations [1820]. However, many sub-Saharan African countries that had been delayed in HPV vaccine introduction still have low coverage [21].

In the world poorest countries, where pre-screening and treatment are few, patients seek medical attention after a complication develops, and the majority lack a variety of prevention programs or services that primarily affect young, uneducated women [7]. Uptake of the HPV vaccine is known to be influenced by a number of factors, including the education level of girls, the household wealth index [14], household family size [22], the marital status of the mother [19], girls received any health service, girls received sexual and reproductive health service, girls mobile ownership [23], and girls working status [24].

In Ethiopia, the projected number of cervical cancer cases and deaths in 2018 is 6294 and 4884, respectively [23]. In the country, cervical cancer is the second highest cause of female cancer in women aged 15–44 years [25]. Ethiopia has around 29 million women aged 15 and older who are at risk of having cervical cancer [26]. Even though 20 million Ethiopian women were eligible for cervical screening, less than 1% were screened [27]. Vaccinating primary school-age girls is the most cost-effective public health intervention against cervical cancer since the vaccination targets girls who have not made their sexual debut [28].

According to the Ethiopian Ministry of Health (MoH), girls between the ages of 9 and 14 should receive the HPV vaccine before they start having sex and are exposed to the virus that can induce cervical alterations that can result in cancer [29]. The HPV vaccine was made available to 14-year-old females in Ethiopia in December 2018. However, because of a worldwide scarcity of HPV vaccines, the nation is only launching the vaccination in one age group (girls aged 14) in the first year. Depending on the vaccines availability worldwide, it plans to roll out the introduction to other age groups in the second year and beyond [30]. HPV vaccination is more challenging than other health campaigns because the targets are 9-to 14-year-old girls, decisions are typically made by their parents, and the information may not be credible [31]. Though Ethiopia has set guidelines to reach global standards, the life-course approach to cervical cancer prevention is in its early stages [32]. The WHO Strategic Advisory Group of Experts on Immunization (SAGE) has recommended that Ethiopia switch to a single-dose HPV vaccination in August 2023 because of the programmatic benefits and similar protection duration and efficacy to the two-dose schedule [33]. Despite the global immunization drive to prevent HPV-related morbidity, HPV vaccination uptake remains low in Ethiopia. Therefore, an evidence-based study on the HPV vaccine and associated factors is a cornerstone for tracking the progress of the program to eliminate diseases caused by HPV and achieve the stated goal. Thus, this research aimed to assess Human Papillomavirus Vaccination uptake and associated factors among school girls in Ethiopia.

Method and materials

Study design and study period

The study represents secondary data from the Performance Monitoring for Action Ethiopia survey. Performance Monitoring for Action Ethiopia (PMA Ethiopia) is a survey project designed to generate data on various reproductive, maternal, and newborn health (RMNH) indicators that can inform national and regional governments. The project conducted cross-sectional and cohort surveys to fill a data gap, collecting information not currently measured by other large-scale surveys. Its focus is measuring the comprehensiveness of RMNH care services and the barriers and facilitators to such care. The period of this cross-sectional study was November 2023 – January 2024 [34].

Study area

Ethiopia was the site of the investigation. Ethiopia is situated in the Horn of Africa. It consists of two city administrative areas (Addis Ababa and Dire-Dawa) and twelve regional states (Tigray, Afar, Amhara, Oromia, Somali, Benishangul-Gumuz, Southern Nations, Nationalities, and People’s Region (SNNP), Gambella, Harari, Sidama, Southwest Ethiopia, and Central Ethiopia.

Study population

All Ethiopian girls in the age range [914] included in the survey comprised the study population.

Sampling technique and Sample size

The two-stage cluster design employed in the PMAET 2023 survey included regions and urban-rural areas as strata. A total of 280 Enumeration Areas (EAs) were chosen at random from the master sample frame, and 35 households were chosen from each EA. All women aged 15–49 in the selected households are eligible for the cross-sectional survey [34]. From among 6712 included in the broader survey, a total of 2963 girls met the inclusion criteria and had complete responses.

Variable of study

Outcome variable.

The outcome variable was “Has received HPV vaccination?” This binary response variable indicated the uptake of the HPV vaccine. Girls who had received the HPV vaccination were categorized as having an uptake, coded as 1. While those who had not received the vaccine were coded as 0, indicating “not uptake HPV vaccinated.”

Independent variable.

Individual-level factors: respondents’ age (categorized as 9–11 and 13–14 years), girls’ education status, Household wealth index, household family size, maternal marital status, girls’ receipt of any health service, girls’ receipt of sexual and reproductive health service, girls’ mobile ownership, and girls’ working status were included as individual-level factors.

Community-level factors: a place of residency (rural, urban), community-level girl received any health service (low level, and high level), community-level girls received sexual and reproductive health service (low and high level), and regions were included under community-level factors.

Operational definition

Community level received any health service: Number of girls who had received any health service. High levels of any health service received were defined as those who fall at or above the median value of the variables. Low levels of any health service received were defined as those that fall below the median value of the variables. Since the normalcy test of community-level poverty was skewed (the Jarque-Bera test’s p-value was less than 0.05, indicating a skewed distribution), the median was utilized as the cutpoint.

Community-level sexual and reproductive health services received a percentage of girls who had received sexual and reproductive health services. We classified this community-level factor in a manner comparable to that of any health service received.

Data collection procedure

Three separate research activities comprise PMA-Ethiopia, a five-year (2019–2023) project executed in collaboration with Addis Ababa University, Johns Hopkins University, and the Federal Ministry of Health. These include yearly cross-sectional surveys of women aged 15–49, longitudinal surveys of women who are pregnant or have recently given birth, and annual service delivery point surveys of health facilities [34]. The Johns Hopkins School of Public Health received an online application through https://www.pmadata.org/data/available-datasets/request-accessdatasets, which was utilized to retrieve the PMA-Ethiopia datasets.

Data management and analysis

Data were edited, coded, cleaned, and analyzed using STATA software version 14. STATA software was developed by the Computing Resource Center in California, and the first version was released in 1985 [35]. Descriptive statistics were employed using frequencies and percentages. The prevalence of HPV vaccine uptake with a 95% Confidence Interval (CI) was reported and presented in a forest plot for the Ethiopia region.

Multilevel analysis

The PMA-ET data exhibits a hierarchical structure, where girls are nested within households, and households are further nested within clusters. This nesting can lead to intra-cluster correlation, meaning that girls within the same cluster may be more similar to one another than to those in different clusters. Consequently, using standard statistical models may underestimate the standard errors of effect sizes, which can distort the assessment of the null hypothesis and increase the risk of Type I errors. It suggests that advanced models have to be used to account for between-cluster variability. Therefore, the outcome variable was binary. In the multilevel logistic regression model, we ran four models to estimate both fixed effects of the individual and community-level factors and random intercept of between-cluster variation. The first null or unconditional model contained no predictor variable used to decompose the amount of variance between cluster levels. The second model consisted of only individual-level factors, whereas the third model had only community-level variables. The final model controlled both individual and community factors (full model).

Intra-class correlation coefficient (ICC) and median odds ratio (MOR)

The Intra-Class Correlation (ICC) was used to express the random effects, or the amount of community variation, which are measures of variation in HPV vaccine uptake among communities or clusters. To determine whether there was variability or a clustering effect, the median odds ratio (MOR) was provided. When two clusters or EAs are randomly selected, it is defined as the median value of the odds ratio between the cluster with high odds of girls’ HPV vaccine uptake and the cluster with lower odds of girls’ HPV vaccine uptake [36].

The Likelihood Ratio (LR) test and deviance (−2LLR) values were utilized to evaluate model comparison and fitness since the models were nested [37]. Accordingly, a mixed-effect logistic regression model (fixed and random effect) was selected as the best-fitted model since it had the highest LLR and lowest deviance value, Akaike’s information criterion (AIC), and Bayesian information criterion (BIC). Variables with p-value < 0.2 in the bi-variable analysis were considered in the multivariable logistic regression model. Adjusted Odds Ratios (AOR) with a 95% Confidence Interval (CI) and p-value <0.05 in the multilevel logistic model were used to declare significant factors associated with HPV vaccine uptake.

Ethics approval and consent to participate

There is no information gathering from subjects in this study. This specific study did not require participant permission or ethical approval. Given that, PMA-Ethiopia records provide the basis for the study’s secondary data analysis. The Johns Hopkins University Bloomberg School of Public Health (JHSPH) Institutional Review Board and Addis Ababa University College of Health Sciences (AAU/CHS) have granted ethical approval to PMA Ethiopia. Institutional Review Board and Addis Ababa University College of Health Sciences (AAU/CHS) approved the verbal consent. Written consent is not necessary when data collection involves non-invasive methods (such as collecting biospecimens) or in low-literacy areas, according to this guidance and the IRB’s records. Institutional review boards at JHBSPH and AAU approved the methods used for data collection [34]. We confirm all methods were carried out according to the relevant guidelines and regulations. The authors do not have access to any information related to personal identifiers during the data collection process.

Results

Socio-demographics characteristics of the respondents

A total of 2,963 people participated in the study. Most of the females were in the 12- to 14-year-old age range. In regards to residency and educational attainment, 2,565 (86.6%) were enrolled in primary school, while 2,216 (74.8%) lived in rural areas. The percentage of girls who had not received sexual and reproductive services was about 20%, while 1,215 (51.8%) had received any health services. (Table 1).

thumbnail
Table 1. Sociodemographic characteristics of the respondents, PMA-ET, 2023 (n = 2,963).

https://doi.org/10.1371/journal.pone.0325557.t001

Prevalence of HPV uptake in Ethiopia

In Ethiopia, the prevalence of HPV vaccine uptake was 30.82% (95% CI: 29.21, 32.45). There were regional differences: HPV vaccine uptake was most common in the Afar, Benishangul-Gumuz, southwest Ethiopia, central Ethiopia, and SNNP regions, while it was least prevalent in Addis Ababa and the Dire Dawa administrative zone of Ethiopia. (Fig 1). In a forest plot, the box shapes around each data point represent the effect estimates for each region.

thumbnail
Fig 1. Prevalence of HPV vaccine uptake among girls by administrative region in Ethiopia, PMA-ET 2023.

https://doi.org/10.1371/journal.pone.0325557.g001

Multilevel logistic regression analysis

Factors associated with Human Papillomavirus Vaccination uptake in Ethiopia.

Multivariable multilevel logistic regression analysis revealed that, at the individual level, older age and having received any health service or sexual and reproductive health service and, at the community level, these factors included living in Afar, Somali, SNNP, and South-West Ethiopia were positively associated with vaccine uptake. The analysis supporting these findings is detailed below. Table 2 shows the random effect model. In model I, the ICC indicated that 41.3% of the total variability for HPV vaccine uptake was due to differences between clusters while the remaining unexplained 58.7% of the total variability of HPV vaccine uptake was attributable to individual differences. Additionally, the model I MOR of 3.92 (95% CI: 3.34, 4.60) showed that there was a difference in the uptake of the HPV vaccine between clusters. If we randomly selected two girls from different groups, the girls from the high cluster would be 3.92 times more likely to have HPV vaccine uptake than girls from the low cluster. The proportional change in variance (PCV) in this model was 56.3%, which showed that both community and individual-level variables explained 56.3% of community variance observed in the final model. The multilevel logistic regression model IV was the best-fitted model because it had the lowest values of AIC and BIC, the highest Log-likelihood Ratio (LLR), and the lowest deviation since the models were nested in the random effect.

thumbnail
Table 2. Model comparison and model fitness for multilevel logistic regression analysis.

https://doi.org/10.1371/journal.pone.0325557.t002

The fixed effects analysis result

In the multivariable mixed effect (individual and community-level factors) binary logistic regression analysis, age, girls who had received sexual and reproductive health services, and any health services, region were significant determinants of HPV vaccine uptake in Ethiopia. (Table 3).

thumbnail
Table 3. Multivariable multilevel logistic regression analysis of individual and community-level factors associated with HPV vaccination uptake.

https://doi.org/10.1371/journal.pone.0325557.t003

In this study, girls in age groups of 12–14 years were 2.44 [AOR = 2.44, 95% CI: 1.86–3.16] times more likely to take the HPV vaccine as compared to girls aged 9–11 years. Similarly, girls who had received any health service and received sexual and reproductive health services had 7.75 times [AOR = 7.75, 95% CI: 5.65–10.62], and 3.24 [AOR = 3.24, 95% CI: 2.33–4.51] were more likely to take HPV vaccine compared to their counterparts respectively.

The finding revealed that community-level factors were significantly associated with HPV vaccine uptake. Girls in Afar, Somali, SNNP, and South-west Ethiopia had 2.34 times [AOR = 2.34, 95% CI: 1.98–4.47], 2.94 [AOR = 2.94, 95% CI: 1.93–4.20], 4.02 [AOR = 4.02, 95% CI: 1.72–9.39], and 3.46 times [AOR = 3.46, 95% CI: 1.69–8.72] were higher the odd of HPV vaccine uptake compared to girls in Tigray, respectively. (Table 3).

Discussion

This study aimed to assess the prevalence of HPV vaccine uptake among girls aged between 9–14 years in Ethiopia based on the most recent PMA data. Ethiopia’s ambitious goal to vaccinate over 7 million girls against the human papillomavirus (HPV) is crucial in the fight against cervical cancer, which poses a significant health risk to women in the country. As of April 2024, more than 6.3 million girls have received at least one dose of the vaccine, reflecting considerable progress in vaccination efforts [29]. The study reported a prevalence of HPV vaccine uptake at 30.8%, highlighting a significant discrepancy compared to the 89.9% two-dose coverage rate recorded in 2023 [38]. The observed variation in vaccination rates following the recent introduction of the HPV vaccination program in Ethiopia may be a lack of knowledge about one’s own risk of developing cervical cancer [39].

Similarly, this finding is lower than a study done in Ethiopia, the uptake of HPV vaccination among female students in Gambella Town (48.0%) [13], and Nekemte City (61.2%) [23], 44.4% in Ambo [40], 66.5% in Minjar Shenkora in North Shoa [28], 50.4% in Arba Minch [41] and 45.3% in Bahir Dar City [14]. A possible explanation might be the difference in the study setting. Adolescents who visited the school were recruited for earlier studies at the facility. These groups typically have greater access to health information and immunization information [42].

In addition, the finding is lower than a study done in Brazil [43], in Uganda (44.6%) [44], in Kibaha Town Council (47.92%) [45]. This disparity could be due to several factors, including differences in socioeconomic level between nations, access to the HPV vaccine, commitment to expansion, and knowledge of the vaccine [46]. Furthermore, disparities may arise from sociocultural barriers to healthcare services, particularly adolescent healthcare services in developing nations [40].

In the multivariable mixed-effect binary logistic regression analysis, age, girls who had received sexual and reproductive health services, and any health services and region were significant determinants of HPV vaccine uptake in Ethiopia. Adolescent girls’ adoption of the Human Papillomavirus (HPV) vaccine is essential for preventing cervical cancer, especially for those between the ages of 9 and 14. The human papillomavirus (HPV) vaccination campaign in Ethiopia aims to reduce the prevalence of 9–14-year-old girls who get cervical cancer when it typically presents at an older age period than this. This finding revealed that girls’ age had a significant effect on HPV vaccine uptake. Girls aged 12–14 had higher odds of taking the HPV vaccine compared to those aged 9–11. This finding is supported by a study conducted in Uganda [22,47], Indonesian [48], Nigeria [49], a prior study done in Nekemte City, Western Ethiopia [23], and a similar finding conducted in Wolida, Northeast, Ethiopia [39]. The possible reason might be a positive association between vaccine uptake and receipt of other services highlighting the importance of linking HPV vaccination to other adolescent healthcare service delivery [50]. Furthermore, as children get closer to the age of sexual debut, parents may feel more pressure to protect them from HPV-related infections, which could further influence vaccine decisions [51].

This finding revealed that girls who had received sexual and reproductive health were strongly positively associated with HPV vaccine uptake. This finding is supported by the study conducted elsewhere [23,52,53]. Similarly, this study revealed that the uptake of any health services was significantly associated with HPV vaccine uptake. This finding is collaborated by studies conducted in Uganda [22], in South Asia [54], in Germany [55], and in Mettu Town, Ethiopia [24]. Students’ decision to receive the vaccination may influenced by their belief that doctors are reliable sources of health information. Additionally, the availability of awareness-raising activities at their school (even if they are sporadic or brief) helps them learn more about the advantages of the vaccine, which in turn encourages them to receive it [40]. Moreover, there is a statistically significant relationship between the HPV vaccine uptake and the residential area. Compared to girls in the Tigray region, girls in Southwest Ethiopia, Somalia, SNNP, and Afar were more likely to receive the HPV vaccine. A potential reason could be that those areas share comparable cultures, religions, and customs.

Strength and limitation

The use of large sample sizes and nationally representative data is the main strength of this study. A causal association cannot be established using PMA data, just like other cross-sectional data. As a result, these restrictions must be considered when analyzing or interpreting findings from this research.

Conclusions

The study findings indicate that the proportion of girls reporting receipt of the HPV vaccine in this nationally representative survey is an alarmingly low 30.8%. In multilevel logistic regression results, age, access to sexual and reproductive health services, general health service utilization, and regional health disparity were significant associated factors with HPV vaccine uptake. These results highlight the critical need for focused public health initiatives that can raise immunization rates. Raising awareness, facilitating access, and assuring the quality of healthcare services should be the main goals to enhance HPV vaccination coverage, particularly in low-uptake areas.

Acknowledgments

We greatly acknowledge the Performance Monitoring for Action (PMA) project Data for granting access to the PMA-Ethiopia dataset. We want to thank all who directly or indirectly supported us.

References

  1. 1. Dorji T, Nopsopon T, Tamang ST, Pongpirul K. Human papillomavirus vaccination uptake in low-and middle-income countries: a meta-analysis. EClinicalMedicine. 2021;34:100836. pmid:33997733
  2. 2. de Martel C, Georges D, Bray F, Ferlay J, Clifford GM. Global burden of cancer attributable to infections in 2018: a worldwide incidence analysis. Lancet Glob Health. 2020;8(2):e180–90. pmid:31862245
  3. 3. Loke AY, Kwan ML, Wong Y-T, Wong AKY. The uptake of human papillomavirus vaccination and its associated factors among adolescents: a systematic review. J Prim Care Community Health. 2017;8(4):349–62. pmid:29161946
  4. 4. Riesen M, Konstantinoudis G, Lang P, Low N, Hatz C, Maeusezahl M, et al. Exploring variation in human papillomavirus vaccination uptake in Switzerland: a multilevel spatial analysis of a national vaccination coverage survey. BMJ Open. 2018;8(5):e021006. pmid:29773702
  5. 5. Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, et al. Global Cancer Statistics 2020: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries. CA Cancer J Clin. 2021;71(3):209–49. pmid:33538338
  6. 6. Onwuamah CK, Feng N, Momoh AE, Uwandu M, Ahmed RA, Idigbe I, et al. Prevalence and risk factors for high-risk human papillomavirus infection among women from three southern geopolitical zones of Nigeria. Front Oncol. 2023;13:1254304. pmid:37876969
  7. 7. Sankaranarayanan R, Anorlu R, Sangwa-Lugoma G, Denny LA. Infrastructure requirements for human papillomavirus vaccination and cervical cancer screening in sub-Saharan Africa. Vaccine. 2013;31 Suppl 5:F47–52. pmid:24331747
  8. 8. Tesfaye E, Kumbi B, Mandefro B, Hemba Y, Prajapati KK, Singh SC, et al. Prevalence of human papillomavirus infection and associated factors among women attending cervical cancer screening in setting of Addis Ababa, Ethiopia. Sci Rep. 2024;14(1):4053. pmid:38374354
  9. 9. Ngabo F, Franceschi S, Baussano I, Umulisa MC, Snijders PJ, Uyterlinde AM. Human papillomavirus infection in Rwanda at the moment of implementation of a national HPV vaccination programme. BMC Infectious Diseases. 2016;16:1–10.
  10. 10. Wall SR, Scherf CF, Morison L, Hart KW, West B, Ekpo G, et al. Cervical human papillomavirus infection and squamous intraepithelial lesions in rural Gambia, West Africa: viral sequence analysis and epidemiology. Br J Cancer. 2005;93(9):1068–76. pmid:16106268
  11. 11. Piras F, Piga M, De Montis A, Zannou ARF, Minerba L, Perra MT, et al. Prevalence of human papillomavirus infection in women in Benin, West Africa. Virol J. 2011;8:514. pmid:22074103
  12. 12. Ferré VM, Ekouevi DK, Gbeasor-Komlanvi FA, Collin G, Le Hingrat Q, Tchounga B, et al. Prevalence of human papillomavirus, human immunodeficiency virus and other sexually transmitted infections among female sex workers in Togo: a national cross-sectional survey. Clin Microbiol Infect. 2019;25(12):1560.e1–1560.e7. pmid:31051265
  13. 13. Woldehawaryat EG, Geremew AB, Asmamaw DB. Uptake of human papillomavirus vaccination and its associated factors among adolescents in Gambella town, Southwest, Ethiopia: a community-based cross-sectional study. BMJ Open. 2023;13(9):e068441. pmid:37669848
  14. 14. Lakneh EA, Mersha EA, Asresie MB, Belay HG. Knowledge, attitude, and uptake of human papilloma virus vaccine and associated factors among female preparatory school students in Bahir Dar City, Amhara Region, Ethiopia. PLoS One. 2022;17(11):e0276465.
  15. 15. Bruni L, Saura-Lázaro A, Montoliu A, Brotons M, Alemany L, Diallo MS, et al. HPV vaccination introduction worldwide and WHO and UNICEF estimates of national HPV immunization coverage 2010-2019. Prev Med. 2021;144:106399. pmid:33388322
  16. 16. World Health Organization. Immunization, Vaccines and Biologicals 2/4/2025 [cited 2025 03/10/2025]. Available from: https://www.who.int/teams/immunization-vaccines-and-biologicals/diseases/human-papillomavirus-vaccines-(HPV)/hpv-clearing-house/hpv-dashboard
  17. 17. mondiale de la Santé O, Organization WH. Human papillomavirus vaccines: WHO position paper (2022 update)–Vaccins contre les papillomavirus humains: note de synthèse de l’OMS (mise à jour de 2022). 2022.
  18. 18. Vujovich-Dunn C, Wand H, Brotherton JML, Gidding H, Sisnowski J, Lorch R, et al. Measuring school level attributable risk to support school-based HPV vaccination programs. BMC Public Health. 2022;22(1):822. pmid:35468743
  19. 19. Ebrahimi N, Yousefi Z, Khosravi G, Malayeri FE, Golabi M, Askarzadeh M. Human papillomavirus vaccination in low-and middle-income countries: progression, barriers, and future prospective. Front Immunol. 2023;14:1150238.
  20. 20. Bruni L, Diaz M, Barrionuevo-Rosas L, Herrero R, Bray F, Bosch FX, et al. Global estimates of human papillomavirus vaccination coverage by region and income level: a pooled analysis. Lancet Glob Health. 2016;4(7):e453–63. pmid:27340003
  21. 21. Perlman S, Wamai RG, Bain PA, Welty T, Welty E, Ogembo JG. Knowledge and awareness of HPV vaccine and acceptability to vaccinate in sub-Saharan Africa: a systematic review. PLoS One. 2014;9(3):e90912. pmid:24618636
  22. 22. Nakayita RM, Benyumiza D, Nekesa C, Misuk I, Kyeswa J, Nalubuuka A, et al. Factors associated with uptake of human papilloma virus vaccine among school girls aged 9-14 years in Lira City northern Uganda: a cross-sectional study. BMC Womens Health. 2023;23(1):362. pmid:37420225
  23. 23. Hailu G, Wirtu D, Tesfaye T, Getachew M. Human papillomavirus vaccine uptake and associated factors among adolescent girls in high schools of Nekemte city, Western Ethiopia, 2020. BMC Womens Health. 2023;23(1):560. pmid:37898731
  24. 24. Dawud A, Kera AM, Bekele D, Hiko D, Zewdie A. Factors associated with uptake of human papillomavirus vaccination among adolescent girls in Mettu town, southwest Ethiopia: a school-based cross-sectional study. BMJ Open. 2023;13(11):e071878. pmid:37996240
  25. 25. Temesgen MM, Alemu T, Shiferaw B, Legesse S, Zeru T, Haile M, et al. Prevalence of oncogenic human papillomavirus (HPV 16/18) infection, cervical lesions and its associated factors among women aged 21-49 years in Amhara region, Northern Ethiopia. PLoS One. 2021;16(3):e0248949. pmid:33760866
  26. 26. Derbie A, Mekonnen D, Yismaw G, Biadglegne F, Van Ostade X, Abebe T. Human papillomavirus in Ethiopia. Virusdisease. 2019;30(2):171–9. pmid:31179353
  27. 27. Mihretie GN, Liyeh TM, Ayele AD, Belay HG, Yimer TS, Miskr AD, et al. Female adolescents’ knowledge and acceptability of human papillomavirus vaccine in Debre Tabor Town, Ethiopia: a cross-sectional study. BMJ Open. 2023;13(3):e061813. pmid:36948550
  28. 28. Kassa HN, Bilchut AH, Mekuria AD, Lewetie EM. Practice and associated factors of human papillomavirus vaccination among primary school students in Minjar-Shenkora district, North Shoa Zone, Amhara Regional State, Ethiopia, 2020. Cancer Manag Res. 2021;6999–7008.
  29. 29. World Health Organization. Human papillomavirus vaccination in Ethiopia protects over 6.3 million girls from cervical cancer 2024 [cited 2024]. Available from: https://www.afro.who.int/countries/ethiopia/news/human-papillomavirus-vaccination-ethiopia-protects-over-63-million-girls-cervical-cancer
  30. 30. World Health Organization. Ethiopia launches Human Papillomavirus Vaccine for 14 year old girls 2018 [cited 2024]. Available from: https://www.afro.who.int/news/ethiopia-launches-human-papillomavirus-vaccine-14-year-old-girls
  31. 31. Muthukrishnan M, Loux T, Shacham E, Tiro JA, Arnold LD. Barriers to human papillomavirus (HPV) vaccination among young adults, aged 18–35. Preventive Med Rep. 2022;29:101942.
  32. 32. Derbie A, Mekonnen D, Misgan E, Maier M, Woldeamanuel Y, Abebe T. Acceptance of human papillomavirus vaccination and parents’ willingness to vaccinate their adolescents in Ethiopia: a systematic review and meta-analysis. Infect Agent Cancer. 2023;18(1):59. pmid:37821992
  33. 33. mondiale de la Santé O OWH. Human papillomavirus vaccines: WHO position paper (2022 update)–Vaccins contre les papillomavirus humains: note de synthèse de l’OMS (mise à jour de 2022). Weekly Epidemiological Record. 2022;97(50):645–72.
  34. 34. Health. AAUSoPHatWHGSIfPaRHatJHBSoP. Performance Monitoring for Action Ethiopia (PMA-ET) 2023 Cross-sectional Household and Female Survey (Version 2.0), PMAET-2023CS-HQFQ. 2023 2024 [cited 2024 10/25/2024]. Available from: https://datalab.pmadata.org/dataset/doi%3A1034976k8hq-b666
  35. 35. Cox NJ. A brief history of Stata on its 20th anniversary. The Stata Journal. 2005;5(1):2–18.
  36. 36. Larsen K, Merlo J. Appropriate assessment of neighborhood effects on individual health: integrating random and fixed effects in multilevel logistic regression. Am J Epidemiol. 2005;161(1):81–8. pmid:15615918
  37. 37. Snijders TA, Bosker RJ. Multilevel analysis: an introduction to basic and advanced multilevel modeling. Sage; 2011.
  38. 38. website WHO. Human papillomavirus (HPV) vaccination coverage page [filtered for Ethiopia, HPV female, final, 2021–2023] 2023 [cited 2024 1/14/2025]. Available from: https://immunizationdata.who.int/global/wiise-detail-page/human-papillomavirus-(hpv)-vaccination-coverage?CODE=ETH&ANTIGEN=HPV_FEM&YEAR=
  39. 39. Bittew SM, Masresha SA, Mulaw GF, Yimam MA, Zimamu AA, Abriham AA, et al. Parental willingness to vaccinate their daughters against human papilloma virus and its associated factors in Woldia town, Northeast Ethiopia. Front Glob Womens Health. 2024;5:1243280. pmid:39049935
  40. 40. Beyen MW, Bulto GA, Chaka EE, Debelo BT, Roga EY, Wakgari N, et al. Human papillomavirus vaccination uptake and its associated factors among adolescent school girls in Ambo town, Oromia region, Ethiopia, 2020. PLoS One. 2022;17(7):e0271237. pmid:35830389
  41. 41. Ukumo EY, Weldehawariat FG, Dessalegn SA, Minamo DM, Weldehawaryat HN. Acceptance of Human Papillomavirus Vaccination and Associated Factors among Girls in Arba Minch Town, Southern Ethiopia, 2020. Infect Dis Obstet Gynecol. 2022;2022:7303801. pmid:36531338
  42. 42. Ukumo EY, Woldehawariat FG, Dessalegn SA, Minamo DM, Ukke GG. Assessment of Knowledge About Human Papillomavirus Vaccination Among Primary School Girls in Arba Minch Town, South Ethiopia, 2020 an Institution-Based Cross-Sectional Study. Cancer Manag Res. 2022;14:2205–14. pmid:35880169
  43. 43. Silva IdAG, Sá ACMGNd, Prates EJS, Malta DC, Matozinhos FP, Silva TMRd. Vaccination against human papillomavirus in Brazilian schoolchildren: National Survey of School Health, 2019. Revista Latino-Americana de Enfermagem. 2022;30:e3834.
  44. 44. Nakendo A, Busingye R, Kakaire O. Prevalence and factors associated with uptake of the second dose of the human papilloma virus vaccine among adolescent girls in Kawempe Division, Kampala. 2022.
  45. 45. Ngailo N, Mushi L. Determinants of human papilloma virus vaccine uptake among adolescent girls at selected secondary schools in Kibaha Town Council. 2024.
  46. 46. Agimas MC, Adugna DG, Derseh NM, Kassaw A, Kassie YT, Abate HK, et al. Uptake of human papilloma virus vaccine and its determinants among females in East Africa: a systematic review and meta-analysis. BMC Public Health. 2024;24(1):842. pmid:38500046
  47. 47. Nakibuuka V, Muddu M, Kraehenbuhl JP, Birungi C, Semitala FC, Tusubira AK. Uptake of human papilloma virus vaccination among adolescent girls living with HIV in Uganda: A mixed methods study. PLoS One. 2024;19(8):e0300155. pmid:39116172
  48. 48. Lismidiati W, Hasyim AVF, Parmawati I, Wicaksana AL. Self-Efficacy to Obtain Human Papillomavirus Vaccination among Indonesian Adolescent Girls. Asian Pac J Cancer Prev. 2022;23(3):789–94. pmid:35345348
  49. 49. Ogochukwu T, Akabueze J, Ezeome I, Aniebue U, Oranu E. Vaccination against human papilloma virus in adolescent girls: mother’s knowledge, attitude, desire and practice in Nigeria. J Infect Dis Preve Med. 2017;5(151):2.
  50. 50. St Sauver JL, Rutten LJF, Ebbert JO, Jacobson DJ, McGree ME, Jacobson RM. Younger age at initiation of the human papillomavirus (HPV) vaccination series is associated with higher rates of on-time completion. Prev Med. 2016;89:327–33. pmid:26930513
  51. 51. Ellingson MK, Sheikha H, Nyhan K, Oliveira CR, Niccolai LM. Human papillomavirus vaccine effectiveness by age at vaccination: a systematic review. Hum Vaccin Immunother. 2023;19(2):2239085. pmid:37529935
  52. 52. Narasimhan M, Pedersen H, Ogilvie G, Vermund SH. The case for integrated human papillomavirus vaccine and HIV prevention with broader sexual and reproductive health and rights services for adolescent girls and young women. Oxford University Press; 2017. p. 141–3.
  53. 53. Real W, Alvarado V. Vacunación contra virus papiloma humano: una experiencia chilena en atención primaria. Revista chilena de infectología. 2012;29(6):686.
  54. 54. Chaudhary K, Rai G, Karn BK. Health literacy on human papillomavirus, its vaccination and risk factor of cervical cancer among adolescent girls. South Asian Res J Nurs Health Care. 2022;4(4):63–71.
  55. 55. Poethko-Müller C, Buttmann-Schweiger N, Takla A. Human papillomavirus (HPV) vaccination of girls in Germany. Results of the cross-sectional KiGGS Wave 2 study and trends. J Health Monit. 2018;3(4):79–86. pmid:35586146