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Prevalence and determinants of precancerous cervical lesions among women screened for cervical cancer in Africa: A systematic review and meta-analysis

  • Berihun Agegn Mengistie ,

    Roles Conceptualization, Data curation, Formal analysis, Methodology, Software, Validation, Writing – review & editing

    berihunagegn21@gmail.com

    Affiliation Department of General Midwifery, School of Midwifery, College of Medicine and Health Sciences, University of Gondar, Gondar, Ethiopia

  • Getie Mihret Aragaw,

    Roles Formal analysis, Methodology, Software, Validation, Visualization, Writing – original draft, Writing – review & editing

    Affiliation Department of General Midwifery, School of Midwifery, College of Medicine and Health Sciences, University of Gondar, Gondar, Ethiopia

  • Tazeb Alemu Anteneh,

    Roles Data curation, Writing – review & editing

    Affiliation Department of Clinical Midwifery, School of Midwifery, College of Medicine and Health Sciences, University of Gondar, Gondar, Ethiopia

  • Kindu Yinges Wondie,

    Roles Data curation, Writing – original draft, Writing – review & editing

    Affiliation Department of Clinical Midwifery, School of Midwifery, College of Medicine and Health Sciences, University of Gondar, Gondar, Ethiopia

  • Alemneh Tadesse Kassie,

    Roles Formal analysis, Software, Writing – review & editing

    Affiliation Department of Clinical Midwifery, School of Midwifery, College of Medicine and Health Sciences, University of Gondar, Gondar, Ethiopia

  • Alemken Eyayu Abuhay,

    Roles Methodology, Visualization, Writing – original draft

    Affiliation University of Gondar Comprehensive Specialized Hospital, Gondar, Ethiopia

  • Wondimnew Mersha Biset,

    Roles Formal analysis, Software, Writing – original draft, Writing – review & editing

    Affiliation Department of Anesthesiology, Critical Care and Pain Medicine, Saint Paul’s Hospital Millennium Medical College, Addis Ababa, Ethiopia

  • Gebrye Gizaw Mulatu,

    Roles Methodology, Visualization, Writing – review & editing

    Affiliation Department of Health Informatics, Institute of Public Health, College of Medicine and Health Sciences, University of Gondar, Gondar, Ethiopia

  • Nuhamin Tesfa Tsega

    Roles Conceptualization, Formal analysis, Methodology, Validation, Visualization, Writing – original draft, Writing – review & editing

    Affiliation Department of Women’s and Family Health, School of Midwifery, College of Medicine and Health Sciences, University of Gondar, Gondar, Ethiopia

Abstract

Background

Precancerous cervical lesions, or cervical intraepithelial neoplasia (CIN), represent a significant precursor to cervical cancer, posing a considerable threat to women’s health globally, particularly in developing countries. In Africa, the burden of premalignant cervical lesions is not well studied. Therefore, the main purpose of this systematic review and meta-analysis was to determine the overall prevalence of precancerous cervical lesions and identifying determinants among women who underwent cervical cancer screening in Africa.

Methods

This study followed the Preferred Reporting Item Review and Meta-analysis (PRISMA) guidelines. The protocol for this systematic review and meta-analysis was registered on the International Prospective Register of Systematic Reviews (PROSPERO) (ID: CRD42025645427). We carried out a systematic and comprehensive search on electronic databases such as PubMed and Hinari. In addition, Google Scholar and ScienceDirect were utilized to find relevant studies related to precancerous cervical lesions. Data from the included studies were extracted using an Excel spreadsheet and analyzed using STATA version 17. The methodological quality of the eligible studies was examined using the Joanna Briggs Institute (JBI) assessment tool. Publication bias was checked by using the funnel plot and Egger’s tests. A random-effects model using the Der Simonian Laird method was used to estimate the pooled prevalence of pre-cancerous cervical lesions in Africa. The I-squared and Cochrane Q statistics were used to assess the level of statistical heterogeneity among the included studies.

Results

A total of 112 eligible articles conducted in Africa, encompassing 212,984 study participants, were included in the quantitative meta-analysis. Thus, the pooled prevalence of pre-cancerous cervical lesions in Africa was 17.06% (95% confidence interval: 15.47%−18.68%). In this review, having no formal education (AOR = 4.07, 95% CI: 1.74, 9.53), being rural dweller(AOR = 2.38, 95% CI: 1.64, 3.46), history of STIs (AOR = 3.94, 95% CI: 2.97, 5.23), history of having multiple partners (AOR = 2.73, 95% CI: 2.28, 3.28), early initiation of coitus (AOR = 2.77, 95% CI: 2.11, 3.62), being HIV-seropositive women (AOR = 3.33, 95% CI: 2.32, 4.78), a CD4 count <200 cells/mm³ (AOR = 5.17, 95% CI: 1.70, 15.71), not being on ART (AOR = 2.58, 95% CI: 1.45, 4.58), smoking (AOR = 3.91, 95% CI: 1.43, 10.67) and prolonged use of oral contraceptive pills (AOR = 4.39, 95% CI: 2.77, 6.96) were significantly associated with precancerous cervical lesions.

Conclusions

In Africa, the overall prevalence of pre-cancerous cervical lesions is high (17%). The findings of this review highlight that health professionals, health administrators, and all other concerned bodies need to work in collaboration to expand comprehensive cervical cancer screening methods in healthcare facilities for early detection and treatment of cervical lesions. In addition, increasing community awareness and health education, expanding visual inspection of the cervix with acetic acid in rural areas, offering special attention to high-risk groups (HIV-positive women), encouraging adherence to antiretroviral therapy for HIV-positive women, overcoming risky sexual behaviors and practices, and advocating early detection and treatment of precancerous cervical lesions.

Introduction

Cervical cancer is the fourth most prevalent malignancy and the fourth leading cause of mortality in women globally [1]. In 2022, it is responsible for approximately 662,000 new cases and around 349,000 deaths [2]. It is the most common cancer among women in 25 countries, many of which are in Sub-Saharan Africa [2]. Despite being a global public health concern, cervical cancer remains the second most prevalent malignancy and the second leading cause of cancer-related death among women in low- and middle-income countries, including in Africa [1,3].

A precancerous cervical lesion (PCL), or cervical intraepithelial neoplasia (CIN), also known as cervical dysplasia, refers to abnormal cellular changes occurring in the transformation zone of the cervix [2,4]. Histologically, it’s commonly classified into three grades, such as CIN 1 (mild), CIN 2 (moderate), and CIN 3 (severe). Cervical carcinogenesis typically begins with the formation of CIN, which progresses from mild dysplasia (CIN1) to high-grade squamous intraepithelial lesions (CIN2, CIN3), which is thought to be a true precursor to advanced cervical cancer [5].

Human papillomavirus (HPV) infection causes nearly 99.7% of precancerous and malignant cervical lesions [68]. Human Papillomavirus (HPV) infections are typically transient, causing mild and self-limiting lesions. However, when the infection persists, it can progress to PCL and cervical cancer [911]. Persistent HPV infection plays a critical role in the cause and progression of CIN, particularly high-risk types such as HPV 16 and 18, which together are responsible for over 70% of cervical cancer cases [2]. Persistent high-risk HPV strains play a pivotal role in the disease’s pathogenesis by integrating their DNA into host cells and disrupting normal cell cycle regulation [12].

In sub-Saharan Africa, cervical cancer is a significant cause of cancer-related morbidity and mortality among women, primarily due to chronic HPV infections and the prevalent occurrence of HIV co-infection [13]. Nevertheless, antiretroviral therapy (ART) has been shown to decrease the likelihood of HPV infection, enhance the body’s capacity to eradicate the virus, and decrease the risk of developing precancerous cervical lesions and its progression into cervical cancer [14,15]. Early detection and treatment of precancerous lesions often halt the gradual progression into cervical uterine cancer [16]. Progression to invasive cervical cancer can take more than 20 years after initial HPV infection, with CIN1 developing slowly and potentially progressing rapidly to high-grade lesions (CIN2 or CIN3) [17,18].

The WHO has launched a Global Strategy to Accelerate Cervical Cancer Elimination by 2030 that involves three important strategies: vaccination against HPV, screening, and treatment [2,19]. In 2020, the WHO introduced the 90-70-90 global plan for preventing cervical cancer. This plan targets 90% of girls fully vaccinated against HPV by age 15 years, 70% of women to be screened for cervical disease with a high-performance test at least twice by the age of 45, and 90% of women with PCL and invasive cervical cancer should receive appropriate treatment [2,20,21].

The primary strategy to combat cervical cancer is HPV vaccination, which effectively prevents the development of precancerous lesions that increase the risk of cervical cancer in women [22]. Moreover, regular and timely cervical cancer screening methods, including Pap smear tests, HPV DNA testing, dual-stain cytology, and visual inspection, serve as a crucial secondary prevention strategy that facilitates early detection and treatment of precancerous lesions, making cervical cancer largely preventable [2,18,23]. However, the majority of women in countries with limited resources have no access to early detection and treatment of PCL. Screening and diagnosis of PCL remains a major challenge in LMICs [24,25]. In resource-limited areas, visual inspection of the cervix with acetic acid (VIA) or with Lugol’s iodine (VILI) followed by treatment (screen-and-treat approach) is the best alternative approach for secondary prevention of invasive cervical cancer [26,27].

Since cervical cancer is the leading cause of cancer-related death for women globally, proper CIN treatment approaches are essential [28]. Effective cervical cancer screening programs, coupled with timely treatment of abnormal findings, can reduce the disease burden by up to 80% [2,29]. Both excisional techniques (cold knife conization, loop electrosurgical excision procedure, or LEEP) and ablative techniques (laser ablation, thermal ablation, and cervical cryotherapy) are effective therapeutic methods for PCL [30,31]. In prior studies women’s age, educational status, history of STIs, history of multiple partners, early initiation of sexual intercourse, being HIV-positive, smoking, and prolonged use of oral contraceptive pills were significantly associated with precancerous cervical lesions [13,3234].

Cervical cancer is notably preventable and manageable through early detection at the pre-invasive stage, widespread HPV vaccination before sexual debut, and access to effective treatment [2]. These measures can significantly reduce individual risk and the broader burden of morbidity and mortality [2,35]. Despite the high morbidity and mortality associated with PCL and cervical cancer in Africa, HPV vaccination coverage (41.38%) and cervical cancer screening uptake (21%) remain significantly below the WHO’s 90–70–90 global targets [36,37]. Furthermore, existing systematic reviews in the region are limited and often characterized by methodological inconsistencies and variations in study populations [13,38,39].

Most existing evidence primarily focuses on the incidence and mortality of invasive cervical cancer, HPV vaccination coverage, or overall screening uptake. However, there is a scarcity of consolidated evidence on PCL and its associated factors in Africa. This systematic review and meta-analysis aimed to synthesize evidence from multiple studies to estimate the pooled prevalence of PCL and identifying determinants among women who underwent cervical cancer screening, irrespective of age or HIV status. This comprehensive evidence is crucial for evaluating the effectiveness of screening programs and implementing evidence-based interventions, specifically as PCL represent a key target for timely treatment and prevention of invasive cervical cancer. It provides evidence-based insights to strengthen both facility-based and community-based cervical cancer screening approaches. Ultimately, it enables the detection and treatment of precancerous cervical lesions, improves survival rates, and reduces morbidity and mortality from cervical cancer.

Research questions

  1. What is the pooled prevalence of precancerous cervical lesions among women screened for cervical cancer in Africa?
  2. What are the determinant factors of precancerous cervical lesions among women screened for cervical cancer in Africa?

Materials and methods

Study protocol and search strategy

This systematic review followed the Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) guidelines [40] (S1 file). The study protocol was developed and registered on PROSPERO (ID: CRD42025645427).

We conducted a comprehensive search on Google Scholar, PubMed, Hinari, and ScienceDirect for primary studies of precancerous cervical lesions and its determinant factors undertaken in Africa. The search technique was based on the condition, context, and study population (CoCo Pop) framework [41]. Publications were retrieved from prior studies meeting the eligibility criteria. A search strategy was developed for databases by combining keywords using Boolean operators. Both published and unpublished articles between January 1, 2015, and February 20, 2025, were included. Finally, we used the following combination of searching terms: “prevalence,” “magnitude,” “burden,” “precancerous cervical lesions,” “premalignant cervical lesions,” “cervical intraepithelial neoplasia,” “CIN”, “cervical lesions,” Africa. In addition, snowballing techniques were used to retrieve further studies from the citation list of papers identified in the available databases (S2 file).

Eligibility criteria

Inclusion criteria.

Condition: The condition of interest was pre-cancerous cervical lesions among women who underwent cervical cancer screening.

Context: All primary studies that reported the prevalence and/or associated factors of precancerous cervical lesions in the Africa context.

Population: The study population included all women aged 15 years and above, regardless of HIV status, who underwent cervical cancer screening.

Study design: All primary observational studies, including cross-sectional, case-control, and cohort studies that reported the prevalence and/or associated factors of pre-cancerous cervical lesions in Africa.

Publication year: Studies published between 2015 and 2025.

Exclusion criteria.

Articles were excluded for the following reasons: the article did not report the outcome of interest, narrative reviews, qualitative reviews, expert opinions, case reports, editorials, correspondence, abstracts, and methodological studies.

Measurement of outcome variables

The primary objective of this study was to determine the overall prevalence of precancerous cervical lesions among women screened for cervical cancer in Africa. The magnitude of PCL was calculated by dividing the number of women who screened positive for precancerous cervical lesions by the total number of women in the study and then multiplying by 100. The second objective of this study was to identify factors associated with pre-cancerous cervical lesions in Africa, which were evaluated using adjusted odds ratios from prior studies.

The WHO recommends screening and treating precancerous lesions to prevent cervical carcinoma [35]. Cervical cancer screening is the practice of checking women for precancerous or malignant cells on the cervix using diagnostic procedures including the cytology (Pap smear), the HPV DNA test, or VIA [35,42]. These procedures involve taking cervical cells for microscopic analysis or diagnosing the presence of HPV, a virus associated with cervical cancer [42,43]. Histologically, CIN can be classified into three stages, CIN 1, CIN 2, and CIN 3. It can also divided into two stages: low-grade squamous intraepithelial lesions (LSIL, CIN 1) and high-grade squamous intraepithelial lesions (HSIL, CIN 2, 3) [2,5].

Additionally, a positive finding is an acetowhite lesion with well-defined margins near the transformation zone, or a white cervix (visual inspection with acetic acid). Visual inspection with acetic acid yields a negative test if there is no acetowhite lesion, but a visible ulcer with seeping and bleeding may indicate cancer [35]. This review included all studies that reported positive findings for PCL, regardless of participants’ age, HIV status, or the cervical cancer screening methods employed.

Quality assessment for included studies

The Joanna Briggs Institute (JBI) Critical Appraisal Checklist for cross-sectional studies was used to evaluate the quality of included articles in this study [41]. This quality assessment checklist contains nine items, ranging from 0 to 9. Studies that scored 5 or higher on the JBI checklist were considered high quality and therefore included in the review. The studies’ quality was evaluated independently by two authors, BAM and NTT. Any disputes in quality assessment between these two authors were handled through open discussion and consultation with a second author, GMA.

Data extraction and management

Two authors (BAM and NTT) carried out data extraction from the included articles using a standardized data abstraction form developed in an Excel spreadsheet. Based on the inclusion and exclusion criteria, all searched studies were transferred to EndNote 20, reference management software [44]. Articles were screened and selected first based on their title and abstract, and then the full text was reviewed. In cases of dispute, discussions with third reviewers (GMA) were held to determine the final article selection to include in this review. Following the comprehensive searching, possibly eligible publications were imported into Endnote software. Duplicate studies were deleted in cases where two or more papers shared similar features. Structured data extraction in a Microsoft Excel spreadsheet was designed and implemented. For each primary study, the following data were extracted: identification data (first author’s last name and publication year), prevalence of PCL, factors associated with PCL, adjusted odds ratio with 95% confidence intervals, study area, sample size, publication bias assessment methods, risk bias assessment method, and scores (S3 file).

Data synthesis and statistical analysis

Data were extracted using a Microsoft Excel spreadsheet and then exported to STATA 17 statistical software, where all statistical data analyses were performed [45]. The extracted data were presented as texts, tables, and forest plots. The standard error of prevalence for each study was calculated using a binomial distribution. The pooled prevalence of the studies was examined for heterogeneity using the Higgins I-squared (I2) test. Heterogeneity among those included was characterized as low, moderate, or high based on I-square values of <25%, 50%−75%, and 75%, respectively [46].

A random-effects meta-analysis approach (Der Simonian and Laird’s method) was employed to estimate the pooled prevalence of PCL in Africa. Subgroup analysis was performed across the country, regions of Africa, screening methods, and study population to identify potential sources of study heterogeneity. Additionally, we conducted a leave-one-out sensitivity analysis to examine the effect of individual studies on the pooled estimate. The pooled estimates across the continent were then displayed using forest plots and tables, along with their respective 95% confidence intervals. Graphically, publication bias was examined using a forest plot (23). Furthermore, the statistical significance of publication bias was tested using both Egger’s and Begg’s tests, and a p-value less than 0.05 was employed to confirm the existence of publication bias [47]. A trim and fill analysis could be performed to determine the number of potentially missed studies and estimate the adjusted pooled prevalence of PCL. In the end, the pooled adjusted odds ratio (AOR) with 95% confidence intervals was displayed using forest plots.

Results

Study selection and characteristics of the included studies

A total of 1,187 studies were retrieved through all searching databases, including Google Scholar; 312 duplicate records were removed, and further screening was performed for the remaining 875 studies. However, we excluded the majority of studies (n = 736) by reading their titles and abstracts. Then, the remaining 139 full-text articles were examined for eligibility criteria, and 27 studies were dropped for different reasons, such as variation in the study context, insufficient data, not being directly related to the outcome of interest, scoping reviews, and qualitative reviews. In total, 112 eligible articles were included in the final quantitative meta-analysis [48144] (Fig 1).

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Fig 1. Prisma flow diagram showing the selection of studies for precancerous cervical lesions in Africa.

https://doi.org/10.1371/journal.pone.0338484.g001

This systematic review and meta-analysis included a total of 212,984 women who underwent cervical cancer screening. In terms of the distribution of the studies across Africa, 54 and 41 studies were conducted in East Africa and West Africa, respectively (Table 1, S3 file).

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Table 1. Descriptive summary of studies included in systematic review of the prevalence of precancerous cervical lesions (PCL) in Africa.

https://doi.org/10.1371/journal.pone.0338484.t001

Magnitude of precancerous cervical lesions in Africa

In this study, the pooled prevalence of precancerous cervical lesions in Africa was 17.06% (95% confidence interval: 15.47%−18.68%). The statistical test found significant heterogeneity among the included studies (heterogeneity I2 = 99.19%, p-value = 0.000). Thus, a random-effects meta-analysis model was applied.

Heterogeneity and sub-group analysis

A subgroup analysis was carried out based on the country in which the study was conducted, the study population, and cervical cancer screening methods. Accordingly, the highest prevalence was found in Zambia, 42.79% (95% CI: 3.89, 89.46), whereas the lowest prevalence was detected in Mali, 6.72% (95% CI: 1.82, 11.62). In addition, a subgroup analysis was carried out based on the study population; a higher overall magnitude of PCL was found among women with HIV (22.87%; 95% CI: 17.28, 28.46). Regarding the screening methods, the highest overall prevalence of PCL was found in HPV DNA and colposcopy diagnostic methods, 24.92% (95% CI: 4.35, 45.50). While the lowest overall prevalence was reported in VIA screening methods, 14.60% (95% CI: 13.13, 16.08). Despite conducting subgroup analysis based on the aforementioned factors, no significant improvement in heterogeneity in the pooled estimate of PCL (Table 2).

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Table 2. Sub-group analysis of precancerous cervical lesions among women who screened in Africa.

https://doi.org/10.1371/journal.pone.0338484.t002

Publication bias, trim and fill analysis

A funnel plot was used to visually check the presence of publication bias, while Egger’s test was employed to confirm it. In this study, the funnel plot looks slightly asymmetrical, which shows the existence of publication bias among the studies. Statistically, Egger’s (p-value = 0.000) and Begg’s tests (p-value = 0.000) were statistically significant, indicating the presence of publication bias (Fig. 2).

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Fig 2. A funnel plot test that demonstrating the prevalence of precancerous cervical lesions in Africa.

https://doi.org/10.1371/journal.pone.0338484.g002

A non-parametric trim and fill statistical analysis was performed to determine the number of potentially missing studies to reduce and adjust for publication bias in the included studies. However, the trim and fill analysis revealed the absence of significant publication bias because the overall prevalence of observed studies was equal to the sum of observed and imputed studies (Table 3).

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Table 3. Non-parametric trim and fill analysis of publication bias for precancerous cervical lesions among women who screened in Africa.

https://doi.org/10.1371/journal.pone.0338484.t003

Sensitivity analysis

A leave-one-out sensitivity analysis using the random-effects model was performed to examine the effect of a single study on the estimated effect size. However, the findings show that a single study did not significantly affect the total effect size, and the point estimate of the omitted study falls within the confidence interval of the overall estimate of PCL. This proved the reliability of the pooled estimate of precancerous cervical lesions in Africa (S4 file).

Factors associated with precancerous cervical lesions in Africa

This systematic review and meta-analysis examined 24 publications that reported factors associated with precancerous cervical lesions in Africa. In this study, no formal education, rural residency, history of STIs, history of multiple partners, early initiation of coitus, HIV seropositive women, low CD4 count, not being on ART, smoking, and OCP were all significantly associated with precancerous cervical lesions in Africa.

In this meta-analysis, women who had no formal education were four times more likely (AOR = 4.07, 95% CI: 1.74, 9.53) to develop PCL than those who had formal education. Women from rural areas were 2.38 times more likely (AOR: 2.38, 95% CI: 1.64, 3.458) to develop precancerous cervical lesions as compared to women living in urban areas. The odds of PCL were 3.94 times more likely in women with a history of STIs (AOR = 3.94, 95% CI: 2.97, 5.23) than in women who did not have a history of STIs.

According to the pooled odds ratio of 21 studies, it was found that having a history of multiple sexual partners was significantly associated with developing precancerous cervical lesions. Moreover, women with multiple sexual partners had 2.73 times (AOR = 2.73; 95% CI: 2.28, 3.28) higher likelihood of developing precancerous cervical lesions compared to their counterparts. Women who began sexual intercourse early, before 18 years, were three times more likely to develop PCL than women who did not begin sexual intercourse early. In addition, the odds of developing precancerous cervical lesions among HIV-positive women were 3.33 times (AOR = 3.33; 95% CI: 2.32, 4.78) higher than those of HIV-negative women.

In this meta-analysis, CD4 count was identified as an independent factor significantly associated with the occurrence of PCL. HIV-positive women with CD4 counts below 200 cells/mm³ had five times higher odds of developing PCL than those with CD4 counts 200 cells/mm³ or above. The odds of developing precancerous cervical lesions among women who did not start ART were 2.58 times higher than those who initiated ART (AOR: 2.58, 95% CI: 1.45, 4.580).

Concerning personal habits, those women who smoked cigarettes were four times more likely (AOR = 3.91, 95% CI: 1.43, 10.67) to develop PCL than those who did not smoke cigarettes. The odds of developing precancerous cervical lesions were 4.39 times more likely among prolonged OCP users (AOR = 4.39, 95% CI: 2.77, 6.96) when compared with those who were non-users (Table 4).

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Table 4. Factors associated with precancerous cervical lesions among women who screened in Africa.

https://doi.org/10.1371/journal.pone.0338484.t004

Discussion

The main objectives of this systematic review and meta-analysis were to determine the magnitude of PCL and its associated factors in Africa. Thus, the overall prevalence of precancerous cervical lesions in Africa was 17.06% (95% CI: 15.47%18.68%). This finding was slightly higher than studies conducted in Ethiopia that reported 15% [146,147]. Similarly, the magnitude of PCL in this study was higher than studies conducted in Ethiopia at 13% and in Latin America at 4% [34]. This difference could be due to variations in study population, sociocultural setting, and diagnostic or screening methods. The study population for the current study was all women screened for cervical cancer. While the study population for the comparable studies was women living with HIV (WLH). The lower prevalence in Latin America among HIV-positive women could be related to the expanded program of ART (72%) and the decreased number of new HIV infections by 14%, which collectively could reduce the incidence of PCL in the region [34,148]. However, there is a significantly higher HIV pandemic and AIDS-related death rate, particularly in Eastern and Southern Africa. Women and girls were approximately 58% of the total HIV infections, despite persistent gender inequities and widespread violence against females [148].

In contrast, the finding of this study was lower than the magnitude of PCL among HIV-positive women in Sub-Saharan Africa that was reported at 25.6% [13]. This was due to variations in the study population; a higher burden of PCL was found among women living with HIV in SSA [13]. There is evidence that the occurrence of precancerous cervical lesions and cervical cancer is strongly correlated with HIV infection [147,149]. Therefore, high-risk women, including HIV-positive women should undergo regular screening for cervical cancer with the available methods for early detection and treatment of PCL.

These findings underline the necessity for enhanced and comprehensive cervical cancer prevention interventions in Africa. Policymakers, health professionals, and public health systems should prioritize expanding primary prevention through HPV vaccination (9–14 years) and strengthening secondary prevention by implementing accessible and population-based screening programs (e.g., VIA, cytological or HPV DNA testing). These initiatives contribute to advancing the WHO’s global agenda for cervical cancer elimination and improving women’s health outcomes across African countries.

With varying degrees of accuracy, this review combined the PCL magnitude using various cervical cancer screening techniques. Therefore, a subgroup analysis based on screening methods was conducted; the lowest overall prevalence of PCL was recorded in VIA screening methods (14.60%), whereas the highest pooled prevalence was identified in HPV DNA and colposcopy testing methods (24.92%). Nowadays, there are two methods for PCL screening and treatment. The initial approach is the screen-and-treat strategy, in which a positive primary screening test is the sole basis for treatment decisions [2]. The second technique is the screen, triage, and treat approach, in which the decision to treat relies on a positive initial screening test followed by a positive subsequent test, known as a “triage” test, with or without histological confirmation of diagnosis [2]. The World Health Organization (WHO) promotes a screen, triage, and treat approach with HPV DNA as the primary screening test for the general female population, followed by additional investigations [2]. However, visual examination with acetic acid (VIA) is an easily and highly cost-effective screening approach for premenopausal women in low- and middle-income countries (LMICs) [150152].

In this systematic review and meta-analysis, precancerous cervical lesions are significantly more prevalent among HIV-positive women (22.87%) than HIV-negative women (12.95%). This finding was in agreement with studies done in Ethiopia and SSA [13,147,149]. This finding was in agreement with studies done in Ethiopia and SSA [34,147,149]. This could be explained by the fact that HIV-positive women are more susceptible to developing PCL due to their compromised immune system, which allows for chronic HPV infections, which is the leading cause of PCL and cervical cancer. Furthermore, co-infection with other STIs and having more lifetime sexual partners increase the risk. Therefore, integrating cervical cancer screening into ART clinics can enhance early detection and timely treatment of PCL, thereby reducing the risk of progression to invasive cervical cancer and improving health outcomes among these high-risk groups.

This study found that having no formal education, being a rural resident, having a history of STIs, having a history of multiple partners, early initiation of coitus, being an HIV-seropositive woman, having a low CD4 count, not being on ART, smoking, and prolonged use of OCPs were all significantly associated with precancerous cervical lesions.

In this study, the odds of developing PCL among women who did not have a formal education were four times higher than those who had formal education. This finding was consistent with other studies [153,154]. This could be explained as a lack of educational attainment might be linked with high-risk sexual behavior and a lack of information on STIs, including HPV, which is the leading cause of PCL and cervical cancer [155].

Moreover, the odds of developing precancerous cervical lesions among women living in rural areas were higher when compared to women living in urban areas. This finding was supported by other studies [156,157]. This is due to the fact that women had limited information and services access, poor health-seeking behavior, and lower coverage of HPV vaccination in rural as compared with urban areas [73,157]. The odds of developing precancerous cervical lesions were higher among women with multiple sexual partners compared to their counterparts [13,147,154]. Women with several sexual partners are clearly more vulnerable to STIs, particularly high-risk HPV strains, resulting in persistent HPV infection and precancerous cervical lesions [8,13].

In comparison to women without a history of STIs, those with a history of STIs were more likely to develop PCL. This finding is in agreement with other study findings [13,147,154]. This elevated risk is mainly associated with the exposure of high-risk HPV strains, primarily HPV 16 and 18, which account for nearly 70% of cervical cancer cases [158,159]. Furthermore, other STIs, such as chlamydia and herpes virus, could potentially contribute to cervical cancer progression by creating chronic inflammation, allowing HPV to persist and progress to PCL [160,161]. As a result, immunization against HPV at the optimal age of children and regular cervical cancer screening are crucial preventive measures to reduce this risk.

Moreover, initiation of early sexual intercourse before the age of 18 years was significantly associated with PCL. This conclusion is similar to other studies [162,163]. Early sexual activity is associated with an immature cervical epithelium during adolescence, particularly the transformation zone (TZ), and prolonged cumulative exposure to HPV, the major cause of cervical cytological abnormalities [164,165]. It has also been linked to risky sexual behaviors, such as using condoms inconsistently or having several sexual partners [166].

The odds of developing precancerous cervical lesions were 3.33 times more likely among HIV-positive women when compared with those HIV-negative women. The finding of this study was supported by another systematic review and meta-analysis [144,149]. In general, HIV-infected women are much more likely to acquire precancerous cervical lesions due to the immunosuppression effect of HIV (low CD4 cells), higher risk of co-infections with other STIs, and persistent HPV infection [149,167]. This highlights the importance of primary HIV prevention, good ART adherence, integrating cervical cancer screening, and preventative strategies in HIV care programs in order to lower the risk of PCL and invasive cervical cancer.

In this study, women’s CD4 counts were the other independent factor that was significantly associated with PCCL. Thus, HIV-positive women with CD4 counts below 200 cells/mm³ were five times more likely to develop PCL when compared to CD4 counts ≥200 cells/mm³. This conclusion is consistent with other study findings [13,15,149,168]. The possible explanation could be related to reactivation and persistent HPV infection due to immune deficiency or high viral load [15,161]. Therefore, prompt initiation and proper adherence to highly active antiretroviral therapy (HAART) is essential for boosting up the immune system and decreasing viral load, which ultimately reduce the occurrence of PCL and malignant cervical cancer.

Likewise, the odds of developing PCL were more likely among women who are not on ART than those on ART. This was in agreement with other studies, and this could be explained as a decrease in high-risk HPV persistence, and the histologic diagnosis of CIN2 + was linked to being on effective ART (i.e., individuals with longer duration, maintained HIV viral suppression, and steady higher CD4 cell count) [15,168,169]. This finding emphasizes the importance of ART in lowering the risk of PCL in HIV-positive women. It strengthens the immune system, accelerating the clearance of high-risk infections caused by HPV and decreasing the progression of cervical lesions, lowering the risk of advanced cervical cancer.

This study also concluded that women who smoked cigarettes were four times more likely to develop PCL than those who did not smoke cigarettes. This finding was congruent with prior meta-analysis studies [32,170,171]. A plausible explanation is that smoking exposes women to toxic chemicals that can directly damage cervical epithelium DNA. Additionally, cigarette smoking is strongly linked to aberrant methylation of tumor suppressor genes, such as p16 (CDNK2A), in women with high-grade CIN and squamous cell carcinoma [172,173]. Nicotine and other tobacco ingredients could harm the immune system’s ability to get rid of HPV infections, which are highly linked to cervical neoplasia. This weakened defense allows for chronic HPV infections, raising the likelihood of CIN [174]. Therefore, health practitioners should always counsel women to undergo regular cervical cancer screening and abstain from smoking or quit smoking in order to prevent the long-term effects of tobacco.

The odds of developing precancerous cervical lesions were 4.39 times more likely among prolonged OCP users when compared with those who were non-users. This finding was congruent with prior meta-analysis studies [175178]. The possible justification might be that prolonged use of oral contraceptives, particularly estrogen, may stimulate cervical epithelial proliferation, thereby making them more susceptible to HPV-induced DNA damage and neoplastic transformation [33,175,179]. So, regular cervical screening is recommended for women who use OCP for extended periods of time to ensure early detection and treatment of cervical abnormalities. Risk-benefit assessment on OCP and considering alternative contraception methods with healthcare professionals to reduce the risk of PCL.

Implications of the study

This review highlights a high burden of precancerous cervical lesions among women undergoing cervical cancer screening across Africa. The pooled estimate indicates that a substantial proportion of screened women are at risk of progression to invasive cervical cancer if timely diagnosis and effective treatment interventions are not implemented. This finding underscores the urgent need to strengthen national and regional efforts targeting both primary and secondary prevention of PCL and advanced cervical cancer. Thus, the findings of this review provide important baseline evidence for health professionals, policymakers, researchers, and global partners to design and implement evidence-based interventions to achieve the WHO 90-70-90 strategy targeted to eliminate CC. Key strategies should include expanding HPV vaccination coverage, scaling up accessible and cost-effective screening methods such as visual inspection with acetic acid and HPV DNA testing, and implementing population-based screening programs.

Furthermore, ensuring timely diagnosis and treatment of precancerous lesions is critical to interrupt disease progression. Integrating cervical cancer screening into existing reproductive healthcare services, such as HIV care and maternal health, can enhance coverage and efficiency. Strengthening health system readiness, including workforce training, provision of essential equipment, and infrastructure improvement alongside regular monitoring, evaluation, and follow-up mechanisms, is crucial to ensure continuity of care and long-term program effectiveness. These measures are vital for facilitating the early detection and management of precancerous cervical lesions, thereby assisting to lower the incidence of cervical cancer.

Strengths and limitations of the study

This systematic review and meta-analysis synthesized evidence on the burden of precancerous cervical lesions and their associated factors in Africa, highlighting a critical public health issue. The findings serve as baseline evidence and offer valuable insights for clinicians, policymakers, researchers, and other stakeholders to prioritize the prevention and control of PCL and cervical cancer.

However, the following limitations should be considered when interpreting the findings of this review. Firstly, the findings of this review are based on previous primary studies that utilized calculated sample populations rather than nationally or regionally representative data. This may limit the generalizability of the finding to broader populations across African countries. Secondly, the presence of significant heterogeneity among the included studies might affect the inference to the continent. This might be due to variations in the study settings and methodologies, including variation in the sampling technique, sample size, analytical techniques, and difference in screening methods, which could affect the generalizability of the pooled estimate. This could be explained as the presence of substantial clinical and methodological heterogeneity across the studies resulting from the diverse in cervical cancer screening modalities utilized in the included studies specifically, VIA, cytology, and HPV DNA testing as well as the application of varying diagnostic algorithms (screen-and-treat, sequential, or combined approaches). These methods exhibit significant variations in sensitivity, specificity, and operator dependence result to diagnosis the presence of PCL.

Additionally, due to the concentration of studies in some countries, such as Ethiopia and Nigeria, it could restrict the conclusion of the finding to the continent. Another potential limitation of this review is the possibility of publication bias due to the use of PubMed as a major database for literature searches. Although PubMed is a well-known and extensive biomedical database, its sole or predominant use could have resulted in the exclusion of important studies indexed in other databases (for example, Embase, Scopus) or unpublished grey literature. To address this gap, we supplemented our search by systematically exploring Google Scholar to identify both published and unpublished studies, and we also used ScienceDirect to retrieve relevant articles from Elsevier-indexed journals.

Despite these limitations, the use of a random-effects model, along with subgroup and sensitivity analyses, strengthens the robustness of the findings and provides a valuable benchmark for future research and evidence-based policy development. Regarding the determinant factors, the confidence intervals for some variables, such as educational status, women’s CD4 count, and smoking, were relatively wide, indicating potential uncertainty in the effect estimates and suggesting the need for cautious interpretation. This may be attributed to the small sample sizes in the primary studies and the limited number of studies included in the quantitative meta-analysis.

Finally, the estimated magnitude of PCL is primarily based on facility-based studies conducted across Africa. Consequently, the exact burden of PCL may be underestimated due to the limited inclusion of community-based data. To address this gap, we strongly recommend the expansion of both facility-based and community-based cervical cancer screening programs to enhance early detection and ensure timely treatment of PCL across African countries.

Conclusions

In conclusion, the overall prevalence of precancerous cervical lesions in Africa is high (17%).

In this meta-analysis study, having no formal education, rural residency, a history of STIs, a history of multiple partners, early initiation of coitus, being an HIV-seropositive woman, a CD4 count of <200 cells/mm³, not being on ART, smoking, and prolonged use of oral contraceptive pills were significantly associated with precancerous cervical lesions. Therefore, health professionals, health administrators, and all other concerned bodies need to work in collaboration to expand comprehensive cervical cancer screening methods in healthcare facilities for early detection and treatment of cervical lesions. In addition, increasing community awareness and health education, expanding VIA in rural areas, expanding accessibility of screening methods, encouraging adherence to ART, overcoming risky sexual behaviors and practices, promoting safe sexual practices, providing special attention for high-risk groups (such as women living with HIV or having multiple sexual partners), and advocating early detection and treatment of precancerous cervical lesions.

References

  1. 1. Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68(6):394–424. pmid:30207593
  2. 2. World Health Organization. WHO guideline for screening and treatment of cervical pre-cancer lesions for cervical cancer prevention: use of dual-stain cytology to triage women after a positive test for human papillomavirus (HPV): World Health Organization; 2024.
  3. 3. Singh D, Vignat J, Lorenzoni V, Eslahi M, Ginsburg O, Lauby-Secretan B, et al. Global estimates of incidence and mortality of cervical cancer in 2020: a baseline analysis of the WHO Global Cervical Cancer Elimination Initiative. Lancet Glob Health. 2023;11(2):e197–206. pmid:36528031
  4. 4. Gupta S, Nagtode N, Chandra V, Gomase K. From Diagnosis to Treatment: Exploring the Latest Management Trends in Cervical Intraepithelial Neoplasia. Cureus. 2023;15(12):e50291. pmid:38205499
  5. 5. Kusakabe M, Taguchi A, Sone K, Mori M, Osuga Y. Carcinogenesis and management of human papillomavirus-associated cervical cancer. Int J Clin Oncol. 2023;28(8):965–74. pmid:37294390
  6. 6. Gakidou E, Nordhagen S, Obermeyer Z. Coverage of cervical cancer screening in 57 countries: low average levels and large inequalities. PLoS Med. 2008;5(6):e132. pmid:18563963
  7. 7. Walboomers JM, Jacobs MV, Manos MM, Bosch FX, Kummer JA, Shah KV, et al. Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol. 1999;189(1):12–9. pmid:10451482
  8. 8. Arbyn M, Weiderpass E, Bruni L, de Sanjosé S, Saraiya M, Ferlay J, et al. Estimates of incidence and mortality of cervical cancer in 2018: a worldwide analysis. Lancet Glob Health. 2020;8(2):e191–203. pmid:31812369
  9. 9. Naucler P, Ryd W, Törnberg S, Strand A, Wadell G, Elfgren K, et al. Human papillomavirus and Papanicolaou tests to screen for cervical cancer. N Engl J Med. 2007;357(16):1589–97. pmid:17942872
  10. 10. Bogani G, Sopracordevole F, Ciavattini A, Vizza E, Vercellini P, Giannini A, et al. Duration of human papillomavirus persistence and its relationship with recurrent cervical dysplasia. Eur J Cancer Prev. 2023;32(6):525–32. pmid:37401466
  11. 11. Lei J, Ploner A, Elfström KM, Wang J, Roth A, Fang F, et al. HPV Vaccination and the Risk of Invasive Cervical Cancer. N Engl J Med. 2020;383(14):1340–8. pmid:32997908
  12. 12. Bhat D. The “Why and How” of Cervical Cancers and Genital HPV Infection. Cytojournal. 2022;19:22. pmid:35510113
  13. 13. Weldegebreal F, Worku T. Precancerous Cervical Lesion Among HIV-Positive Women in Sub-Saharan Africa: A Systematic Review and Meta-Analysis. Cancer Control. 2019;26(1):1073274819845872. pmid:31043067
  14. 14. Gupta R, Mariano LC, Singh S, Gupta S. Highly active antiretroviral therapy (HAART) and outcome of cervical lesions and high-risk HPV in women living with HIV (WLHIV): A systematic review and meta-analysis. Eur J Obstet Gynecol Reprod Biol. 2022;278:153–8. pmid:36194939
  15. 15. Kelly H, Weiss HA, Benavente Y, de Sanjose S, Mayaud P, ART and HPV Review Group. Association of antiretroviral therapy with high-risk human papillomavirus, cervical intraepithelial neoplasia, and invasive cervical cancer in women living with HIV: a systematic review and meta-analysis. Lancet HIV. 2018;5(1):e45–58. pmid:29107561
  16. 16. Lili E, Chatzistamatiou K, Kalpaktsidou-Vakiani A, Moysiadis T, Agorastos T. Low recurrence rate of high-grade cervical intraepithelial neoplasia after successful excision and routine colposcopy during follow-up. Medicine (Baltimore). 2018;97(4):e9719. pmid:29369205
  17. 17. Mogtomo MLK, Malieugoue LCG, Djiepgang C, Wankam M, Moune A, Ngane AN. Incidence of cervical disease associated to HPV in human immunodeficiency infected women under highly active antiretroviral therapy. Infect Agent Cancer. 2009;4:9. pmid:19493339
  18. 18. Bedell SL, Goldstein LS, Goldstein AR, Goldstein AT. Cervical Cancer Screening: Past, Present, and Future. Sex Med Rev. 2020;8(1):28–37. pmid:31791846
  19. 19. World Health Organization. Global strategy to accelerate the elimination of cervical cancer as a public health problem: World Health Organization; 2020.
  20. 20. World Health Organization. WHO’s new recommendations for screening and treatment to Prevent cervical cancer. World Health Organization. 2023. https://www.who.int/news/item/06-07-2021-new-recommendations-for-screening-and-treatment-to-prevent-cervical-cancer. 2021.
  21. 21. World Health Organization. Cervical cancer elimination initiative: from call to action to global movement. Geneva: World Health Organization. 2023. https://www.who.int/initiatives/cervical-cancer-elimination-initiative#cms
  22. 22. Rosalik K, Tarney C, Han J. Human Papilloma Virus Vaccination. Viruses. 2021;13(6).
  23. 23. Okyere J, Aboagye RG, Seidu A-A, Asare BY-A, Mwamba B, Ahinkorah BO. Towards a cervical cancer-free future: women’s healthcare decision making and cervical cancer screening uptake in sub-Saharan Africa. BMJ Open. 2022;12(7):e058026. pmid:35906053
  24. 24. Zhu G, Zhang B, Feng XL. Changes in rate and socioeconomic inequality of cervical cancer screening in. Eliminating cervical cancer from low-and middle-income countries: an achievable public health goal. 2023;78.
  25. 25. Gakidou E, Nordhagen S, Obermeyer Z. Coverage of cervical cancer screening in 57 countries: low average levels and large inequalities. PLoS Med. 2008;5(6):e132. pmid:18563963
  26. 26. Megevand E, Denny L, Dehaeck K, Soeters R, Bloch B. Acetic acid visualization of the cervix: an alternative to cytologic screening. Obstet Gynecol. 1996;88(3):383–6. pmid:8752244
  27. 27. Sheth TM, Maitra N. Study to assess the acceptability and feasibility of cervical cancer screening using visual inspection with acetic acid and treatment of precancerous lesions using cryotherapy in low resource settings. International Journal of Reproduction, Contraception, Obstetrics and Gynecology. 2014;3(3):615–22.
  28. 28. Lycke KD, Kahlert J, Petersen LK, Damgaard RK, Cheung LC, Gravitt PE, et al. Untreated cervical intraepithelial neoplasia grade 2 and subsequent risk of cervical cancer: population based cohort study. BMJ. 2023;383:e075925. pmid:38030154
  29. 29. Chakkalakal RJ, Cherlin E, Thompson J, Lindfield T, Lawson R, Bradley EH. Implementing clinical guidelines in low-income settings: a review of literature. Glob Public Health. 2013;8(7):784–95. pmid:23914758
  30. 30. Santesso N, Mustafa RA, Schünemann HJ, Arbyn M, Blumenthal PD, Cain J, et al. World Health Organization Guidelines for treatment of cervical intraepithelial neoplasia 2-3 and screen-and-treat strategies to prevent cervical cancer. Int J Gynaecol Obstet. 2016;132(3):252–8. pmid:26868062
  31. 31. Hurtado-Roca Y, Becerra-Chauca N, Malca M. Efficacy and safety of cryotherapy, cold cone or thermocoagulation compared to LEEP as a therapy for cervical intraepithelial neoplasia: Systematic review. Rev Saude Publica. 2020;54:27. pmid:32187314
  32. 32. Zhao R, Sekar P, Bennis SL, Kulasingam S. A systematic review of the association between smoking exposure and HPV-related cervical cell abnormality among women living with HIV: Implications for prevention strategies. Prev Med. 2023;170:107494. pmid:37001607
  33. 33. Zou YL, Peng R, Di Xu K, Jiang XR, Sun QY, Song CH. Oral Contraceptives and Health Outcomes: an Umbrella Review of Systematic Reviews and Meta-analyses in Women and Offspring. Journal of Nutritional Oncology. 2022;7(1):9–37.
  34. 34. Fernández-Deaza G, Negrete-Tobar G, Caicedo M, Téllez N, Mello MB, Ghidinelli M, et al. Cervical precancer and invasive cancer among women living with HIV in Latin America: A systematic review and meta-analysis. Int J STD AIDS. 2024;35(13):1008–18. pmid:39222397
  35. 35. World Health Organization. WHO guidelines for screening and treatment of precancerous lesions for cervical cancer prevention: World Health Organization; 2021.
  36. 36. Mengistie BA, Melese M, Gebiru AM, Getnet M, Getahun AB, Tassew WC, et al. Uptake of cervical cancer screening and its determinants in Africa: Umbrella review. PLoS One. 2025;20(7):e0328103. pmid:40690469
  37. 37. Mengistie BA, Yirsaw AN, Lakew G, Mekonnen GB, Shibabaw AA, Chereka AA, et al. Human papillomavirus vaccine uptake and its determinants among women in Africa: an umbrella review. Front Public Health. 2025;13:1537250. pmid:40538696
  38. 38. Ferede YA, Tassew WC, Zeleke AM. Precancerous cervical lesion and associated factors among HIV-infected women in Ethiopia: systematic review and meta- analysis. BMC Cancer. 2024;24(1):678. pmid:38831404
  39. 39. Zena D, Elfu B, Mulatu K. Prevalence and Associated Factors of Precancerous Cervical Lesions among Women in Ethiopia: A Systematic Review and Meta-Analysis. Ethiop J Health Sci. 2021;31(1):189–200. pmid:34158766
  40. 40. Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021;372:n71. pmid:33782057
  41. 41. Munn Z, Moola S, Lisy K, Riitano D, Tufanaru C. Methodological guidance for systematic reviews of observational epidemiological studies reporting prevalence and cumulative incidence data. Int J Evid Based Healthc. 2015;13(3):147–53. pmid:26317388
  42. 42. Web Annex A. WHO guideline for screening and treatment of cervical pre-cancer lesions for cervical cancer prevention. World Health Organization. 2021.
  43. 43. Yirsaw AN, Nigusie A, Andualem F, Getachew E, Getachew D, Tareke AA, et al. Cervical cancer screening utilization and associated factors among women living with HIV in Ethiopia, 2024: systematic review and meta-analysis. BMC Womens Health. 2024;24(1):521. pmid:39300442
  44. 44. Gotschall T. EndNote 20 desktop version. J Med Libr Assoc. 2021;109(3):520–2. pmid:34629985
  45. 45. Fisher DJ, Zwahlen M, Egger M, Higgins JP. Meta‐analysis in Stata. Systematic reviews in health research: meta‐analysis in context. 2022. 481–509.
  46. 46. Huedo-Medina TB, Sánchez-Meca J, Marín-Martínez F, Botella J. Assessing heterogeneity in meta-analysis: Q statistic or I2 index?. Psychol Methods. 2006;11(2):193–206. pmid:16784338
  47. 47. Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics. 1994;50(4):1088–101. pmid:7786990
  48. 48. Abera GB, Yebyo HG, Hailekiros H, Niguse S, Berhe Y, Gigar G, et al. Epidemiology of pre-cancerous cervical lesion and risk factors among adult women in Tigray, Ethiopia. PLoS One. 2023;18(1):e0280191. pmid:36608041
  49. 49. Mona Omar Adam, Abd El monim Bashir Yagoub, Aisha Mohamed Adam, Hammad Ali Fadlalmola. Cervical Pap Smear Abnormalities among Women with Diabetics Versus Non Diabetics Women at Omdurman Military Hospital, Sudan. IJONE. 2023;15(1):49–54.
  50. 50. Ago B, Etokidem A, Ebughe G. Prevalence of abnormal cervical cytology among postnatal clinic attendees at the University of Calabar Teaching Hospital, Nigeria. Open Access Library Journal. 2016;3.
  51. 51. Ali KE, Mohammed IA, Difabachew MN, Demeke DS, Haile T, Ten Hove R-J, et al. Burden and genotype distribution of high-risk Human Papillomavirus infection and cervical cytology abnormalities at selected obstetrics and gynecology clinics of Addis Ababa, Ethiopia. BMC Cancer. 2019;19(1):768. pmid:31382907
  52. 52. Ambounda-Ledaga N, Mabika-Obanda AKF, Tekem VNS, Riveri E, Mombo C, Mangala C, et al. Prevalence and predictors of precancerous cervical lesions among women living with HIV in Libreville, Gabon. Discov Med. 2024;1(1).
  53. 53. Awolude OA, Oyerinde SO, Ayeni AO, Adewole IF. Human papillomavirus-based cervical precancer screening with visual inspection with acetic acid triage to achieve same-day treatments among women living with human immunodeficiency virus infection: test-of-concept study in Ibadan, Nigeria. Pan Afr Med J. 2021;40:48. pmid:34795828
  54. 54. Bateman AC, Katundu K, Mwanahamuntu MH, Kapambwe S, Sahasrabuddhe VV, Hicks ML, et al. The burden of cervical pre-cancer and cancer in HIV positive women in Zambia: a modeling study. BMC Cancer. 2015;15:541. pmid:26205980
  55. 55. Belayneh T, Mitiku H, Weldegebreal F. Precancerous cervical lesion and associated factors among HIV-infected women on ART in Amhara Regional State, Ethiopia: A hospital-based cross-sectional study. Int J Health Sci (Qassim). 2019;13(3):4–9. pmid:31123433
  56. 56. Chibvongodze R, Nyirakanani C, Ojwang J, Mutuku OM, u J, Kyama CM. HPV DNA testing and Pap smear cytology co-testing as a ‘test of cure’ in patients previously treated for CIN III at Kenyatta National Hospital, Nairobi, Kenya. East African Medical Journal. 2019;94:19676–202.
  57. 57. Chris-ozoko L, Barovbe M, Oyem J, Ekanem V. 5-Year Retrospective Study of the Prevalence of Cervical Lesions at the University of Benin Teaching Hospital, Nigeria. Acta Scientiae. 2020;1:235–43.
  58. 58. Daniel GO, Musa J, Akindigh TM, Shinku F, Shuaibu SI, Kwaghe B, et al. Prevalence and predictors of precancerous cervical lesions among HIV-positive women in Jos, north-central Nigeria. Int J Gynaecol Obstet. 2020;151(2):253–9. pmid:32683675
  59. 59. Darré T, Djiwa T, Ladekpo KJO, M’Bortche BK, Douaguibe B, Aboubakari A-S, et al. Factors Associated With Precancerous Cervical Lesions in Human Immunodeficiency Virus-Infected Women: A Cross-Sectional Survey in Togo. Clin Med Insights Oncol. 2024;18:11795549241234620. pmid:38510316
  60. 60. Deksissa ZM, Tesfamichael FA, Ferede HA. Prevalence and factors associated with VIA positive result among clients screened at Family Guidance Association of Ethiopia, south west area office, Jimma model clinic, Jimma, Ethiopia 2013: a cross-sectional study. BMC Res Notes. 2015;8:618. pmid:26515769
  61. 61. Derbie A, Amare B, Misgan E, Nibret E, Maier M, Woldeamanuel Y, et al. Histopathological profile of cervical punch biopsies and risk factors associated with high-grade cervical precancerous lesions and cancer in northwest Ethiopia. PLoS One. 2022;17(9):e0274466. pmid:36094938
  62. 62. Desire BK, Philippe CM, Thierry K, Félix KWM, Wembodinga GU, Prosper KL, et al. Visual inspection with acetic acid and Lugol’s iodine in cervical cancer screening at the general referral hospital Kayembe in Mbuji-Mayi, Democratic Republic of Congo. Pan Afr Med J. 2016;23:64. pmid:27217888
  63. 63. Diop A, Mvundura M, Dieng Y, Anne M, Vodicka E. Cervical cancer screening and treatment costing in Senegal. Pan Afr Med J. 2024;47:151. pmid:38974700
  64. 64. Doh G, Mkong E, Ikomey GM, Obasa AE, Mesembe M, Fokunang C, et al. Preinvasive cervical lesions and high prevalence of human papilloma virus among pregnant women in Cameroon. Germs. 2021;11(1):78–87. pmid:33898344
  65. 65. Donkoh ET, Agyemang-Yeboah F, Asmah RH, Wiredu EK. Prevalence of cervical cancer and pre-cancerous lesions among unscreened Women in Kumasi, Ghana. Medicine (Baltimore). 2019;98(13):e14600. pmid:30921178
  66. 66. Effah K, Tekpor E, Wormenor CM, Allotey J, Owusu–Agyeman Y, Kemawor S. Cervical precancer screening using self-sampling, HPV DNA testing, and mobile colposcopy in a hard-to-reach community in Ghana: a pilot study. BMC Cancer. 2024;24(1):1367.
  67. 67. Eljabu N, Abudher A. Prevalence of Abnormal Cervical Smear at Yash-feen Gynaecological Clinic Tripoli, 2009-2012. Age. 2019;25:22.
  68. 68. Ephrem Dibisa K, Tamiru Dinka M, Mekonen Moti L, Fetensa G. Precancerous Lesion of the Cervix and Associated Factors Among Women of West Wollega, West Ethiopia, 2022. Cancer Control. 2022;29:10732748221117900. pmid:35947527
  69. 69. Eseoghene D, Lawan A, Mohammed A, Musa Y, Usman Y, Dase E. Obstetrics & Gynaecology Pattern of Pre-Malignant Cervical Lesions among Women Attending HIV Clinic in a Tertiary Hospital in North East Nigeria. Tropical Journal of Obstetrics and Gynaecology. 2021;37:301–8.
  70. 70. Essmat A, Meleis M, Elsokkary H, Ahmed SS, El-Soody E. Study of Prevalence of Abnormal Cervical Cytology in Al-Shatby Maternity University Hospital. OJOG. 2021;11(04):434–49.
  71. 71. Fentie AM, Tadesse TB, Gebretekle GB. Factors affecting cervical cancer screening uptake, visual inspection with acetic acid positivity and its predictors among women attending cervical cancer screening service in Addis Ababa, Ethiopia. BMC Womens Health. 2020;20(1):147. pmid:32677933
  72. 72. Getinet M, Jemal M, Baylie T, Fenta E, Belew H, Azanaw G, et al. Magnitude of precancerous cervical lesions induced by human papillomavirus subtypes 16 and 18 and associated factors among affected women. World Acad Sci J. 2024;6(6).
  73. 73. Getinet M, Taye M, Ayinalem A, Gitie M. Precancerous Lesions of the Cervix and Associated Factors among Women of East Gojjam, Northwest Ethiopia, 2020. Cancer Manag Res. 2021;13:9401–10. pmid:35002317
  74. 74. Gnatou GYS, Onivogui Z, Gbeasor-Komlanvi FA, Sadio AJ, Konu YR, Tchankoni MK, et al. Prévalence des lésions précancéreuses du col de l’utérus chez les femmes en âge de procréer dans la région de la Kara au Togo en 2022. Revue d’Épidémiologie et de Santé Publique. 2023;71:101925.
  75. 75. Hailemariam G, Gebreyesus H, Wubayehu T, Gebregyorgis T, Gebrecherkos K, Teweldemedhin M, et al. Magnitude and associated factors of VIA positive test results for cervical cancer screening among refugee women aged 25-49 years in North Ethiopia. BMC Cancer. 2020;20(1):858. pmid:32894100
  76. 76. Hailemariam T, Yohannes B, Aschenaki H, Mamaye E, Orkaido G, Seta M. Prevalence of Cervical Cancer and Associated Risk Factors among Women Attending Cervical Cancer Screening and Diagnosis Center at Yirgalem General Hospital, Southern Ethiopia. J Cancer Sci Ther. 2017;9(11).
  77. 77. Hayumbu V, Hangoma J, Hamooya BM, Malumani M, Masenga SK. Cervical cancer and precancerous cervical lesions detected using visual inspection with acetic acid at Livingstone Teaching Hospital. Pan Afr Med J. 2021;40:235. pmid:35178146
  78. 78. Hoffman LD, Wu H-T. The histological significance of atypical glandular cells on cervical cytology: Experience at Groote Schuur Hospital, Cape Town, South Africa. S Afr Med J. 2016;106(9):907–11. pmid:27601118
  79. 79. Ibrahima C, Sekouba K, Daniel William Atanase L, Thierno Ibrahima D, Alhassane Mohamed S, Yaya D, et al. Precancerous Lesions of the Cervix: Screening and Management at the Matam Maternity Hospital and the Donka Gynaecological Cancer Prevention Centre (Guinea). IJCOCR. 2023.
  80. 80. Inuwa U, Chama C, Audu B, Obed J, Nggada H, Bukar M, et al. Correlates and risk factors for abnormal papanicolaou smear among HIV infected and HIV non infected women in northeastern Nigeria. 2016;4:2326–691.
  81. 81. Irabor G, Isiwele E, Nnoli M, Omoruyi K. The relationship between age and histological types of cervical cancer. International Journal of Scientific Research. 2018;7.
  82. 82. Kagoné TS, Paré PG, Dembélé A, Kania D, Zida S, Bonané/Thiéba B, et al. Cervical cancer in the Hauts-Bassins region of Burkina Faso: Results of a screening campaign by visual inspection with acetic acid (VIA screening in Burkina Faso). Afr J Reprod Health. 2022;26(6):97–103. pmid:37585062
  83. 83. Kamdem DEM, Ngalame AN, Rakya I, Tchounzou R, Mwadjie DW, Neng HT, et al. Contribution of Colposcopy in the Diagnosis of Precancerous Lesions of the Uterine Cervix at the Douala Gynaeco-Obstetric and Pediatric Hospital, Cameroon. OJOG. 2022;12(10):1031–41.
  84. 84. Karuri JW, et al. Conventional pap smear and human papilloma virus DNA co-testing in HIV infected women attending comprehensive care centre in Kenyatta National Hospital. University of Nairobi. 2015.
  85. 85. Kaseka PU, Kayira A, Chimbatata CS, Chisale MRO, Kamudumuli P, Wu T-SJ, et al. Histopathological profile of cervical biopsies in northern Malawi: a retrospective cross-sectional study. BMJ Open. 2022;12(3):e048283. pmid:35277397
  86. 86. Kassa LS, Dile WM, Zenebe GK, Berta AM. Precancerous lesions of cervix among women infected with HIV in Referral Hospitals of Amhara Region, Northwest Ethiopia: a cross sectional study. Afr Health Sci. 2019;19(1):1695–704. pmid:31149000
  87. 87. Katz IT, Butler LM, Crankshaw TL, Wright AA, Bramhill K, Leone DA, et al. Cervical Abnormalities in South African Women Living With HIV With High Screening and Referral Rates. J Glob Oncol. 2016;2(6):375–80. pmid:28717723
  88. 88. Kirabira J, Kayondo M, Bawakanya SM, Nsubuga EJ, Yarine F, Namuli A, et al. Association between HIV Serostatus and premalignant cervical lesions among women attending a cervical cancer screening clinic at a tertiary care facility in southwestern Uganda: a comparative cross-sectional study. BMC Womens Health. 2024;24(1):266. pmid:38678278
  89. 89. Kiros M, Mesfin Belay D, Getu S, Hailemichael W, Esmael A, Andualem H, et al. Prevalence and Determinants of Pre-Cancerous Cervical Lesion and Human Papillomavirus Among HIV-Infected and HIV-Uninfected Women in North-West Ethiopia: A Comparative Retrospective Cross-Sectional Study. HIV AIDS (Auckl). 2021;13:719–25. pmid:34234573
  90. 90. Kurtay S, Ali KY, Hussein AI. Frequency of cervical premalignant lesions in the gynecologic patients of a tertiary hospital in Mogadishu, Somalia. BMC Womens Health. 2022;22(1):501. pmid:36476212
  91. 91. Lawal I, Agida TE, Offiong RA, Oluwole PO. Cervical cytology among HIV positive and HIV negative women in a tertiary hospital in North Central Nigeria: a comparative study. Annals of Medical and Health Sciences Research. 2017.
  92. 92. Ledaga NA, Woromogo SH, Yagata-Moussa F-E, Mihindou AS, Simo Tekem VN, Kouanang AJ. The epidemiological profile of women screened for precancerous cervical lesions at Benjamin Ngoubou Regional Hospital in Tchibanga, Gabon. Int J Reprod Contracept Obstet Gynecol. 2022;11(3):720.
  93. 93. Lemma TM, Bala ET, Hordofa MA, Solbana LK. Precancerous cervical lesions and associated factors among women on antiretroviral therapy at Dukem Health Center, Central Ethiopia: A cross-sectional study. Health Sci Rep. 2024;7(3):e1972. pmid:38476585
  94. 94. Lemu LG, Woldu BF, Teke NE, Bogale ND, Wondimenew EA. Precancerous Cervical Lesions Among HIV-Infected Women Attending HIV Care and Treatment Clinics in Southwest Ethiopia: A Cross-Sectional Study. Int J Womens Health. 2021;13:297–303. pmid:33688268
  95. 95. Macharia CM. Visual inspection with acetic acid and pap smear findings in HIV positive women attending Mbagathi District Hospital. UON. 2021.
  96. 96. Magaji FA, Mashor MI, Anzaku SA, Hinjari AR, Cosmas NT, Kwaghe BV, et al. Community cervical cancer screening and precancer risk in women living with HIV in Jos Nigeria. BMC Public Health. 2024;24(1):193. pmid:38229083
  97. 97. Makuza JD, Nsanzimana S, Muhimpundu MA, Pace LE, Ntaganira J, Riedel DJ. Prevalence and risk factors for cervical cancer and pre-cancerous lesions in Rwanda. Pan Afr Med J. 2015;22:26. pmid:26664527
  98. 98. Mariko S. Epidemioclinical study of cervical cancer screening by visual tests at the hospital in Mali Bamako. Sch Int J Tradit Complement Med. 2021;4(12).
  99. 99. Mayeri DG, Kahasha PM, Kibalama IB, Mongane J, Louguè M, Birindwa EK, et al. Cervical precancerous and cancerous lesions screening using Pap smear test at Provincial Referral Hospital of Bukavu, Eastern DR Congo: profile and recommendations to stakeholders. Pan Afr Med J. 2024;47:57. pmid:38646136
  100. 100. Mekuria M, Edosa K, Endashaw M, Bala ET, Chaka EE, Deriba BS, et al. Prevalence of Cervical Cancer and Associated Factors Among Women Attended Cervical Cancer Screening Center at Gahandi Memorial Hospital, Ethiopia. Cancer Inform. 2021;20:11769351211068431. pmid:34992337
  101. 101. Merera D, Jima GH. Precancerous Cervical Lesions and Associated Factors Among Women Attending Cervical Screening at Adama Hospital Medical College, Central Ethiopia. Cancer Manag Res. 2021;13:2181–9. pmid:33688261
  102. 102. Kebede HM, Hailay SB, Teklehaymanot HA. Prevalence of precancerous cervical lesion and associated factors among women in North Ethiopia. J Public Health Epidemiol. 2017;9(3):46–50.
  103. 103. Mremi A, Mchome B, Mlay J, Schledermann D, Blaakær J, Rasch V. Performance of HPV testing, Pap smear and VIA in women attending cervical cancer screening in Kilimanjaro region, Northern Tanzania: a cross-sectional study nested in a cohort. BMJ Open. 2022;12(10):e064321. pmid:36316070
  104. 104. Muia MO, Mathenge SG, Njoroge WG, Karuga TK, Mutinda KC. Prevalence and patterns of cervical cytological lesions among HIV-positive women in Machakos County Hospital Kenya. Journal Title. 2023;105(1):1–10.
  105. 105. Mukanyangezi MF, Sengpiel V, Manzi O, Tobin G, Rulisa S, Bienvenu E, et al. Screening for human papillomavirus, cervical cytological abnormalities and associated risk factors in HIV-positive and HIV-negative women in Rwanda. HIV Med. 2018;19(2):152–66. pmid:29210158
  106. 106. Mulugeta Y. Prevalance and associated factors of pre-cancerous cervical lesion among HIV-infected and HIV-uninfected women at health institutions in Bahir Dar City, North West, Ethiopia. 2022.
  107. 107. Musa J, Mehta SD, Achenbach CJ, Evans CT, Jordan N, Magaji FA, et al. HIV and development of epithelial cell abnormalities in women with prior normal cervical cytology in Nigeria. Infect Agent Cancer. 2020;15:50. pmid:32760435
  108. 108. Mutuku OM. Analysis of manual liquid-based cytology, histopathology and HPV DNA testing among HIV-positive women at Machakos Level 5 Hospital, Machakos County, Kenya. Kenyatta University. 2022.
  109. 109. Ngwibete A, Ogunbode O, Swende LT, Agbada MM, Omigbodun A. Prevalence of precancerous lesions and other cervical abnormalities among internally displaced women in Benue State Nigeria. Pan Afr Med J. 2024;47:50. pmid:38681110
  110. 110. Njagi SK, Ngure K, Mwaniki L, Kiptoo M, Mugo NR. Prevalence and correlates of cervical squamous intraepithelial lesions among HIV-infected and uninfected women in Central Kenya. Pan Afr Med J. 2021;39:44. pmid:34422167
  111. 111. Nkfusai NC, Mubah TM, Yankam BM, Tambe TA, Cumber SN. Prevalence of precancerous cervical lesions in women attending Mezam Polyclinic Bamenda, Cameroon. Pan Afr Med J. 2019;32:174. pmid:31303943
  112. 112. Ntuli ST, Maimela E, Skaal L, Mogale M, Lekota P. Abnormal cervical cytology amongst women infected with human immunodeficiency virus in Limpopo province, South Africa. Afr J Prim Health Care Fam Med. 2020;12(1):e1–4. pmid:33054270
  113. 113. Nzang J-L, Ebong CE, Manga S, Manjuh F, Essiben F, Tompeen I, et al. Prevalence of Precancerous Lesions Based on Digital Cervicography with VIA/VILI among Women Positive for High-Risk Human Papillomavirus Serotypes: A Screening Center-Based Study in Cameroon. OJOG. 2024;14(06):967–78.
  114. 114. Oduor MJ. Prevalence of cervical intraepithelial neoplasia among women who screen via/vili positive: are we overtreating with screen and treat approach?. University of Nairobi. 2018.
  115. 115. Okorie OC, Ohidueme OS, Banjo AA. Abnormal cervical epithelial cytology in HIV-seropositive women and correlation with CD4 counts and viral load in Uyo, Akwa Ibom State, Nigeria. Infection. 2018;5:6.
  116. 116. Okunade KS, Badmos KB, Soibi-Harry AP, Garba S-R, Ohazurike EO, Ozonu O, et al. Cervical Epithelial Abnormalities and Associated Factors among HIV-Infected Women in Lagos, Nigeria: A Cytology-Based Study. Acta Cytol. 2023;67(3):248–56. pmid:36516788
  117. 117. Okunowo AA, Ugwu AO, Ajose AO, Kuku JO, Okunowo BO, Ani-Ugwu NK, et al. Pattern and predictors of cervical epithelial cell abnormalities among unscreened and under-screened women in Lagos, Nigeria: a cross-sectional study. Ecancermedicalscience. 2023;17:1504. pmid:37113726
  118. 118. Okwi AL, Wandabwa J, Okoth A, Othieno E. Prevalence of cancerous and pre-malignant lesions of cervical cancer and their association with risk factors as seen among women in the regions of Uganda. 2017.
  119. 119. Omeke CA, Enebe JT, Ugwu AI, Onyishi NT, Omeke MC, Enebe NO, et al. The magnitude and predictors of cervical squamous intraepithelial lesions among women in Enugu, Nigeria: a cross-sectional study of women in a low-resource setting. Pan Afr Med J. 2022;41:130. pmid:35480408
  120. 120. Omoyeni OM, Tsoka-Gwegweni JM. Prevalence of cervical abnormalities among rural women in KwaZulu-Natal, South Africa. Pan Afr Med J. 2022;41:110. pmid:35432696
  121. 121. Oringo J. Prevalence of pre-malignant cervical lesions among HIV-positive women on HAART attending home care clinic at St. Francis hospital Nsambya, Uganda. University of Nairobi. 2020.
  122. 122. Paluku JL, Carter TE, Lee M, Bartels SA. Massive single visit cervical pre-cancer and cancer screening in eastern Democratic Republic of Congo. BMC Womens Health. 2019;19(1):43. pmid:30832697
  123. 123. Rantshabeng PS, Tsima BM, Ndlovu AK, Motlhatlhedi K, Sharma K, Masole CB, et al. High-risk human papillomavirus diversity among indigenous women of western Botswana with normal cervical cytology and dysplasia. BMC Infect Dis. 2024;24(1):1163. pmid:39407130
  124. 124. Siad ISH. The prevalence of cervical cancer and screening in Mogadishu, Somalia. N/A. 2023.
  125. 125. Simo RT, Mbock CV, Kamdje AHN, Nono AGD, Nangue C, Telefo PB, et al. Cervical precancerous lesions and associated factors among women screened in two hospitals in the city of Douala, Cameroon. Cureus. 2023;15(7).
  126. 126. Ssedyabane F, Niyonzima N, Nambi Najjuma J, Birungi A, Atwine R, Tusubira D, et al. Prevalence of cervical intraepithelial lesions and associated factors among women attending a cervical cancer clinic in Western Uganda; results based on Pap smear cytology. SAGE Open Med. 2024;12:20503121241252265. pmid:38764539
  127. 127. Stroetmann CY, Gizaw M, Alemayehu R, Wondimagegnehu A, Rabe F, Santos P, et al. Adherence to Treatment and Follow-Up of Precancerous Cervical Lesions in Ethiopia. Oncologist. 2024;29(5):e655–64. pmid:38394385
  128. 128. Teame H, Addissie A, Ayele W, Hirpa S, Gebremariam A, Gebreheat G, et al. Factors associated with cervical precancerous lesions among women screened for cervical cancer in Addis Ababa, Ethiopia: A case control study. PLoS One. 2018;13(1):e0191506. pmid:29352278
  129. 129. Temesgen K, Gashu A, Dilnessa T, Abate M, Hospital E, Kong H. Proportions of pre-cancerous cervical lesions and its associated factors among women clients in the age group of 30-49 years in gynecology ward of Dessie referral hospital and FGAE, North-East Ethiopia, 2016. 2019.
  130. 130. 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
  131. 131. Temesgen T, Adhena G, Figa Z. Precancerous Cervical Lesion Among Women in Public Hospitals of Addis Ababa, Ethiopia. CRJ. 2020;8(4):94.
  132. 132. Tenkir L, Mamuye A, Jemebere W, Yeheyis T. The magnitude of precancerous cervical lesions and its associated factors among women screened for cervical cancer at a referral center in southern Ethiopia, 2021: a cross-sectional study. Front Glob Womens Health. 2023;4:1187916. pmid:37664421
  133. 133. Tirkaso BH, Bayisa TH, Desta TW. Histopathologic patterns and factors associated with cervical lesions at Jimma Medical Center, Jimma, Southwest Ethiopia: A two-year cross-sectional study. PLoS One. 2024;19(4):e0301559. pmid:38635603
  134. 134. TSO O. Precancerous and cancerous lesions of the cervix in African environments (Healthdistrict of Thecommune 5 of Bamako in Mali). Sch Int J Obstet Gynec. 2021.
  135. 135. Ugboaja JO, Oguejiofor CB, Ogelle OM. Highly active antiretroviral therapy and cervical cytologic abnormalities among women with HIV infection in a limited-resource setting. Int J Gynaecol Obstet. 2018;140(2):228–32. pmid:29080312
  136. 136. Umemmuo MU, Oguntebi E. Trends In Cervical Pap Smear Cytology In A Tertiary Hospital: Implications For Cervical Cancer Screening In Low-Income Countries. pmjg. 2022;8(2):93–100.
  137. 137. Vieira R, Montezuma D, Barbosa C, Macedo Pinto I. Cervical cytology and HPV distribution in Cape Verde: A snapshot of a country taken during its first HPV nation-wide vaccination campaign. Tumour Virus Res. 2024;17:200280. pmid:38621479
  138. 138. Wabo B, Nsagha DS, Nana TN, Assob CJN. Prevalence and risk factors associated with precancerous cervical lesions among women in two cities in Cameroon. Pan Afr Med J. 2022;41:276. pmid:35784594
  139. 139. Wakwoya EB, Gemechu KS. Prevalence of Abnormal Cervical Lesions and Associated Factors Among Women in Harar, Eastern Ethiopia. Cancer Manag Res. 2020;12:12429–37. pmid:33299351
  140. 140. Worku E, Yigizaw G, Admassu R, Mekonnen D, Gessessa W, Tessema Z, et al. Prevalence and risk factors associated with precancerous and cancerous cervical lesions among HIV-infected women in University of Gondar specialized comprehensive referral hospital, Northwest Ethiopia: cross-sectional study design. BMC Womens Health. 2024;24(1):322. pmid:38834999
  141. 141. Woromogo SH, Ambounda Ledaga N, Yagata-Moussa FE, Mihindou AS. Uterine cervical neoplasms mass screening at the University Hospital Centre of Libreville, Gabon: Associated factors with precancerous and cancerous lesions. PLoS One. 2021;16(7):e0255289. pmid:34297784
  142. 142. Zelalem W, Weldegebreal F, Ayele BH, Deressa A, Debella A, Eyeberu A, et al. Precancerous Cervical Lesion Among Adult Women With Human Immune Deficiency Virus on Anti Retroviral Therapy At Saint Peter Specialized Hospital, Ethiopia: A Hospital-Based Cross-Sectional Study. Front Oncol. 2022;12:910915. pmid:35957869
  143. 143. Omoragbon P. Papanicoleau smear usage and prevalence of premalignant cervical lesion among women living with HIV attending a federal teaching hospital in south-west Nigeria: A comparative study. 2017.
  144. 144. Jolly PE, Mthethwa-Hleta S, Padilla LA, Pettis J, Winston S, Akinyemiju TF, et al. Screening, prevalence, and risk factors for cervical lesions among HIV positive and HIV negative women in Swaziland. BMC Public Health. 2017;17(1):218. pmid:28222714
  145. 145. Daniel GO, Musa J, Akindigh TM, Shinku F, Shuaibu SI, Kwaghe B, et al. Prevalence and predictors of precancerous cervical lesions among HIV-positive women in Jos, north-central Nigeria. Int J Gynaecol Obstet. 2020;151(2):253–9. pmid:32683675
  146. 146. Belayneh T, Mitiku H, Weldegebreal F. Precancerous cervical lesion and associated factors among HIV-infected women on ART in Amhara Regional State, Ethiopia: A hospital-based cross-sectional study. Int J Health Sci (Qassim). 2019;13(3):4–9. pmid:31123433
  147. 147. Ferede YA, Tassew WC, Zeleke AM. Precancerous cervical lesion and associated factors among HIV-infected women in Ethiopia: systematic review and meta- analysis. BMC Cancer. 2024;24(1):678. pmid:38831404
  148. 148. AIDS Data book 2021. UNAIDS. https://www.unaids.org/sites/default/files/media_asset/JC3032_AIDS_Data_book_2021_En.pdf. 2021.
  149. 149. Geremew H, Tesfa H, Mengstie MA, Gashu C, Kassa Y, Negash A, et al. The association between HIV infection and precancerous cervical lesion. A systematic review and meta-analysis of case-control studies. Health Sci Rep. 2023;6(8):e1485. pmid:37547356
  150. 150. Sauvaget C, Fayette J-M, Muwonge R, Wesley R, Sankaranarayanan R. Accuracy of visual inspection with acetic acid for cervical cancer screening. Int J Gynaecol Obstet. 2011;113(1):14–24. pmid:21257169
  151. 151. Brevik TB, da Matta Calegari LR, Mosquera Metcalfe I, Laake P, Maza M, Basu P, et al. Training health care providers to administer VIA as a screening test for cervical cancer: a systematic review of essential training components. BMC Med Educ. 2023;23(1):712. pmid:37770904
  152. 152. Maina E, Maingi N, Ongeso A. Effectiveness of Clinical Training in Influencing the Outcome of Visual Inspection with Acetic Acid in Selected Facilities at a County in Kenya. AJHES. 2024;3(2):1–20.
  153. 153. Corral F, Cueva P, Yépez J, Montes E. Limited education as a risk factor in cervical cancer. Bull Pan Am Health Organ. 1996;30(4):322–9. pmid:9041743
  154. 154. Tsehay B, Afework M. Precancerous lesions of the cervix and its determinants among Ethiopian women: Systematic review and meta-analysis. PLoS One. 2020;15(10):e0240353. pmid:33112875
  155. 155. Taye BT, Mihret MS, Muche HA. Risk factors of precancerous cervical lesions: The role of women’s socio-demographic, sexual behavior and body mass index in Amhara region referral hospitals; case-control study. PLoS One. 2021;16(3):e0249218. pmid:33770125
  156. 156. Yu L, Sabatino SA, White MC. Rural-Urban and Racial/Ethnic Disparities in Invasive Cervical Cancer Incidence in the United States, 2010-2014. Prev Chronic Dis. 2019;16:E70.
  157. 157. Mupepi SC, Sampselle CM, Johnson TRB. Knowledge, attitudes, and demographic factors influencing cervical cancer screening behavior of Zimbabwean women. J Womens Health (Larchmt). 2011;20(6):943–52. pmid:21671779
  158. 158. Choi YJ, Park JS. Clinical significance of human papillomavirus genotyping. J Gynecol Oncol. 2016;27(2):e21. pmid:26768784
  159. 159. Bao YP, Li N, Smith JS, Qiao YL. Human papillomavirus type-distribution in the cervix of Chinese women: a meta-analysis. Int J STD AIDS. 2008;19(2):106–11. pmid:18334063
  160. 160. Abebe M, Eshetie S, Tessema B. Prevalence of sexually transmitted infections among cervical cancer suspected women at University of Gondar Comprehensive Specialized Hospital, North-west Ethiopia. BMC Infect Dis. 2021;21(1):378. pmid:33888090
  161. 161. Geremew RA, Agizie BM, Bashaw AA, Seid ME, Yeshanew AG. Prevalence of Selected Sexually Transmitted Infection (STI) and Associated Factors among Symptomatic Patients Attending Gondar Town Hospitals and Health Centers. Ethiop J Health Sci. 2017;27(6):589–600. pmid:29487468
  162. 162. Mekonnen AG, Mittiku YM. Early-onset of sexual activity as a potential risk of cervical cancer in Africa: A review of literature. PLOS Glob Public Health. 2023;3(3):e0000941. pmid:36962975
  163. 163. Jiang Y, Hu SY, Hernandez Donoso L, Li X, Zheng MH, Zhao FH. A Systematic Literature Review on Risk Factors for Cervical Cancer in Chinese Population. Value Health. 2014;17(7):A733-4. pmid:27202622
  164. 164. Tao L, Han L, Li X, Gao Q, Pan L, Wu L, et al. Prevalence and risk factors for cervical neoplasia: a cervical cancer screening program in Beijing. BMC Public Health. 2014;14:1185. pmid:25410572
  165. 165. Rodríguez AC, Schiffman M, Herrero R, Hildesheim A, Bratti C, Sherman ME, et al. Longitudinal study of human papillomavirus persistence and cervical intraepithelial neoplasia grade 2/3: critical role of duration of infection. J Natl Cancer Inst. 2010;102(5):315–24. pmid:20157096
  166. 166. Winer RL, Hughes JP, Feng Q, O’Reilly S, Kiviat NB, Holmes KK, et al. Condom use and the risk of genital human papillomavirus infection in young women. N Engl J Med. 2006;354(25):2645–54. pmid:16790697
  167. 167. Liu G, Sharma M, Tan N, Barnabas RV. HIV-positive women have higher risk of human papilloma virus infection, precancerous lesions, and cervical cancer. AIDS. 2018;32(6):795–808. pmid:29369827
  168. 168. Konopnicki D, Manigart Y, Gilles C, Barlow P, de Marchin J, Feoli F, et al. Sustained viral suppression and higher CD4+ T-cell count reduces the risk of persistent cervical high-risk human papillomavirus infection in HIV-positive women. J Infect Dis. 2013;207(11):1723–9. pmid:23463709
  169. 169. Kelly HA, Sawadogo B, Chikandiwa A, Segondy M, Gilham C, Lompo O, et al. Epidemiology of high-risk human papillomavirus and cervical lesions in African women living with HIV/AIDS: effect of anti-retroviral therapy. AIDS. 2017;31(2):273–85. pmid:27755107
  170. 170. Malevolti MC, Lugo A, Scala M, Gallus S, Gorini G, Lachi A, et al. Dose-risk relationships between cigarette smoking and cervical cancer: a systematic review and meta-analysis. Eur J Cancer Prev. 2023;32(2):171–83. pmid:36440802
  171. 171. Nagelhout G, Ebisch RM, Van Der Hel O, Meerkerk G-J, Magnée T, De Bruijn T, et al. Is smoking an independent risk factor for developing cervical intra-epithelial neoplasia and cervical cancer? A systematic review and meta-analysis. Expert Rev Anticancer Ther. 2021;21(7):781–94. pmid:33663309
  172. 172. Lea JS, Coleman R, Kurien A, Schorge JO, Miller DS, Minna JD, et al. Aberrant p16 methylation is a biomarker for tobacco exposure in cervical squamous cell carcinogenesis. Am J Obstet Gynecol. 2004;190(3):674–9. pmid:15041998
  173. 173. Fonseca-Moutinho JA. Smoking and cervical cancer. ISRN Obstet Gynecol. 2011;2011:847684. pmid:21785734
  174. 174. Xi LF, Koutsky LA, Castle PE, Edelstein ZR, Meyers C, Ho J, et al. Relationship between cigarette smoking and human papilloma virus types 16 and 18 DNA load. Cancer Epidemiol Biomarkers Prev. 2009;18(12):3490–6. pmid:19959700
  175. 175. Asthana S, Busa V, Labani S. Oral contraceptives use and risk of cervical cancer-A systematic review & meta-analysis. Eur J Obstet Gynecol Reprod Biol. 2020;247:163–75. pmid:32114321
  176. 176. Damayanti S, Budihastuti UR, Murti B. Meta-Analysis: Effects of Hormonal Contraceptive Use and History of Sexually Transmitted Disease on the Risk of Cervical Cancer. J Matern Child Health. 2023;8(6):711–22.
  177. 177. Partha Sarathi Mitra, Medhatithi Barman, Pramit Goswami, Jayita Saha, Debjit Saha. Correlation of cervical cancers with long-term use of hormonal oral contraceptive pills - A retrospective observational multicentric study in suburban-based medical colleges in West Bengal. Asian J Med Sci. 2023;14(12):99–105.
  178. 178. Kamani M, Akgor U, Gültekin M. Review of the literature on combined oral contraceptives and cancer. Ecancermedicalscience. 2022;16:1416. pmid:36072240
  179. 179. Bovo AC, Pedrão PG, Guimarães YM, Godoy LR, Resende JCP, Longatto-Filho A, et al. Combined Oral Contraceptive Use and the Risk of Cervical Cancer: Literature Review. Rev Bras Ginecol Obstet. 2023;45(12):e818–24. pmid:38141603