Abstract
Objectives
Primary human papillomavirus (HPV) testing by clinician-collection is endorsed by U.S. guideline organizations for cervical cancer screening, but uptake remains low and insights into patients’ understanding are limited. This study aims to primarily address patient awareness of primary HPV screening by clinician-collection and acceptance of primary HPV screening by clinician- and self-collection, and secondarily assess factors associated with awareness and acceptance.
Setting
Primary care practices affiliated with an academic medical center.
Methods
A cross-sectional survey study of screening-eligible women aged 30–65 years was conducted to assess awareness and acceptability of primary HPV screening. We analyzed bivariate associations of respondent characteristics with awareness of primary HPV screening by clinician-collection, willingness to have clinician- or self-collected primary HPV testing, and reasons for self-collection preference.
Results
Respondents (n = 351; response rate = 23.4%) reported cervical cancer screening adherence of 82.8% but awareness of clinician-collected primary HPV as an option was low (18.9%) and only associated with HPV testing with recent screening (p = 0.003). After reviewing a description of primary HPV screening, willingness for clinician-collected (81.8%) or home self-collected (76.1%) HPV testing was high, if recommended by a provider. Acceptability of clinician-collected HPV testing was associated with higher income (p = 0.009) and for self-collection was associated with higher income (p = 0.002) and higher education (p = 0.02). Higher education was associated with reporting self-collection as easier than clinic-collection (p = 0.02). Women expected self-collection to be more convenient (94%), less embarrassing (85%), easier (85%), and less painful (81%) than clinician-collection.
Conclusions
Educational interventions are needed to address low awareness about the current clinician-collected primary HPV screening option and to prepare for anticipated federal licensure of self-collection kits. Informing women about self-collection allows them to recognize benefits which could address screening barriers.
Keywords
Introduction
Cervical cancer incidence in the United States (U.S.) declined more than 50% from the mid-1970s to the mid-2000s and cervical cancer mortality has decreased approximately 75% since the Papanicolaou (Pap) test screening was introduced.1,2 However, U.S. Cancer Statistics program data show a worrisome trend from 2001 to 2018 with a 1.3% annual increase in distant (stage IVA-B) cervical cancer. 3 This increase corresponds with declines in self-reported cervical cancer screening rates since the year 2000 from 86.5% to only 73.5% in 2019 based on National Health Interview Survey (NHIS) data, well below the originally published Healthy People 2030 goal of 84.3%.4–6 Recently, the NHIS reported 2021 screening rates at 73.9% and the Healthy People 2030 target was changed to 79.2%. 7 Concerns about further declines in screening rates related to the impact of the COVID-19 pandemic have been validated by a reported 36% decrease in the second quarter of 2020 with initial recovery followed by continued decline through 2021 in a nationally representative all-payer dataset. 8 In addition to the decrease in cervical cancer screening rates exacerbated by the COVID-19 pandemic, inequities in cervical cancer screening associated with specific sociodemographics persist. Cervical cancer screening rates are lower among racial/ethnic minorities, uninsured or government insured, those not identifying as heterosexual, those living in rural (vs urban) regions, and among those with less education, lower income, and fewer years since immigration to the United States.9,10 Addressing these disparities is critical as most cases of invasive cervical cancer are associated with either delayed or no prior screening. 11
Cervical cancer screening recommendations have evolved from a focus on cytology-based (Pap test) to human papillomavirus (HPV)-based testing. Primary HPV testing as a stand-alone screening option by clinician-collection received Federal Drug Administration (FDA) approval in 2014 and was endorsed by the U.S. Preventive Services Task Force (USPSTF) in 2018 for women aged 30–65 years old, along with continued USPSTF support for Pap alone and Pap/HPV co-testing, based on provider and patient preference as well as test availability. 12 Guideline endorsement of clinician-collected primary HPV screening has provided an opportunity to explore patient self-collection outside of clinic of a vaginal swab for HPV testing as a strategy to address declining screening rates. A meta-analysis of 26 studies reported high levels of concordance between HPV test results performed on vaginal samples collected by patients compared with cervical samples collected by clinicians. 13 Research efforts of the National Cancer Institute's (NCI's) “Last Mile” Initiative are expected to result in eventual FDA approval of home self-collection devices for vaginal HPV testing paired with specific lab platforms which may address screening barriers by eliminating the need for a speculum exam, thus providing flexibility for patients in screening location and time. 14 Acceptance of HPV test self-collection among diverse groups of women in low-resource settings has been observed in pilot studies performed in Appalachian Kentucky, and with Somali immigrants in Minnesota, Latina and Haitian women in Miami, and Black women in the Mississippi Delta, with various test collection settings including homes, clinics, and a church building.15–18
In a systematic review that included quantitative studies of women's acceptance of clinician-collected primary HPV screening in the United States, Canada, and Australia, acceptance ranged from 13% to 84%, with greater than 50% acceptance observed in five of the six studies. 19 A mixed-methods study, not included in the systematic review, was conducted immediately following USPSTF 2018 endorsement of clinician-collected primary HPV screening and reported themes of “uncertainly or distrust with HPV testing,” though generalizability is limited by the study size of 46 participants. 20 The USPSTF is the principal authority for practice guidelines in primary care, yet uptake of primary HPV screening is low in clinical practice as demonstrated by Qin et al.'s report that among almost 7 million women in 2019, < 0.5% were screened with a primary HPV test. 21
It is currently unclear whether patient awareness and acceptability of primary HPV screening has improved since the USPSTF's 2018 endorsement, in regard to both guideline-supported clinician-collection at the office and with anticipated approval of patient self-collection of HPV testing at home. Therefore, the primary objective of this study was to provide an updated evaluation of awareness and acceptability of primary HPV testing by clinician-collection and acceptability of patient self-collection for cervical screening among screening-eligible women. The secondary objective was to assess survey respondent characteristics associated with acceptability and awareness.
Methods
Study setting
A cross-sectional survey evaluating patient awareness and acceptance of HPV screening by clinician-collection and self-collection was mailed to cervical cancer screening-eligible women empaneled to a primary care provider in the Mayo Clinic Midwest healthcare system. The healthcare system includes 62 primary care clinics across Minnesota, Wisconsin, and Iowa. The study was approved by the Institutional Review Board at Mayo Clinic in Rochester, Minnesota (study ID: 20-009185).
Study population
Women aged 30–65 years old who qualified for routine cervical cancer screening, with documented research authorization status, and empaneled in the Mayo Clinic Midwest Primary Care practice, met the inclusion criteria. Exclusion criteria included those who did not qualify for screening due to history of hysterectomy or did not qualify for routine screening intervals due to a history of in utero diethylstilbestrol exposure, cervical cancer, HIV infection, solid organ transplant, or being on immunosuppressant medication. Diagnosis and billing codes were used to apply the inclusion and exclusion criteria, and approximately 106,000 women met enrollment criteria. A simple random sampling approach, without stratification, was then used to select 1500 women to invite to participate in the survey study via mailed letter and survey.
Survey content and administration
The study team conducted a literature search to identify publications addressing patient perspectives on primary HPV screening and patient self-collection. Questions about survey respondent demographics including race, ethnicity, marital status, household income, housing status, and geographic area of residence (rural vs urban) were included in the survey (see online Supplement) along with questions about timing of last cervical cancer screening and the screening test type (Pap and/or HPV testing). A description of primary HPV testing by clinician-collection as a guideline-endorsed cervical cancer screening option was embedded in the survey and women were then asked if they had heard of using HPV testing alone for cervical cancer screening prior to taking the survey. Investigator-developed questions included “Would you be willing to have primary HPV testing for cervical cancer screening in clinic as an alternative to a Pap or Pap/HPV co-test if recommended by your primary care provider?” and “Would you be willing to self-collect an HPV test at home for cervical cancer screening as an alternative to a Pap or combined Pap/HPV test in the clinic if recommended by your primary care provider?” Prior to the latter question, survey respondents were provided with a description of the vaginal swab self-collection as inserting and removing a device similar to a throat swab, in the same way as a tampon. We also queried likelihood of following up with a healthcare provider for further testing if an HPV self-collection test was abnormal.
Additional survey questions about anticipated convenience, ease, embarrassment, and discomfort of self-collection at home compared with clinician-collection were adapted from Sultana et al. (an open access source) and with expressed author permission from Mao et al.22,23 The survey draft was piloted in the sampling frame population with probes to evaluate clarity of the questions. Feedback from the pilot centered around the HPV self-collection questions with requests for a more detailed description of the self-collection device and the collection process, using simpler language and comparisons, resulting in the explanation described above.
Survey administration and data collection were conducted by the Mayo Clinic Survey Research Center. A multiple contact data collection protocol with up to three USPS mailings was deployed. The survey was first mailed on 4 December 2020. After 4 weeks, a second mailing was sent to non-respondents. After an additional 4 weeks, a third and final survey was mailed to remaining non-respondents. The Mayo Clinic IRB granted a waiver of written consent for this minimal risk study and approved inclusion in the survey invitation letter of the following statement: “Completion and return of the survey serves as your consent for participation.” A Health Insurance Portability and Accountability Act privacy authorization form was included and was required to be signed and returned by the survey respondents to enable linking of patient survey data with the medical record data. Study subject remuneration was not included.
Statistical analyses
Given our primary outcome variables were single proportion estimates, our sample size estimates were based on calculations of precision. For a 95% confidence level that the true values for awareness and acceptability of HPV screening were within a 5% margin of error of the surveyed values and with an essentially unlimited sample size (but limited by study budget) and presumed population proportion of 50%, the minimum number of samples was calculated to be 385 respondents. With an assumption of an approximately 25% response rate, the decision was made to sample 1500 study subjects. Descriptive statistics were provided for survey respondent characteristics. Associations between survey respondent characteristics and awareness of the primary HPV screening option by clinician-collection, acceptability of being screened (clinician and self-screen options), and endorsement of self-collection features were tested using Pearson's Chi-Square tests or Fisher's Exact test where tables were sparse with p-values reported. No multiple testing correction is presented. However, a sensible, likely overly conservative approach would be to assess an outcome-wise Bonferroni correction with the threshold of statistical significance set at 0.05/10 = 0.005 for the awareness outcome, while 0.05/11 = 0.0045. Logistic regression analysis was not conducted as this analysis is intended to be primarily descriptive. As well, logistic regression models would be limited due to the correlation of many of the patient characteristics, low level of awareness of primary HPV screening, and high levels of screening willingness and endorsement of self-collection features.
Results
Survey respondent characteristics and association with awareness of clinician-collected primary HPV screening option
The survey was sent to 1500 women and 351 responded (23.4% response rate). Based on our sample size calculations, this provided a 95% confidence interval that the real value was within ± 5.23% margin of error of the surveyed value. Table 1 summarizes characteristics of survey respondents and their association with awareness of the clinician-collected primary HPV screening option. Most survey respondents were aged 50–65 years old (50.7%), non-Hispanic white (93.7%), college educated or higher (64.8%), married (81.0%), had a household income of $50,000 or higher (78.4%), were homeowners (85.4%), resided in a rural geographic area (61.7%), and reported cervical cancer screening within the past 5 years (82.8%). Only 18.9% were aware of clinician-collected primary HPV testing as a screening option and awareness was only associated with having had prior HPV testing (p = 0.003). An additional descriptive question (not included in Table 1) explained that positive HPV results on a self-collected test would require a clinic visit for a Pap test and asked how likely women would be to follow-up with their primary care provider in that scenario; 95.1% reported they would be very likely to follow-up, 3.7% reported somewhat likely, and only 1.2% reported unlikely.
Survey respondent characteristics and association with clinician-collected primary HPV screening awareness.
Association of survey respondent characteristics with acceptability of primary HPV screening (by clinician- or self-collection) and with potential attributes of self-collection
After reviewing written explanations embedded in the survey about primary HPV testing and self-collection, 81.8% of respondents reported willingness to have a clinician-collected primary HPV test and 76.1% reported willingness to self-collect a primary HPV test at home if either was recommended by their primary care clinician (Table 2). Clinician-collection acceptability was associated with higher income (p = 0.01); self-collection acceptability was associated with higher income (p = 0.002) and higher education (p = 0.02).
Association of survey respondent characteristics and acceptability of primary HPV screening by clinician-collection or self-collection.
Most women reported expecting self-collection of a vaginal swab for HPV screening at home to be more convenient (93.7%), less embarrassing (85.0%), easier (85.3%), and less painful (81.1%) than a clinician-collection. Education beyond high school was associated with reporting self-collection of an HPV test as being easier than a clinic-collection (p = 0.02) but no other associations were observed between survey respondent characteristics and reported descriptions of self-collection (Table 3).
Association of survey respondent characteristics and potential attributes of home-based self-collection.
Questions measured on 4-point scale: strongly agree, somewhat agree, somewhat disagree, strongly disagree. Responses dichotomized to Agree (somewhat to strongly agree) and Disagree (somewhat to strongly disagree).
Discussion
Awareness of the clinician-collected primary HPV test option for cervical cancer screening among the surveyed women in our study was low, similar to a recent report from Great Britain that only 13.5% of screening-eligible women correctly understood a description of clinician-collected primary HPV screening as the method used in their organized screening program. 24 In our study, after reviewing a brief description of the primary HPV test option and clinician versus in-home self-collected HPV testing, most women reported willingness to be screened by either option, if recommended by their primary care clinician. The observed acceptance rate (81.8%) for clinician-collected primary HPV screening in our study was higher than for most of the studies included in the Nothacker et al. systematic review, though aligned with rates reported in two of the studies. 19 All subjects in our study had a primary care provider and higher acceptance of primary HPV screening by clinician-collection or self-collection may have resulted from the survey question's wording that included “if recommended by your primary care provider” which could reflect trust of the primary care provider or social desirability bias. A study by Kraut et al. found that 60% of women surveyed about self-collection at a primary care clinic in Edmonton, Canada, wanted the option of self-collection, despite only 7% having heard of the option before the survey. 25 This is similar to our observed 76.1% acceptance of self-collected primary HPV screening. Participants in Kraut et al.'s study were like those in our study in terms of education and cervical cancer screening up-to-date status. However, participants in their study were younger on average (median age 35) than those included in our study. While both studies reveal generally low knowledge of primary HPV testing for cervical cancer screening, both demonstrate high levels of acceptability of primary HPV screening by self-collection as an option.
Survey respondents in our study endorsed potential benefits of self-collection including convenience, less embarrassment, greater ease, and less pain. Similar observations were noted by women who participated in an HPV test self-collection trial in Australia, with most reporting that self-collection was easier (93%), more convenient (98%), less embarrassing (94%), and less uncomfortable (90%) compared to a having a clinician-collected Pap test. 26 Mao et al. reported a preference for self-collection among University of Washington healthcare system patients driven mostly by testing logistics including convenience, ease of collection, and time saving compared with a clinic visit for screening. 23
Although self-collection of a vaginal sample outside of a clinic-based setting for primary HPV testing could be an option for all screening-eligible people once FDA-approved and guideline-endorsed, most past research has focused on self-collection as an intervention targeted toward underscreened women. Our results suggest home-based self-collection to be more acceptable to those with higher income and education, demographics associated with higher screening uptake. 10 This is consistent with the findings of Mao et al.; self-collected HPV testing was increasingly preferred in correlation with higher levels of education and household income. 23 In interviews of Hispanic women of any race and non-Hispanic Black women receiving care in a safety net clinic in Dallas, Texas, or an urban medical center in Seattle, Washington, preference for self-collection was lower at 32% and 55% respectively. 27 Research has documented slower uptake of novel cancer screening options among traditionally underserved populations.28,29 Further research into identifying ways to overcome reluctance and enhance the adoption of novel screening tests, particularly among groups with lower screening rates, may be valuable.
One concern with self-collection is whether patients will follow-up in clinic as would be required for abnormal HPV results. Our study, along with Zhu et al., found high rates (>90%) of patients endorsing that they would follow-up as directed. 30 This is encouraging and consistent with findings from the Netherlands that found a follow-up compliance rate of just over 90%. 31
Strengths and limitations
Study strengths include providing updated data on awareness and acceptability of primary HPV testing among screening-eligible women both by clinician-collection following endorsement by USPSTF in 2018 and by home-based self-collection. The study drew from a large regional area including multiple clinic sites and largely from a rural demographic that has historically been underscreened for cervical cancer. The random sample was fairly evenly distributed across the healthcare system service area and by age groups. However, given the survey respondents were primarily white, non-Hispanic, married, college-educated, and living in the rural Midwest, the results may not be representative of more diverse populations. The lack of sociodemographic information for the non-responders is also a limitation. Additional limitations include the response rate of 23.4% and, as with all survey studies, the potential for non-response bias, particularly with simple random sampling rather than stratified oversampling.
Conclusions
Addressing limited awareness about primary HPV testing as a cervical cancer screening option among screening-eligible women may increase acceptance and thereby uptake of clinician-collection while preparing women for future self-collection options, which have the potential to remove barriers to screening.
Supplemental Material
sj-docx-1-msc-10.1177_09691413241260019 - Supplemental material for Primary human papillomavirus testing by clinician- versus self-collection: Awareness and acceptance among cervical cancer screening-eligible women
Supplemental material, sj-docx-1-msc-10.1177_09691413241260019 for Primary human papillomavirus testing by clinician- versus self-collection: Awareness and acceptance among cervical cancer screening-eligible women by Kathy L. MacLaughlin, Gregory D. Jenkins, Jennifer St Sauver, Chun Fan, Nathaniel E. Miller, Amanda F. Meyer, Robert M. Jacobson, and Lila J. Finney Rutten in Journal of Medical Screening
Footnotes
Acknowledgments
We thank Ms. Lisa Guenther and the Mayo Clinic Survey Research Center for assisting with the survey design and data collection.
Authorship confirmation statement
All authors have made substantial contributions to the conception or design of the work (KLM, RMJ, LJFR) or the acquisition, analysis, or interpretation of data for the work (KLM, LJFR, RMJ, GDJ, CF, JLSS, NEM, AFM) and were involved in drafting (KLM) or critically revising the manuscript (AFM, NEM, RMJ, JLSS, GDF, CF, LJFR) for important intellectual content. All authors have provided final approval of publication. The authors are accountable for all aspects of the work.
Author disclosure statements
There are no potential conflicts of interest with respect to this manuscript.
Dr St Sauver receives research support grants from Moderna (related to studies of infectious mononucleosis and cytomegalovirus) and from Exact Sciences (related to studies of Cologuard colorectal cancer screening).
Dr Jacobson serves on the external data monitoring committee for Merck & Co.
Dr Finney Rutten reports employment with Exact Sciences from 5/31/2022 to 3/15/2023.
There are no additional declarations from Dr MacLaughlin, Mr Jenkins, Ms. Fan, Dr Miller or Dr Meyer.
Declaration of conflicting interests
The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding
This study was made possible using the resources of the Mayo Clinic Robert D. and Patricia E. Kern Center for the Science of Health Care Delivery in Rochester, Minnesota.
Mayo Clinic Robert D. and Patricia E. Kern Center for the Science of Health Care Delivery,
References
Supplementary Material
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