Cervical cancer screening using visual inspection in HIV-positive women at a Nigerian tertiary hospital

¹Department of Family Medicine, Bowen University, Iwo and Bowen University Teaching Hospital, Ogbomoso, Oyo State, Nigerian

^&Corresponding author
Adepeju Olatayo Adegoke, Department of Family Medicine, Bowen University Iwo and Bowen University Teaching Hospital, Ogbomoso, Oyo State, Nigerian

Introduction    

Cervical cancer is a slow-growing cancer that starts in the cervical tissues and can spread to nearby organs, including the uterus and vagina [1]. It results from a chronic or ongoing infection with the human papillomavirus (HPV), a sexually transmitted infection [2]. While the majority of women naturally clear HPV infections, some risk factors can increase the chances of the infection progressing to cervical cancer. These risk factors include early initiation of sexual activity, having multiple sexual partners, high parity, smoking, prolonged use of oral contraceptives, and HIV infection [2,3]. Approximately 1 in 20 cervical cancers globally, and about 1 in 5 in sub-Saharan Africa, are attributable to HIV-associated increases in persistent HPV infection, which is the actual driver of cervical cancer [4]. The high incidence of HPV infection in women living with HIV and the lack of efficient cervical cancer screening programs are the two main causes of the high cervical cancer burden in developing countries like Nigeria [5]. As a result of this increased vulnerability, prompt detection and treatment are essential to reducing the incidence of cervical cancer in this population. In response to global burden of cervical cancer, the World Health Organization (WHO) aims to eradicate cervical cancer by 2030 in women worldwide by vaccinating 90% of girls aged 15 and above against the human papillomavirus (HPV), screening 70% of women in the reproductive age group, and treating and caring for 90% of those who are diagnosed [6]. The WHO also recommends that women between the ages of 30 and 49 be screened for cervical cancer regardless of their HIV status, and that sexually active women living with HIV should undergo screening promptly after diagnosis [7]. This becomes very important because cervical cancer is considered an AIDS-defining illness [3]. In certain countries, cervical cancer screening guidelines are specifically adapted for women living with HIV (WLWH) to account for their increased risk by recommending more frequent screening and discontinuing screening at an older age [3]. Cervical screening is a way of checking women regularly for changes in the cells of the cervix [8].

The different techniques for screening for cervical cancer include colposcopy, HPV DNA testing, visual inspection of the cervix with acetic acid (VIA), and papanicolaou (Pap) smear [5]. Although Pap smears have been effective in lowering the incidence of cervical cancer in high-income countries, their accessibility is limited in low-income countries because it is beyond the capacity of the health services in many of these countries. Some of the challenges include, adequate infrastructure, funding, logistics for follow-up care, availability of appropriate equipment and a shortage of qualified healthcare professionals [9]. In developing countries, visual inspection of the cervix after application of 5% acetic acid (VIA) provides a simple test for the early detection of cervical precancerous lesion and early invasive cancer [10]. Results are available immediately, and in order to prevent multiple patient visits and potential loss of follow-up which is a common challenge in low-resource settings, treatment can be provided at the time of screening [9]. There are many benefits to using a VIA-based screening test over alternative cervical cancer screening methods. It is less expensive, requires minimal skill to perform and interpret, and works best in community-based clinics where sufficient lighting and privacy for examinations can be guaranteed [11]. Therefore, integrating VIA into existing HIV care programs allows for synergistic screening efforts, ensuring that HIV-positive women receive comprehensive reproductive health services in a single healthcare visit. This study aims to determine the prevalence of VIA positivity among women living with HIV receiving care at a tertiary hospital in Southwest Nigeria and to examine its association with sociodemographic, clinical and reproductive characteristics. The findings will contribute to the evidence on cervical cancer screening among women living with HIV in Nigeria and other similar low-resource settings. The study sought to answer the following research questions: i) what is the sociodemographic, clinical and reproductive characteristics of women living with HIV screened for cervical cancer? ii) what is the prevalence of VIA positivity among women living with HIV attending the antiretroviral clinic? ii)is VIA positivity associated with sociodemographic, clinical and reproductive characteristics of these women?

Methods     

Setting: the study was conducted at the Antiretroviral Clinic of Bowen University Teaching Hospital, Ogbomoso, Southwest Nigeria. The hospital is a mission-based private teaching hospital and an APIN-Public Health Initiatives comprehensive site offering HIV prevention, care, and treatment. Free VIA screening and treatment services are routinely offered to eligible HIV-positive women.

Study design: this was a retrospective cross-sectional study conducted between July 2022 and June 2024. All three hundred eligible women screened during the study period were included in the study.

Study participants: the medical records of all 300 eligible sexually active HIV-positive women aged ≥18 years who attended the clinic and underwent VIA screening during the study period were reviewed, and the required information was extracted from their records. All included records had complete data for the variables of interest. Women who were acutely ill, pregnant, or in the puerperium were excluded because these conditions may limit the safety of pelvic examination or affect the interpretation of VIA findings. Women with a previous history of cervical precancerous or cancerous lesions were excluded because they require surveillance rather than routine screening, while women who had undergone total hysterectomy were excluded because the absence of the cervix precludes VIA screening.

Sample size and bias: a sample size calculation was not performed as all the records of the three hundred women screened during the study period were included, thereby ensuring complete capture of available data within the timeframe. To minimize bias, all eligible records available during the study period were included. Data extraction was standardized using a structured proforma to reduce information bias. Selection bias was limited since screening was routinely offered to all HIV-positive women attending the clinic.

Screening and treatment procedures: from the records of all the participants, the VIA screening done involved the application of 5% diluted acetic acid to the cervix and observing for colour changes after one minute. A positive reaction for VIA was the appearance of well-defined, densely opaque white coloration termed acetowhite lesions in the transformation zone or close to the external os. Participants with acetowhite lesions subsequently had thermal ablation done, a procedure where an ablative method uses heat to treat cervical precancerous lesions. The probe is placed on the cervix for about 45-60 seconds to complete the treatment cycle. Participants were screened at first contact and subsequently once in a year.

Variables: the primary outcome variable was the VIA screening result, categorized as positive or negative. Predictor variables extracted included: sociodemographic characteristics (age, religion, occupation, marital status, family type), clinical characteristics (viral load), reproductive characteristics (parity and contraceptive use). The patients≥ occupation was determined using the Standard Occupational Classification System designed by the Office of Population Census and Surveys, London (OPCS 1991) as classes 1, 2, and 3. Class 1 are skilled workers, e.g., professionals and managerial officers, and retirees of this cadre, class 2 are unskilled workers, e.g., artisans and traders; while class 3 are dependents e.g., retirees of class 2, those not on pension, housewives of class 2 cadre, and students whose parents are unskilled workers [12]. Viral load was classified as suppressed (viral load <1000 copies/ml) and unsuppressed (viral load >1000 copies/ml) [13].

Data source and management: data extraction was guided by the study objectives: Information on VIA screening outcomes and participants' sociodemographic, clinical, and reproductive characteristics was extracted from patient folders using a structured data collection proforma. Each participant's data was de-identified and assigned a unique study identification number to ensure confidentiality. Data were entered into SPSS version 26 and double-checked before analysis.

Quantitative variables: data normality was assessed visually using histograms to determine the appropriateness of parametric tests. Normally distributed continuous variables such as age and parity were presented as mean ± standard deviation, while categorical variables such as religion, occupation, marital status, family type, viral load suppression, contraceptive use and VIA result were expressed as frequencies and percentages.

Statistical methods: the study objectives guided statistical analysis. To describe the sociodemographic, clinical and reproductive characteristics of the participants, frequencies and percentages were calculated. To determine the prevalence of VIA positivity among women living with HIV, the numbers and percentages of participants with positive and negative VIA results were calculated. To examine the association between VIA positivity and participant characteristics, Fisher's exact test was used to assess associations between VIA result and categorical variables including religion, occupation, marital status, family type, viral load suppression, and contraceptive use, while an independent-samples t-test was used to compare the mean age and parity of women with positive and negative VIA results. Statistical significance was set at p <0.05. No multivariable analysis was performed because the small number of VIA-positive cases limited the statistical power to obtain reliable adjusted estimates.

Ethical consideration: ethical approval was obtained from the Research and Ethics Committee of Bowen University Teaching Hospital, Ogbomoso, with Approval Number: BUTH/REC-2206 before the commencement of this research. Anonymity and confidentiality of reports was ensured by de-identifying each participant and using a unique identification number for data generated.

Results     

Participants' characteristics: Table 1 presents the sociodemographic, clinical, and reproductive characteristics of the 300 women living with HIV included in the study. Participants were predominantly aged 40-49 years (33.7%), Christians (72.3%), engaged in unskilled occupations (94.0%), and married (86.0%). Most women belonged to monogamous families (69.0%), had suppressed viral loads (<1000 copies/mL) (94.0%), had 1-4 children (62.6%), and were not using contraception (66.0%).

Visual inspection with acetic acid positivity among women living with HIV: Table 2 presents the VIA screening results. Overall, 9 of the 300 women screened were VIA-positive, giving a prevalence of 3.0%, while 291 (97.0%) had negative VIA results.

Association between sociodemographic, clinical and reproductive characteristics, and VIA positivity of the study participants: Table 3 presents the association between sociodemographic, clinical and reproductive characteristics, and VIA positivity of the study participants. There was no statistically significant difference between the mean age of participants with a positive and negative VIA results (39.78 ± 9.60 vs 44.51± 10.76 years, t = -1.302, p = 0.194). Similarly, there was no statistically significant difference between the mean parity of participants with a positive and a negative VIA result (3.22± 1.2 vs 3.37 ± 2.06, t = -0.216, p = 0.829). Among the categorical variables examined, marital status was the only factor significantly associated with VIA positivity (p=0.049). No significant associations were observed for religion, occupation, family type, or clinical and reproductive characteristics of the study participant.

Discussion     

This study determined the prevalence of VIA positivity among women living with HIV receiving care at a tertiary hospital in Southwest Nigeria and examined its association with sociodemographic, clinical, and reproductive characteristics. The mean age of women living with HIV (WLWH) in this study was 44.4 ± 10.8 years, indicating that the study population largely comprised middle-aged women. This finding is higher than the mean ages reported among HIV-positive women in Uganda, Ethiopia, and Eswatini [1,4,14]. The older age observed in the present study could reflect differences in the demographic characteristics of women enrolled in HIV care and the increasing life expectancy of people living with HIV following widespread access to effective antiretroviral therapy. Nevertheless, the age distribution remains consistent with the population targeted for cervical cancer screening. Most of the study participants were Christians, reflecting the religious composition of the study setting. Similar findings have been reported in Uganda [15] whereas studies conducted in predominantly Muslim populations have reported a higher proportion of Muslim participants [6,16]. Most participants were engaged in unskilled occupations, likely reflecting the socioeconomic characteristics of women accessing HIV care at the study site. Comparable data from similar studies are limited. The majority of the participants were married, which may reflect greater engagement with reproductive and maternal health services. This is considerably higher than rates reported in Southeast and South-south Nigeria [5,17]. However, a study done in Urban Uganda [1] found that most of the study participants were separated or widowed. Most participants in this study belonged to monogamous families. Comparative evidence on family type among women living with HIV undergoing cervical cancer screening is limited.

The present study found that 94.0% of participants had suppressed viral load, reflecting successful HIV treatment outcomes among women receiving care at the study site. This proportion is comparable to the 92.0% viral suppression reported among women living with HIV in Malawi [18] and is slightly higher than the 84.8% reported in studies from Calabar, Nigeria [13], and Eswatini [4]. The high level of viral suppression observed in this study may reflect effective HIV treatment services, sustained engagement in care, and access to potent antiretroviral therapy within the study setting. Differences between studies may be attributable to variations in study populations, healthcare delivery systems, ART program performance, and the timing of viral load assessment. Most of the participants had 1-4 children. Similar patterns have been reported in Nigeria and other sub-Saharan African countries [5,6,19]. Contraceptive use in this study was relatively low, with only 34.0% reporting current use. This may reflect that many participants were peri- or post-menopausal. Lower contraceptive use has also been reported in Nigeria, [10] whereas higher rates have been reported in Uganda [1,15]. This is likely because most of the study participants in those studies were younger. This study found a VIA positivity rate of 3.0%. This prevalence is lower than the 7.1% reported in a multicenter Nigerian study by Ogunsola et al.[11] and the 15% reported from a community outreach program in Rivers State, Nigeria [17]. The lower VIA positivity observed in the present study may reflect differences in study setting, participant characteristics, and screening methods. Unlike the community-based study in Rivers State, screening in our study was integrated into routine HIV care within a tertiary hospital, and it relied solely on VIA, whereas the study in Rivers State used both VIA and visual inspection with Lugol's iodine (VILI).

Internationally, VIA positivity rates among women living with HIV have varied considerably. A lower prevalence of 2.6% was reported in Eswatini [4], whereas substantially higher rates of 24.5% in Ethiopia [20] and 38% in the Democratic Republic of Congo [21] have been reported. These differences are likely attributable to variations in participant recruitment, previous screening history, healthcare access, community awareness initiatives, and screening practices. For example, the Ethiopian study enrolled women who had never previously been screened, while the study in Democratic Republic of Congo followed extensive community awareness campaigns that may have encouraged women with previously undetected cervical lesions to present for screening. Regardless of the prevalence observed, continued integration of cervical cancer screening into routine HIV care remains essential to facilitate early detection and treatment of cervical precancerous lesions among women living with HIV. In this study, VIA positivity was found to be significantly associated with marital status, while age, religion, occupation, family type, and clinical and reproductive characteristics were not significantly associated with VIA positivity. The significant association observed with marital status may reflect differences in sexual behavior, duration of sexual exposure, and biological factors among the different marital groups. However, this finding should be interpreted with caution because of the small number of VIA-positive cases in the present study.

In contrast to this finding, Odafe et al. [22] reported no statistically significant association between marital status and VIA positivity among women living with HIV in Abuja, Nigeria, suggesting that this relationship may vary across study populations. The absence of significant associations with occupation and religion in the present study may reflect that these factors are more likely to influence healthcare access and screening uptake than the biological processes underlying cervical dysplasia. Although viral load was not significantly associated with VIA positivity in the present study, women with unsuppressed viral load tended to have a higher frequency of VIA positivity than those with suppressed viral load. This finding is consistent with previous reports. Mapaona et al. [4] demonstrated that an undetectable viral load was independently associated with substantially lower odds of VIA positivity compared with unsuppressed viral load. Biologically, uncontrolled HIV replication results in greater immune dysfunction, reducing the body's ability to clear HPV infection and thereby promoting persistence of high-risk HPV and progression to cervical dysplasia. The lack of statistical significance in the present study is likely attributable to the small number of VIA-positive cases, which substantially limited statistical power compared with larger studies such as that of Mapaona et al. [4]. Neither family type nor reproductive characteristics was significantly associated with VIA positivity. Although polygamous family structures may theoretically increase HPV exposure, this was not supported by our findings. These results suggest that among women living with HIV, cervical dysplasia may be more strongly influenced by persistent HPV infection and immune status rather than by family type or reproductive characteristics.

Strength: inclusion of all eligible women screened during the study period minimized selection bias and enhanced the representativeness of the study population.

Limitations: the statistical power is limited because of the small number of positive cases; ii) other key confounding factors, such as HPV infection status and smoking history, were not recorded or accounted for in the analysis. Consequently, we cannot rule out the potential influence of these variables on our findings.

Generalizability: the findings are most applicable to HIV-positive women accessing care in similar tertiary and mission-based hospitals in Nigeria and comparable low-resource settings. However, caution is required when generalizing to community-based populations or regions with lower ART coverage

Conclusion     

This study found a VIA positivity rate of 3.0% among women living with HIV receiving care at a Nigerian tertiary hospital. Marital status was the only participant characteristic significantly associated with VIA positivity. Although the observed VIA positivity rate was lower than that reported in several comparable studies, differences in study populations, settings and screening practices may account for this variation. Continued integration of cervical cancer screening into routine HIV care remains essential to facilitate early detection and treatment of cervical precancerous lesions among women living with HIV.

Competing interests     

The author declare no competing interests.

Authors' contributions     

Adepeju Olatayo Adegoke: study conception, design and manuscript drafting. Stephen Adesope Adesina, Isaac Olusayo Amole: ata analysis and revision of manuscript. All authors: literature review, data interpretation and final approval of the manuscript. They have read and approved the final version of this manuscript.

Acknowledgments     

We appreciate the efforts of our staff nurses (Mrs O B Ogunlowo, Mrs E. O. Adetutu and Miss T. Bamidele) for their assistance in screening and data extraction. The authors used AI tools to assist with language editing and sentence-structure refinement in parts of this manuscript. AI was not used to generate, analyze, or interpret study data or results. All outputs were reviewed and verified by the authors, who take full responsibility for the manuscript's content.

Tables      

Table 1: sociodemographic characteristics, clinical and reproductive characteristics of the study participants. (n=300)

Table 2: visual inspection with acetic acid positivity among women living with HIV

Table 3: association between sociodemographic, clinical and reproductive characteristics, and VIA positivity of the study participants

References