Abstract
Objective To determine the uptake and feasibility of human papillomavirus self-sampling (HPV SS) offered to patients in a family medicine clinic.
Design Implementation study.
Setting Community family medicine clinic in Edmonton, Alta, with a cervical cancer screening rate of 80%.
Participants Patients 25 to 69 years old with a cervix who had not received a Papanicolaou (Pap) test in 2.5 years or more. Exclusion criteria included being pregnant; experiencing colposcopy care or having been discharged from care within 11 months; having history of invasive cancer; experiencing abnormal vaginal bleeding or current menstruation; identifying as transgender; and having abnormal results on the last Pap test.
Interventions Eligible patients were opportunistically offered HPV SS in the clinic (September 2024 to November 2024) as the first phase of the Alberta Cervical Cancer Screening HPV SS pilot program.
Main outcome measures The primary outcome was the proportion of patients who completed HPV SS. Secondary outcomes were factors associated with completing HPV SS, HPV SS results, patient preferences, physician perspectives, and environmental impact.
Results Overall, 226 patients were offered HPV SS. Characteristics of patients included the following: the median age was 43 years (interquartile range [IQR]=32 to 56); 89% lived in urban areas; 14% were immigrants; 4% were Indigenous; 58% were panelled (ie, attached to a family physician); and the median number of months since a last Pap test was 37 (IQR=32 to 45). Overall, 81% completed HPV SS: 165 had negative results, 17 were positive, and 2 were indeterminate, resulting in 7 Pap tests and 10 direct colposcopy referrals. Among patients who completed HPV SS, 98% preferred to have HPV SS as an option for future screening. Family physicians supported its use and HPV SS has the potential to decrease carbon impact by up to 20%.
Conclusion The study suggests that HPV SS may be the preferred cervical cancer screening approach for patients attending a family medicine clinic. Screening programs should consider improving access to HPV SS for this population.
Cervical cancer screening programs introduced in Canada in the 1950s have led to substantial reductions in cervical cancer morbidity and mortality.1,2 The age-standardized mortality rate has decreased approximately 2.1% since 1984.2 Recently, human papillomavirus (HPV) testing has been replacing Papanicolaou (Pap) tests as the primary screening method due to greater accuracy.3-5 The shift to screening for HPV has the added benefit of HPV self-sampling (HPV SS), which allows individuals with a cervix to collect their own sample. HPV SS is as accurate as samples collected from a clinician and care is not compromised by the absence of a pelvic examination.6,7 A systematic review by Nishimura et al found that participants preferred HPV SS due to its comfort, convenience, and privacy.8
However, there is limited research on HPV SS uptake and feasibility in regular family practice. Studies in this population primarily focus on providing HPV SS to underscreened individuals or assess preferences through surveys.9-17 This study aims to fill this gap by examining the participation rate in HPV SS when it is made available to all patients attending a Canadian family medicine clinic. Secondary objectives include examining factors associated with completion, HPV SS results, patient and physician preferences, and environmental impacts of HPV SS compared with the Pap test.
METHODS
Strengthening the Reporting of Observational Studies in Epidemiology reporting guidelines were used to report the results of this study.18 Ethics approval was granted by the University of Alberta Health Research Ethics Board in Edmonton (Pro00128729). A waiver of consent was approved due to minimal risk to patients, HPV SS being the standard of care in other jurisdictions, the impracticality of completing the study with consent, and the potential for selection bias if consent were required.
Setting
The Alberta Cervical Cancer Screening Program has been conducting a pilot project to increase cervical cancer screening access for populations who are underscreened in Alberta as well as to lay the foundation for future expansion to total population screening. The initial phase of the project took place at Shifa Medical Clinic (SMC) in Edmonton, Alta.
SMC has 12 female physicians, 6 of whom manage patient panels totalling about 3500 patients. Panelled patients receive ongoing care from a specific family physician, while nonpanelled patients may visit regularly but are not assigned to a specific doctor.19 The clinic handles around 2000 visits per month, with approximately 50% of visits from panelled patients. Demographic characteristics of SMC patients include the following: 79% are female, with a mean (standard deviation [SD]) age of 39 (11); 88% have completed postsecondary education; 16% are immigrants who have arrived in Canada in the past 10 years; 54% are white; 33% are Asian; and 13% are Black, Hispanic, or Indigenous.14,20 SMC’s cervical cancer screening rate is approximately 80%.
Population
All patients documented as female in the clinic’s electronic medical record (EMR) between the ages of 25 and 69 years, and who had an appointment at SMC between September 24, 2024, and November 23, 2024, were included. Exclusion criteria included having a Pap test within the past 2.5 years; being pregnant; having a history of invasive cervical cancer; having abnormal results on the last Pap test; currently receiving colposcopy care or having undergone colposcopy care in the past 11 months; currently experiencing their menstrual cycle or abnormal vaginal bleeding; never having been sexually active, and being transgender (due to potential distress about being asked about HPV SS at reception).
HPV device, platform, and clinical pathway
Patients collected vaginal samples using flocked swabs. The dry swabs were sent to the laboratory where they were rehydrated and tested. Prior to the pilot program, the Alberta Cervical Cancer Screening Program developed an HPV SS clinical pathway with guidance from their HPV SS Clinical Working Group based on the 2023 Canadian Guideline on the Management of a Positive Human Papillomavirus Test and Guidance for Specific Populations.21,22
Study process
All patients who had booked an appointment during the study period were reviewed for eligibility using a custom EMR form with automatic eligibility notifications. Upon check-in, medical office assistants provided a form for eligibility confirmation and demographic characteristic data, as well as an HPV SS information sheet. For eligible patients, medical office assistants put the HPV SS swab, a QR code for a demonstration video, and a 1-question survey in the examination room, along with a 1-page physician information sheet on the external door handle, which included key talking points and alerted physicians of patient eligibility. Patients could ask questions about HPV SS during the appointment and had an opportunity to complete the HPV SS and survey after the visit. If HPV SS was not completed, staff investigated the reason. The clinic administrator notified patients of results, conducted the same 1-question survey again, triaged positive results, and informed physicians (supplementary file 1, available from CFPlus*).
Before the study began, physicians and staff attended a 10- to 15-minute orientation session. At the end of the study, physicians completed a 1-page anonymous survey on their experience with HPV SS (supplementary file 2, available from CFPlus*). Since HPV SS is not reimbursed, compensation at a similar rate of Pap tests ($30.17/Pap test, billing code 13.99BA) was provided to prevent income loss.23
Data
Patient demographic characteristics were collected from the form patients had completed upon check-in and were entered de-identified, along with study outcomes, into a Google spreadsheet. Data were only accessible to the study team. Data for the patient flow chart were extracted from the custom EMR form and spreadsheet.
Analysis
The participation rate was calculated as the number of patients completing HPV SS divided by those offered it. To compare the characteristics of patients who completed versus those who did not, we used
, z, t, and Mann-Whitney U tests for categorical variables, proportions, means, and medians, respectively. Attribute percentages were calculated excluding missing data. We also calculated the percentage of patients who preferred HPV SS based on survey responses and thematically analyzed physician survey data. The carbon footprint of 1 HPV SS test was compared with 1 Pap test using published carbon emissions data from invitation screening to preparation of the sample for laboratory transport.24
RESULTS
Patient flow
A total of 1176 patients were assessed for eligibility (Figure 1). The most common reason for ineligibility was a Pap test being done less than 2.5 years ago (n=607). Among the 215 eligible patients, 37% had scheduled an appointment for a Pap test or periodic health examination (which often includes a Pap test), and the remaining had appointments for other reasons.
Patient flow sheet
Demographic characteristics
Table 1 provides the demographic characteristics of participating patients. The patients were diverse, spanning various ages, screening histories, and socioeconomic backgrounds. Attributes between patients completing HPV SS and those who declined were not statistically significantly different.
Demographic characteristics of patients: Percentages may not equal 100% due to rounding.
Participation rate
Overall, 81% of patients offered HPV SS completed the test (184 of the 226). The reasons for declining are listed in Table 2, with the most frequent reasons being lack of time (8), lack of interest in screening (7), and preferring the Pap test (3).
Reasons for patients declining HPV SS
HPV SS results
Table 3 presents the HPV SS results. We did not complete statistical testing as there were insufficient numbers of patients in the positive and indeterminate groups.
HPV SS test results
Patient and physician preference
Tables 4 and 5 provide patient and physician preferences and supplementary file 3, available from CFPlus,* provides patient feedback on HPV SS after completing the test. Among patients who completed HPV SS, 98% indicated they would prefer the option of HPV SS for future screening. Additionally, physicians felt strongly HPV SS should be an option to patients for cervical cancer screening.
Patient preferences
Physician survey results: All clinic physicians (N=11) besides the principal investigator completed the survey.
Environmental impact
Table 6 provides the carbon footprint of 1 HPV SS test compared to 1 Pap test with the assumption that disposable speculums are used in a clinical setting. The carbon footprint of 1 HPV SS test was 2803.8 gCO2e (grams of carbon dioxide equivalents), while the carbon footprint of 1 Pap test was 3573.9 gCO2e, a reduction of 770.0 gCO2e or 22% per test.
Carbon cost estimate per test
DISCUSSION
Our study evaluated HPV SS in a family medicine patient population—a group less frequently evaluated for HPV SS but important to consider as they represent a substantial portion of the screening population.
HPV SS was well received among patients and physicians, with high participation in the study and in follow-up tasks. Nearly all patients who completed the screening and the subsequent survey preferred the option, similar to the preference among patients in underscreened and marginalized populations.8 While this study was conducted in 1 family medicine clinic, the high patient preference may be applicable across Canada, given the diverse patient population at SMC. Additionally, HPV SS offers several other compelling advantages: It is cost-effective, reduces the carbon footprint of screening with minimal extra effort, and may allow family physicians to make better use of their limited time.24-26
HPV SS has long been recognized as a tool to improve equity in cervical cancer screening, particularly among underscreened and marginalized populations.27 However, providing HPV SS as part of regular screening in family practice is also a means to improve equity; it provides an alternative for patients who consistently decline clinician-collected screening and also does not disadvantage patients who come in regularly for screening but face a more invasive test. Perhaps the concept of equity with HPV SS should be reframed in terms of delivery method: for instance, marginalized populations may benefit from a community-based approach, while the family medicine population may benefit by having HPV SS available as an option within their clinics.
The delivery method used in this study—family physicians actively involved and patients completing their screening in clinic—was highly effective. This aligns with other studies conducted in family practice and broader cervical cancer literature: participation rates increase with direct health care provider contact and there is higher uptake when screening has fewer steps.11,12,28,29 Moreover, family physicians in this study and other studies appear supportive of in-clinic HPV SS.30-32
Barriers to implementation of HPV SS in clinic, such as difficulty identifying eligible participants, time constraints, and physicians’ skepticism of HPV SS, were largely absent in our study.30-32 SMC already tracked screening and routinely used EMR prompts. HPV SS information was also provided to patients at check-in, which likely reduced the time needed to address it during appointments. In addition, physicians may have been more supportive given the adoption of HPV SS in other Canadian jurisdictions and reimbursement available.5
The study took place as Canadian screening programs have been transitioning from cytology to primary HPV screening using various approaches: introducing HPV SS after, before, or together with primary HPV screening.5 There no longer appears to be a need to implement HPV SS after primary HPV screening, given its comparable efficacy and minimal concerns around loss to follow-up.6,33 In fact, introducing HPV SS later may lead some providers to perceive it as less effective.34 In contrast, offering HPV SS before or alongside primary HPV screening appears better aligned to the current context, which includes strong patient and provider preferences, limited primary care capacity, and environmental sustainability.8,24,35
Limitations
Our study lacked a comparator group and involved a population with a high baseline screening rate, but this was consistent with our objectives to evaluate uptake, preference, and environmental cost in a family medicine clinic rather than to assess whether HPV SS increased participation rates. Moreover, given the similar participation rate among individuals who had not been screened in more than 4 years and those from groups who are marginalized, this approach may also help improve screening in family medicine clinics. However, the aim was to assess whether HPV SS was acceptable, not to determine if it increased participation rates. Patients were not offered the option to complete HPV SS at home, so its uptake in that scenario is unknown. While the EMR notification approach used to recruit patients is unlikely to be feasible for regular clinics, it was necessary for this study and will not be required for routine HPV SS screening. The limited number of positive HPV SS results restricts conclusions about HPV-positive patients having differing attributes, and more data are needed. While the perspectives of SMC’s family physicians may not fully represent the broader physician view, the diversity of SMC’s physicians helps mitigate this concern.
Conclusion
HPV SS offered to patients attending a family medicine clinic had a high participation rate, was highly preferred by patients and their health care providers, increased cancer screening equity, and reduced the environmental impact of screening. Screening programs should strongly consider making HPV SS available to all patients attending family medicine clinics.
Acknowledgment
We thank the health care providers at Shifa Medical Clinic who participated in this study, including Dr Amira Aissiou, Dr Fabiola Diaz, Dr Kaili Harvie, Dr Uzma Khan, Dr Stephanie Liu, Dr Lana Myroniuk, Dr Alexandra Okihiro, Dr Jane Polley, Dr Andrea Tamm, Dr Anita Weng, and Dr Ying Yao, as well as clinic nurses Krystal Morton and Hamama Obansa. We also thank Clinic Owner and Manager Mohammad Ali Kamal for his time and support, and the office assistants for their outstanding diligence. We appreciate the Alberta SPOR SUPPORT Unit for facilitating Pampalon Material Deprivation Index data. We also thank Stephanie Balko, previous Improvement Facilitator at Edmonton Southside Primary Care Network, for her assistance during the initial stages of this study. We received funding from the Northern Alberta Academic Medicine Fund (R20P16) and the Alberta Cervical Cancer Screening Program received a grant from Alberta Health Cancer Research for Screening and Prevention Funding Program (AH CRSP #017117) for the pilot.
Footnotes
↵* Supplemental files 1 to 3 are available from https://www.cfp.ca. Go to the full text of the article online and click on the CFPlus tab.
Contributors
Dr Roni Y. Kraut conceptualized and planned the trial with input from all authors. Dr Kraut, Faith Wierenga, Holly Dievert, Bonnie Chiang, and Dr Oksana Babenko developed the study materials, including the surveys. Elisa Molstad screened eligible patients using the custom electronic medical record form. Omar Kamal designed the Google spreadsheet. Dr Babenko conducted the statistical analysis. All authors contributed to data interpretation. Dr Kraut and Michelle Umali coordinated the study. Dr Kraut acquired funding. Faith Wierenga drafted the manuscript. All authors reviewed, provided feedback, and approved the final version.
Competing interests
Dr Roni Y. Kraut has received research funding from M.S.I. Foundation in Edmonton, Alta, and Health Data Research Network Canada in Vancouver, BC, and travel funding from The Society of Gynecologic Oncology of Canada in Ottawa, Ont, to attend their National HPV (human papillomavirus) Steering Committee meeting. Dr Oksana Babenko has received research funding from the Social Sciences and Humanities Research Council in Ottawa, Ont.
This article has been peer reviewed.
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