Cervical cancer screening for PLWHIV; experiences from an innovative cervical screening and treatment program in Nigeria

doi:10.21203/rs.3.rs-2485721/v1

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Cervical cancer screening for PLWHIV; experiences from an innovative cervical screening and treatment program in Nigeria

https://doi.org/10.21203/rs.3.rs-2485721/v1

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We evaluated cervical cancer program for women living with HIV (WLHIV) to determine program screening rate, primary case finder screening accuracy and treatment and post-treatment screening rate among screen-positive patients.

Methods

A one-year review of cervical cancer program data among WLHIV aged 15-49 years on HIV care across forty-one comprehensive ART sites supported by APIN (a PEPFAR implementing partner) in Nigeria was conducted from October 2020 to July 2021. Initial screening was done using visual inspection with acetic acid (VIA) followed by a gynaecologist expert review through a program-designed software named AVIVA, as a confirmatory test. Associations were measured between the primary case finder screening accuracy and study covariates at p-value of 0.05.

Results

About 10,289 asymptomatic women aged 15-49 years living with HIV were screened for cervical cancer by primary case finders using VIA-based screening test. 732 (7.1%) had a positive screening test suggestive of precancerous lesions or cervical cancer. 315 (43.0%) of VIA positive women had treatment using thermal ablation and less than one-third (21.6%) of those treated came back for post-treatment screening test. Primary case finder screening sensitivity, specificity, positive predictive and negative predictive accuracy using gynaecologist review as confirmatory test were 60.8%, 71.5%, 41.7% and 84.5% respectively. Overall screening accuracy was 68.8%.

Conclusion and Recommendation

This innovative approach to cervical cancer screening among WLHIV yielded modest results in preventing program error and wastages. Wider deployment of expert-based reviews of VIA though AVIVA software might be a veritable approach to improve screening accuracy in low resource settings.

Cervical cancer screening

WLHIV

Nigeria

Globally, cervical cancer ranks fourth among the common cancers affecting women. In 2018, over half a million women were diagnosed with cervical cancer worldwide and almost half of them died from the disease.[1] Cervical cancer remains the leading cause of cancer-related deaths among women in low resource countries especially in eastern, western, middle, and southern Africa[1].The disease burden is higher in HIV infected population, with a six-fold increased risk of cervical cancer in HIV positive women when compared to women without HIV[2]. This higher risk is manifested throughout the lifecycle starting with an increased risk of acquiring human papilloma virus infection, serotype 16 and 18, an organism that has been implicated in the occurrence of 70 - 75% of all cervical cancer cases worldwide[2,3]. The higher the HIV prevalence, the higher the occurrence of cervical cancer attributable to HIV infection, underscoring the major contribution of HIV epidemics to cervical cancer in Sub-Saharan Africa[2].

In Nigeria, one of the Sub-Saharan Africa countries with HIV epidemics, cervical cancer ranks as the second most prevalent cancer amongst women of reproductive age after breast cancer[4,5]. As at 2019, 14, 943 new cases of cervical cancer occurred amongt women per year with a case fatality rate of 70%[6] in the country. HPV infection remains the most implicated causative organism for cervical cancer in Nigeria with prevalence of 66.9% among cervical cancer patients⁶. Estimates of HPV infection among sexually active women across states in Nigeria ranged from 76% in Kano, 48.1% in Gombe state to a lower prevalence of 19.6% and 26.3% in Lagos and Oyo state respectively[7–9]. Studies have reported higher prevalence of high risk HPV and cervical precancerous lesion of 19.6% and 6.0% respectively among women living with HIV in Nigeria compared to their HIV negative colleagues, with HPV 16 being the most implicated serotype[8]. In 2013, the World Health Organization (WHO) launched the three level prevention strategies for the control of cervical cancer with focus on HPV vaccination for children between ages of 9-13 years, early detection through screening for pre-cancer changes in the cervix and treatment of invasive cervical cancer[10]. They went further to propose 'a screen and treat' approach to prevention for resource poor settings which uses the low-cost technology of visual inspection with acetic acid (VIA) followed by cryotherapy. This was in accordance with the earlier adopted strategy by Nigeria Federal Ministry of Health (FMOH) cancer control plan of 2008, which recognised cervical cancer screening with visual inspection with acetic acid or lugol iodine, and cryotherapy treatment of precancerous lesions[11].

VIA-based screening test has several advantages over other cervical cancer screening tests. It is less expensive, require less expertise in conducting and interpreting, and very suitable for community-based clinics wherever privacy for examination and availability of good light source can be ensured. However, some studies have demonstrated wide variation in the reliability of VIA in detecting pre-malignant cervical lesions[12–14]. A meta-analytic study that pooled data from studies conducted among asymptomatic population, and using colposcopy and histologic testing as confirmatory reported high sensitivity and specificity for VIA-based tests with a pooled sensitivity rate of 80% and specificity rate of 92%, and showed no significant differences in testing accuracy in relation to the category of health care worker who conducted the screening[14]. Vahedpoor et al[15] reported higher sensitivity and specificity rate for VIA based test in India, with a lower false negative rate of 4.6% and false positive rate of 21.2% in relation to Pap Smear. On the contrary, Gravitt et al[13] in India reported very low sensitivity rate for VIA based test compared to HPV testing and cytology. VIA screening was only able to identify 31.6% of screened women who were confirmed to have precancerous lesion using histology compared to HPV testing (100%) and pap cytology (78.2%), although the VIA specificity still remained high (87.5%)[13].

Common to all these studies was the reported low positive predictive value of VIA based test[13,16–18]. A significant proportion of women who test positive to VIA may not have the disease, thereby resulting in misdiagnosis, excessive treatment and unwarranted anxiety among individuals tested. Other major concerns with VIA test include the subjective nature, which makes interpretation different from one health care provider, the unavailability of a permanent test record for possible future review and its limited reliability for screening among postmenopausal women whose cervical region have likely undergone transformation[19].

In improving VIA based screening test accuracy and ameliorating the accompanying social and economic implication of misdiagnosis due to the low positive predictive value of the test, APIN introduced multiple level of reviews of VIA cervix stained images using APIN developed software named AVIVA. AVIVA is a lightweight android mobile application designed using googles’ frontline programming language Angular version 11 and packaged for mobile deployment using Ionic and running on the Apache Cordova mobile application development framework. The framework implements several key services that enhances the VIA screening service both for the case finder and the specialist reviewer. It utilizes services like the HTTP API (Application Programming Interface) that runs a real-time handshake with a cloud-based data warehouse system for the storage of all captured images and analytics to ascertain the level of concurrence between case finder diagnosis and reviewer diagnosis, tracks the progress of the case finder in bridging the concurrence gap and displays performance at case finder, facility, state and program levels respectively. A notification service for real time alerts and a feedback mechanism for case finders when their findings have been reviewed are implemented using the application and SMS. The AVIVA software application is downloadable online via APIN configured URL and installed on android smart phones, preferably smart phones with high camera quality. The case finder makes the first diagnosis via tying up the findings from a direct visual inspection of the native, acetic and lugol iodine stained cervix respectively. In the course of making the baseline diagnosis, she takes serial, clear and well-illuminated three images of the native cervix, acetic and lugol iodine stained cervix respectively and uploads on the AVIVA. Mainly positive VIA test results or cases in doubt is expected to be uploaded on the AVIVA app. Then designated gynecologists, who also have access to the pictures, is prompted by a notification sound that beeps every 5 minutes to provide expert review. Same notification is sent to the APIN State and central cervical cancer focal persons who also call the attention of the expert reviewer on the uploaded cases. On review, the expert reviewer proffers the necessary treatment modalities based on observed findings. The case finder within minutes receives the feedbacks and adequately attend to the client still on the couch.

This study aimed at estimating (1) the prevalence and treatment outcome of precancerous lesion in APIN cervical cancer screening and treatment program, (2) the case finder screening sensitivity, specificity, positive and negative predictive value, (3) factors associated with case finder screening accuracy, and (4) the case finder screening error rate that could be prevented by using sequential expert gynaecologist agreement as a confirmatory test before treatment.

Study design and setting: A review of cervical cancer screening and treatment program data of women of reproductive age living with HIV in 41 comprehensive ART sites (3 Primary Health Facilities, 25 Secondary Health Facilities, 13 Tertiary Health Facilities) in 7 APIN supported states in Nigeria (Benue, Plateau, Ondo, Ekiti, Oyo, Osun and Ogun states), within a one (1) year period. APIN is one of PEPFAR funded non-governmental organizations in Nigeria responsible for the provision of prevention, care and treatment services to patients with HIV/AIDS. APIN has data for more than 1 million patients with over 340,000 currently enrolled in her ART care program in eight states and in over 4400 supported health facilities. A comprehensive site in APIN program is either a secondary level or tertiary level health facility. These facilities serve as a referral center for provision of secondary or tertiary care for most primary and secondary level health facilities. The HIV clinic in the comprehensive sites provides ART services to paediatric, non-pregnant adult clients and PMTCT services to pregnant ART clients. It has different sub-units including adherence counselling unit, consulting rooms, records, phlebotomy unit, patient waiting room and data room for electronic medical records (EMR) operations. Most of the facilities open every weekday and operate block appointment for cohort of patients with similar attributes.

Procedure: Furthermore, in assessing cervical cancer screening accuracy, a one-year review of the piloted electronic VIA cervical images of women who received HIV care from 16 selected comprehensive care sites) was conducted across 3 administrative regions in Nigeria; Plateau region, Oyo region (Osun and Oyo states) and Ondo region (Ondo and Ekiti states). These images were taken by primary case finders (community health extension workers and Nurses) across APIN Public Health Initiatives (APIN) supported health facilities, uploaded to a software (named AVIVA) developed by the organization and were subsequently reviewed by corresponding expert gynaecologists. One primary case finder each was selected from the sixteen comprehensive sites for HIV care in the administrative regions. The selected comprehensive sites comprised of 9 secondary health facilities (SHFs) and 6 tertiary health facilities (THFs). The primary case finders in this study were mandated to conduct cervical cancer screening for all consenting women living with HIV aged at least 15 years and enrolled in ART care, using the visual inspection with acetic acid (VIA) screening method, and upload all positive VIA cases and 10% of all negative VIA cases to the APIN AVIVA software for expert gynaecologists review and concurrence. A total of 7 trained gynaecologists were engaged on the project, 1 per state, to do daily review of case finder’s uploads and post comments in agreement or disagreement with case finder diagnosis. Following agreement of positive results of precancerous lesion by reviewer, the cases are scheduled for immediate thermal ablation and 6 months post treatment screening to confirm treatment success in them. The details of this process are included in Figure 1

A total of 295 cervical visual images were uploaded by primary case finders for gynaecologist review over the 1-year period; 187 negative images and 108 positive images. Positive VIA test result was defined as the presence of acetowhite lesions in the transformation zone, near the squamocolumnar junction or the os of the cervix, 1 minute after the direct application of a 3% to 5% diluted solution of acetic acid, while absence of this is termed as negative result.

Study variables: The primary case finder assessment is considered as the primary screening test while the AVIVA reviewers’ comments are considered as a confirmatory test. The numbers of each combination of results—true positive (TP; positive results to both VIA and confirmatory testing), false positive (FP; positive VIA result but negative result to confirmatory testing), false negative (FN; negative VIA result but positive result to confirmatory testing), and true negative (TN; negative result to both VIA and confirmatory testing) were extracted from the study, and the following 4 parameters of accuracy and performance for VIA were estimated:

Data Analysis: Data were entered into an Excel spreadsheet (Microsoft), cleaned and analyzed using SPSS IBM version 20. Data were presented using tables and charts. T-test analysis was utilized to examine association between covariates and case finder cervical VIA screening accuracy rate. Covariates examined were region, state, facility level of care.

Ethical approval: Ethical approval was obtained from APIN research institution board.

Ten thousand, two hundred and fifty-nine (10259) asymptomatic women aged 15-49 years living with HIV were screened for cervical cancer by primary case finders across 41 health facilities in 7 APIN supported states in Nigeria, using VIA based screening test from October 2020 to July 2021. About 732 (7.1%) had a positive screening test suggestive of a precancerous lesion or cervical cancer . More women were positive in Northern region (7.7%), Plateau state (15.8%) and tertiary health facilities (11.7%), when compared to Southern region, other states and level of health care Table 1.

Table 1 Primary Case Finder Cervical Cancer Screening Outcome by Facility Characteristics

Variable (s)		Case Finder VIA screening test Outcome		Total
		Positive (n = 732)	Negative (9527)
		Freq (%)	Freq (%)
Region
	North	565 (7.7)	6764 (92.3)	7329
	South	167 (5.7)	2763 (94.3)	2930
State
	Benue	150 (3.2)	4558 (96.8)	4708
	Plateau	415 (15.8)	2206 (84.2)	2621
	Ekiti	4 (1.3)	307 (98.7)	311
	Oyo	123 (9.3)	1203 (90.7)	1326
	Osun	2 (0.7)	299 (99.3)	301
	Ondo	38 (8.7)	400 (91.3)	438
	Ogun	0 (0.0)	554 (100.0)	0
Level of Care
	Primary	0 (0.0)	41 (100.0)	41
	Secondary	239 (4.0)	5751 (96.0)	5990
	Tertiary	493 (11.7)	3735 (88.3)	4228

The overall treatment rate and retention using thermal ablation therapy across the states were below average as only 315 (43.0%) patients identified with precancerous lesion had thermal ablation therapy and less than one-third (21.6%) of those who had treatment returned back for post treatment screening Table 2.

Table 2 Summary of treatment history for positive VIA clients

PLHIV who had positive test outcome	VIA Positive patients treated who had thermal ablation therapy	Treated patients who returned for 6 months post treatment screening
Number	Freq (%)	Freq (%)
732	315 (43.0)	68 (21.6)

Furthermore, two hundred and ninety-seven (297) cervical visual images stained with acetic acid (VIA reports) of women living with HIV age 15 years and above in 16 health facilities across the 5 APIN supported states were uploaded for expert gynaecologists’ review using AVIVA software from October 2020 to July 2021. Majority of the uploads were from Northern Region, 215 (72.9%), Plateau states 215 (72.9%), and SHFs, 269 (91.2%) Table 3.

Table 3. Background Characteristics of VIA images uploaded.

Variable (s)		Frequency	Percent
Region
	Northern	215	72.9
	Southern	80	27.1
	Total	295	100.0
APIN Administrative regions
	Plateau Region	215	72.9
	Oyo Region (Osun and Oyo)	69	23.4
	Ondo Region (Ondo and Ekiti)	11	3.7
	Total	295	100.0
Level of Care
	Secondary	269	91.2
	Tertiary	26	8.8
	Total	295	100.0

Forty-five out of the 108 positive cases identified by case finders VIA test were truly positive, resulting in a positive predictive rate (PPV) of 41.7%, while about 158 out of 187 negative cases identified by case finders were truly negative, giving a negative predictive value (NPV) of 84.5%. The case finder VIA screening test sensitivity and specificity rates were 60.8% and 71.5% respectively. The expert review through AVIVA software was able to prevent type 1 error (False positivity error) among 63 positives (28.5%) and type 2 error (False negative error) among 29 negatives (39.1%) Table 4.

Table 4. Comparison of case finder screening to AVIVA expert reviewers’ confirmation

Variable (s)		AVIVA Reviewer's Report			Predictive Value (%)
		Negative	Positive	Total
		Freq (%)	Freq (%)	Total
Case Finder CIN screening results using VIA
	Negative	158 (84.5)	29 (15.5)	187	NPV = 84.5
	Positive	63 (58.3)	45 (41.7)	108	PPV = 41.7
	Total	221 (74.9)	74 (25.1)	295
Accuracy (%)		Specificity = 71.5	Sensitivity = 60.8

Overall accuracy of case finder screening test = TN+TP/Overall total, = 68.8%

Case finders in the northern region had higher overall mean screening test accuracy rate (74.8) compared to those in Southern region (27.4) (p = 0.03). Similarly, case finders in Plateau (74.8) and Ondo state (70.8) had higher mean screening test accuracy rate compared to those in Oyo state (17.7) (p = 0.01) Table 5.

Table 5 Factors associated with the accuracy of case finder VIA screening.

Variable (s)		N	Mean	Std. Deviation	F or t-statistics	df	P value
Geographical Region
	Southern	11	27.4	33.7	-2.51	14	0.03*
	Northern	5	74.8	38.2	-2.51	14	0.03*
Facility level of care
	Secondary	11	42.2	44.1	< 0.01	14	1.00
	Tertiary	5	42.1	37.0	< 0.01	14	1.00
APIN administrative region
	Plateau	5	74.8	38.2	6.37	2	0.01*
	Oyo	9	17.7	29.0
	Ondo	2	70.8	5.9

Cervical cancer screening using VIA-based tests aim to save lives through early detection and treatment of precancerous cervical lesions. This study provides evidence to project the achievements and innovations adopted by APIN in its cervical cancer control program among WLHIV. According to the result of our study, the primary case finder screening strategy using VIA-test indicated a prevalence of 7.1% precancerous or cervical cancer lesions among WLHIV, approximately 710 cases per 10,000 population. Our finding compares with a previous study conducted in Nigeria Federal Capital Territory, where prevalence of precancer or cervical cancer lesions was estimated as 6.0%using visual inspection with acetic acid (VIA) screening test²¹. However, the it was far lower than prevalence of cervical intraepithelial lesions reported by two other studies done in Enugu and Jos, where estimated prevalence were put at 12.6% and 29.0% respectively. Of note was that these two studies adopted cytology-based testing approach which is a more effective, albeit expensive, screening test[20,21]. Many studies also reported higher prevalence of cervical precancerous lesion among HIV positive women compared with HIV negative women in Nigeria.

Our study also showed low retention along the cervical cancer continuum of care. Overall, out of 732 WLHIV diagnosed with precancerous lesions 43.0% (315) had thermal ablation therapy while less than 40% came back for post treatment screening. Reasons for poor adherence to treatment and screening schedules remain unknown consequently, this requires further investigation but could include additional cost of transportation to facilities for retesting[22]

In this study, we also reported geographical variation in cervical cancer among WLHIV. This suggests a much higher risk of developing cervical cancer in northern Nigeria compare to southern part of the country. Although 72.9% of the samples uploaded were cases from Northern part of Nigeria which may explain why there was a higher positive screening test result from Northern Nigeria. Nevertheless, understanding the risk factors and reasons behind geographical disparities is critical to defining priority areas for cervical cancer prevention efforts and targeting women who are most likely to be at risk. Our findings also compares with similar studies reported by Marie-Josèphe et al[23], where geographical and racial/ethnic variation were identified and reported in cervical cancer incidence and mortality in United States[23].

The study went further to examine the predictive ability and accuracy of the primary case finder VIA imaging using APIN’s developed AVIVA technology as confirmatory test. Sensitivity, specificity, positive and negative predictive values were calculated to be 60.8, 71.5, 41.7 and 84.5 respectively. The confirmatory test suggests that 15% of WLHIV who received VIA negative results could have received a false-negative screening result if they were tested alone with VIA. Conversely, 58.3% of WLHIV who received VIA positive results could have received a false-positive screening result if tested alone with VIA while 41.7% tested positive to both VIA and AVIVA confirmatory testing. Other studies that have adopted VIA screening tests reported similar findings regarding the low sensitivity and PPV but higher specificity and NPV of VIA test results[24,25].

Another significant finding in our study revealed 58.3% false-positives following AVIVA confirmatory tests demonstrating the need for further testing to confirm the presence or absence of cervical cancer. These false positives possibly could be attributable to confounding factors or errors during testing and interpretation by primary case finders during VIA screening tests. However, APIN’s AVIVA technology was critical in avoiding over-diagnosis furthermore, such outcome (false positives) following confirmatory test using AVIVA could pave new ways to improve performance and accuracy of VIA based screening program at all APIN’s cervical screening facilities.
In this study, we observed comparable case finder VIA screening accuracy among case finders in secondary health facilities when compared to their counterparts in tertiary facilities. Although the case finder screening accuracy was observed to be low (<43%) across both levels of healthcare, this finding suggests that VIA screening can be performed by competent healthcare providers at all levels of healthcare when properly equipped with necessary training. VIA test is recommended for use in low resource settings like our study location[26,27]. In Nigeria, secondary and tertiary health facilities may not be easily accessible to clients eligible for specific healthcare services[28], including HPV screening test services. Thus, availability of competent HPV case finders across all levels of healthcare is necessary in addressing cervical cancer control in the country. Although, there is also a need to ensure second level review of screening test results in these facilities, considering the low PPV of VIA test results observed in this study. Studies have shown comparable accuracy in the screening test results among different cadres of healthcare workers[29,30].

According to various studies conducted in Nigeria, evidence exists that the prevalence of HPV infection is higher in the northern part of the country when compared to the southern region of the country[7,31–33]. The prevalence of a disease condition affects the diagnostic accuracy of screening tests[34]. The lower VIA test accuracy observed among case finders in the southern region compared to their northern counterparts could be influenced by the lower prevalence of HPV infection in the region. The knowledge of the prevalence of a disease condition could influence reader expectation of a screening test result and hence, its accuracy[34]. A major limitation of the study is the use of only one expert reviewer to review VIA images for each screening test. Generally, the subjective nature of VIA affects its validity as interpretation of test results could be different from one health care provider[19]. However in this study, expert gynaecologists were engaged as reviewers and therefore, we believe their reviews were largely representative of the nature of the cervical region of the clients enrolled in this study. In addition, we did not collect information about the age of our participants. VIA tests have been reported to be less effective for use as a screening test among postmenopausal women whose cervical region have likely undergone transformation[19]. Significant age difference may exist among the clients enrolled across region and facility level of care, thereby influencing our screening test result and accuracy.

Future studies to assess the yield and reliability of VIA in relation to the social and biological characteristics of WLHIV are appropriate. Also, implementation science research through the use of some innovative approaches in improving the reliability of VIA is required. Such approaches may entail randomised clinical trials which will employ a combination of cytology, histology and expert review of VIA images by histopathologists among others.

In conclusion, the innovative approach to cervical cancer screening (AVIVA) adopted by APIN in its cervical cancer control program among WLHIV appears to have yielded modest results in terms of its reliability and feasibility. The “AVIVA model” may be a veritable tool for cervical screening in low resource settings if the health workers (case finders) who perform visual inspection with Acetic acid can be further trained to ensure optimal standards. In addition, the integration of cervical cancer screening program into existing ART programs as demonstrated in this study is feasible, practicable and realistic and this is recommended as a standard of care for all eligible WLHIV who are accessing care at any comprehensive ART site.

There is the need to establish a cervical cancer awareness and education program for WLHIV as part of comprehensive ART services, so that they are readily motivated to uptake cancer screening services as required. Also, a special counselling and follow up program is recommended for persons who get screened for cervical cancer so as to reduce loss to follow and default from treatment for precancerous lesions. We recommend that an appropriate policy framework for cervical cancer screening as part of routine care for WLHIV should be provided to ensure that such screening programs are institutionalized and sustainable.

Acknowledgments: The authors would like to appreciate our ART staff at all the sites used for this study for their cooperation and dedication in providing the study data. Our appreciation also goes to the expert gynaecologists who participated in the study.

Authors' contributions: Olabanjo Okunlola Ogunsola , Oluseye Ajayi and Prosper Okonkwo conceptualized the study, Olabanjo Okunlola Ogunsola , Oluseye Ajayi, Yewande Akinro, Kucheli Wudiri , Emmanuel Osayi , Babatunde Amoo , Rita Ayoka-Ikechukwu , Chukwuemeka Ifechelobi were involved in the data collection process. Oluseye Ajayi, Temitope Ojo and Olumeyan Olufemi were involved in the data analysis and interpretation. All authors contributed to writing the draft of the manuscript. All the authors have read and agreed to the final manuscript.Funding: The authors did not receive any funding for this study

Data Availability: The survey data is available upon reasonable request.

Competing interests: The authors have no financial or nonfinancial interests to disclose.

Ethical approval: The project was approved by the Institutional Review Boards (IRB) of APIN, Nigeria

Informed Consent: We obtained a written informed consent from all clients who participated in the study.

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No competing interests reported.

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Cervical cancer screening for PLWHIV; experiences from an innovative cervical screening and treatment program in Nigeria

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