Utility of colposcopy for the screening and management of cervical cancer in Africa: a cross-sectional analysis of providers’ training and practices

Introduction: Cervical cancer is a public health issue in Africa with devastating socioeconomic consequences due to the lack of organized screening programs. The success of screening programs depends on the appropriate investigation and management of women who test positive for screening. Colposcopic assessment following positive screening results is a noteworthy issue in Africa. This study aimed to assess the utilization of colposcopy by providers in the region. Methods: A cross-sectional study was conducted in 2021-2022 among healthcare providers involved in cervical cancer prevention activities in Africa. They were invited to report prior colposcopy training, whether they performed colposcopy and the indications of colposcopy in their practice. Results: Of the 130 providers from 23 African countries who responded to the survey (mean age [SD]: 39.0 years [9.4]), half were female (65 [50.0%]), and 90.7% were working in urban areas. Overall, only 12.6% of respondents indicated having received prior training on colposcopy, and 11.7% reported that they were performing colposcopy in their current practice. Among the providers who reported performing colposcopy in their practice, colposcopy was indicated for routine visual screening in 21.2% of clinicians, to visualize the transformation zone in 15.2% of respondents, to assess vascularization of cervical mucosa in 33.3% of respondents, and to determine treatment modality in 12.1% of respondents. Conclusion: Providers’ training and utilization of colposcopy for cervical cancer screening remain suboptimal in Africa. To increase utilization of colposcopy in the region, further training is needed to improve providers' knowledge and engagement. With the development of lower-cost and portable colposcopes, efforts to equip cervical cancer prevention programs and facilities with colposcopy should be enhanced to ensure that women can be screened and managed appropriately in the clinical setting and communities.


Introduction
Assessing women presenting with positive cervical screening results and selecting those suitable for immediate therapy usually relies on the colposcopic assessment of the transformation zone to visualize and characterize cervical epithelium and guide biopsies. 1In the standard practice, colposcopy guidance is required to perform excision of transformation zone for treatment of high grade cervical precancers.Thus, colposcopy is an essential part of an effective cervical cancer prevention program.
A major challenge to the successful implementation of cervical cancer prevention activities is the lack of colposcopy utilization following positive screening results.3][4] Various health systems and patient factors in uence access to colposcopy in low and middle-income countries (LMICs).System barriers include a limited number of colposcopy services, which are mostly found in tertiary-level facilities, with long waiting times for patients and few opportunities for non-specialist clinicians to develop the required skills. 5The limited numbers of specialist gynecologists, coupled with the high demands on these doctors for emergency and obstetrical and gynecology services, results in lesser time available for diagnostic or non-urgent procedures like colposcopy. 6colposcope is a binocular telescope used to directly visualize the cervical mucosa under a good light source.Since it was invented in 1925, 7 it has undergone modi cations to improve its diagnostic accuracy and make it more suited to settings with poor health infrastructures.Traditionally, the colposcope has been developed as an optical diagnostic instrument designed for specialists in higher-level healthcare facilities and requires a minimum infrastructure (electricity, examination room, etc) to operate.In recent years, high-resolution images taken with digital cameras have improved the detection of cervical lesions and enabled images to be shared between senior colposcopists and less experienced ones. 8Digital colposcopy has several advantages (including cost, portability, and ease of use) that make it more adapted to LMICs compared to its optical counterpart or traditional colposcopes.
In LMICs, the need to create more opportunities for cancer care is growing considering the lack of specialist services and other constraints. 9Primary healthcare professionals (PHPs) in these settings act as frontline providers in delivering preventive services, including cervical cancer prevention.They strengthen the coordination of care and educate patient using culturally adapted interventions. 10Not only they assist women in the screening procedure, but also, they support those with abnormal results by offering them post-screening counseling and management.
The contribution of PHPs in addressing cervical cancer has been highlighted in LMICs. 10In the innovative approach developed by our team, hands-on training 11 is combined with distant learning through the use of a practical and low-cost tele-mentoring tool (the Project ECHO) aimed at sharing best care practices.In this model, PHPs diagnose and manage patients with the assistance of specialists who act as mentors and provide feedback, guidance, and didactical training. 10,12Using this approach, PHPs are equipped with the skills, self-con dence, and knowledge to manage cervical pre-invasive or early-invasive disease.This reduces travel time, wait time, costs, and complications stemming from these delays.With this telementoring model, PHPs retain their duty of care to patients as their competencies and independence build up, which reduces referral rates and improves patients' outcomes. 10spite logistical and technological advances aimed at making colposcopy more accessible to LMICs, little is known about African providers' training and knowledge of the utility of colposcopy.Thus, the present study aims to describe the utilization of colposcopy by PHPs involved in cervical cancer prevention activities in Africa.

Study population and study design
The study population consisted of African-based clinicians involved in cervical cancer prevention activities from 23 African countries who were enrolled in a distance learning program focusing on cervical cancer and other HPV-related anogenital diseases. 12In 2022, providers were invited to take an online survey (in English or French) to assess their training, knowledge, and attitudes toward cervical cancer screening and management of pre-invasive lesions, including the use of colposcopy.The questionnaire was pre-tested and validated before being administered to the target population.This was done in two steps: In the rst step, after developing the survey tool, we shared it with 4 experts to get their feedback and remarks regarding content validity.Suggestions from these experts were then incorporated into the survey tool.In a second step, the self-administered survey was pilot-tested with a convenience sample of 20 individuals of varying healthcare provider professions based in Africa to ensure clarity of questions and ease of administration.Further comments from this set of HCPs were accounted for in the nal revision of the questionnaire.Participation was anonymous and voluntary, and refusal to take the survey had no consequence on participation in the distance learning program.A detailed description of the survey design, content, and administration has been published elsewhere. 10

Outcome measures
We assessed whether African-based providers involved in cervical cancer prevention activities performed colposcopy in their practice using the following questions related to optical or digital colposcopy."Do you currently perform colposcopy in your practice?"If the answer to this question was "yes," two follow-up questions were asked: "How many times have you performed colposcopy in the last 6 months?".In those who reported performing colposcopy in their practice, we also asked the question: "For what purpose do you use a colposcope?", and the possible responses to this question were: "For routine visual screening," "To better visualize cervical mucosa," "To visualize the transformation zone," "To assess vascularization of the cervical mucosa," "To determine treatment modality in screen-positive women."Multiple responses were allowed for this question.

Additional variables
Prior training on colposcopy was assessed with the following question: "Have you previously had formal training in performing colposcopy?" (Yes/No).
To better describe the study population, we collected the following socio-demographic variables: age (years), gender (Male/Female), and location according to the United Nation's classi cation of African regions (Eastern Africa, Middle Africa, Western Africa, Southern Africa, and Northern Africa), and setting (urban/rural).Providers were also classi ed according to their educational background into doctors/residents (including family medicine physicians, internists, obstetricians-gynecologists, oncologists, pediatricians, surgeons, pathologists, etc.), and nurses (including midwives).
In addition to these variables, self-reported knowledge about colposcopy was assessed with the following statement: "My knowledge about colposcopy is adequate for my current practice."Possible responses to this statement included: "Agree," "Disagree," "Neither Agree nor Disagree," and "I don't know."

Statistical analysis
The descriptive statistical analyses, prevalence, and associated con dence intervals were obtained using statistical analysis software The SAS (v9.4).

Ethics approval
This research conformed to the principles embodied in the Declaration of Helsinki.All participants provided written informed consent.The study protocol was approved by the University of Texas MD Anderson Cancer Center's IRB.Among providers who reported performing colposcopy in their practice, colposcopy was indicated for routine visual screening in 21.2% of clinicians, to visualize the transformation zone in 15.2% of respondents, to assess vascularization of cervical mucosa in 33.3% of respondents, and to determine treatment modality in 12.1% of respondents.(Fig. 1) In this group, the median number of colposcopies performed in the last 6 months was 30 (Interquartile range: 19-65).

Perceived knowledge about colposcopy
Providers were also if their knowledge about colposcopy was adequate for their current practice.Of the 92 providers who responded to this question, half (50.0%) agreed with this statement (Table 2).

Discussion
Colposcopy is a critical triaging investigation in the assessment, diagnosis, and management of women with positive cervical screening tests. 13However, colposcopy typically is not available in a primary care setting, and in many LMICs, the alternative is to visualize the cervix with the naked eye after application of acetic acid and Lugol's iodine, which may result in missed diagnoses. 14,15Indeed, the sensitivity of triaging with VIA/VILI in detecting high-grade cervical lesions among HPV-positive women has been reportedly suboptimal. 15,16A key role of colposcopy in cervical screening continuum is assessing the type of transformation zone and guiding treatment.Studies have reported higher residual disease after excisional treatment (positive excision margin) when treatment was performed without colposcopic guidance. 17,18Further, colposcopy evaluation of screen-positive women has proven to reduce the rate of overtreatment, thereby increasing the effectiveness of screening programs. 19,20Limited resource settings should be enhanced to provide quality healthcare, particularly when specialized physicians are lacking.Priority interventions include task-shifting and provision of more simple and cost-effective equipment for diagnosis and management of conditions of public health concern.Our that 12.6% of clinicians involved in cervical cancer prevention activities in Africa had been trained at performing colposcopy highlight the lack of skilled colposcopists in the region.
While organizing colposcopy training courses is an effective way to strengthen the diagnostic ability of colposcopists, 11 setting-up these courses in practice may be challenging and di cult to scale.Therefore, distant continuing educational programs where expert colposcopists review cervical images of women screened for cervical cancer provide an opportunity for providers in LMICs to increase their experience and competence in accurately performing colposcopy. 10,12While harmonized diagnostic standards and quality control procedures for colposcopy practice are released by relevant professional organizations, 13 many colposcopists in LMICs, because they lack adequate training, do not rigorously apply colposcopy guidelines in their practice, which leads to unharmonized reporting of colposcopy examinations.
The clinical performance of colposcopy depends on the training and experience of colposcopists and the clinical setting, from basic to referral facilities. 21When practiced by competent hands, colposcopy is more accurate and may barely miss severe disease, while it can lead to false-positive results when performed by less experienced providers.These weaknesses of colposcopy can be overcome by adequate training, continuing practice, and quality assessment. 10,22Although only one in eight clinicians in our study sample had been trained to perform colposcopy, 50% of respondents reported that their knowledge about colposcopy was adequate for their clinical practice.This nding suggests that colposcopy is not considered by many African providers as a procedure that requires speci c training, which is a matter of concern as it may have implications on the effectiveness of cervical cancer prevention programs in LMICs.
The use of digital colposcopes as an alternative to optic colposcopes may help improve access to cervical cancer screening and early detection. 23Previous studies found that certain digital colposcopes perform comparably to stationary colposcopes, 24 including when performed by mid-level providers like nurses. 25,26While the feasibility and accuracy of portable colposcopes in LMICs have been reported, their effectiveness in routine clinical practice is yet to be proven, especially to triage HPV positive women. 27,28he relevance of building capacity to perform colposcopy in African countries with high HIV prevalence has signi cantly increased after the publication by the World Health Organization (WHO) in 2021, of the new guidelines for cervical cancer screening and management. 29This guideline recommended that all women living with HIV and tested positive for HPV require triaging with VIA, cytology, or colposcopy.
In our model, frontline clinicians (including nurses) are trained to perform VIA and basic colposcopy. 10,11lposcopy in our study sample was used for routine cervical screening, to better visualize the transformation zone, and to determine treatment modality in screen-positive women.The practicability of colposcopy performed by trained PHPs using a portable colposcope implies that more women in LMICs can access colposcopy, especially in remote areas.
Considering the dearth of providers skilled to perform colposcopy in Africa, a strategy with HPV testing followed by optic colposcopy may result in delays in early detection and increase the risk of lost-to-follow up.Therefore, portable colposcopy performed by trained nurses can be offered in the same setting where HPV testing is done and much earlier than a referral to a physician.While colposcopy practice has been limited to medical doctors in most LMICs, our experience shows that PHPs supervised by experienced gynecologists can perform colposcopy with little side effects. 10,11In our program, capturing of cervical images with colposcopes and other digital equipment helps train PHPs through e-learning sessions (casebased presentation complemented by the review of cervigrams).Moreover, colposcopy with portable devices can be performed during outreaches and generate images that can be used for quality assurance.
Quality assurance is critical to the effectiveness of a cervical cancer screening program.We employ a collaborative approach for quality assurance through regular meetings in which in-house and external experts discuss cases with attending providers. 10Adding quality assurance review by specialists using colposcopy has been reported to improve the diagnostic accuracy of VIA. 30 PHPs in more remote facilities can also engage with expert colposcopists through anonymized cervigrams on social media platforms, and colposcopic images can be uploaded to the cloud for quality assurance assessment.This facilitates timely consultation with a distant colposcopist while the patient is still in the healthcare facility and reinforces quality control. 31,32ti cial intelligence (AI) as an adjunct to colposcopy has raised concerns about the importance of training PHPs in basic colposcopy.Introducing AI-based evaluation and interpretation of cervigrams may reduce the learning curves for PHPs in performing colposcopy.While AI is expected to assist less skilled PHPs in providing more accurate diagnosis 33,34 , follow-up, and treatment of precancerous lesions of the cervix, its use will still require hands-on training and skilled providers.
There were limitations to this study.First, most respondents to the survey were clinicians working in urban settings, suggesting that our ndings may not representatively re ect colposcopy practices among providers living in rural areas.Second, respondents were selected among clinicians invited to attend a continuing education e-learning program aimed at building the capacity of African providers in the eld of cervical cancer prevention and management, and the survey was administered online.As a result, providers in areas with limited internet penetration were underrepresented in our study sample.

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