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      Leveraging COVID-era innovation for cervical cancer screening: Clinician awareness and attitudes toward self-sampling and rapid testing for HPV detection

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          Abstract

          Cervical cancer screening rates are declining in the US, with persistent disparities among vulnerable populations. Strategies to better reach under-screened communities are needed. The COVID pandemic sparked major shifts in healthcare delivery, including the accelerated development and adoption of rapid diagnostic testing, broadened access to remote care, and growing consumer demand for self-testing, which could be leveraged for cervical cancer. Rapid tests for the detection of Human Papillomavirus (HPV) have the potential to improve cervical cancer screening coverage, and if coupled with patient-collected cervicovaginal samples, create an opportunity for self-testing. The objectives of this study were: 1) to examine whether COVID influenced clinician perspectives of rapid testing as a screening modality; and 2) to assess clinician awareness, perceived benefits and limitations, and willingness to adopt point-of-care HPV testing, patient self-sampling, and rapid HPV self-testing with self-collected samples. The methodology adopted consisted of an online cross-sectional survey (n = 224) and in-depth interviews (n = 20) were conducted with clinicians who perform cervical cancer screening in Indiana, ranked in the top ten states for cervical cancer mortality and with marked disparities across socio-demographic groups. The main findings show that about half the clinicians reported that the COVID pandemic had influenced their views on rapid testing as a screening modality both positively (greater public acceptability of rapid testing and impact on patient care) and negatively (concerns regarding accuracy of rapid tests). The majority of clinicians (82%) were willing to adopt rapid HPV testing at the point-of-care, while only 48% were willing to adopt rapid HPV self-testing with self-collected samples. In-depth interviews revealed provider concerns around patients’ ability to collect their own sample, report results correctly, and return to the clinic for follow-up and other preventive care. Addressing clinician concerns about self-sampling and rapid HPV testing, such as ensuring that rapid tests include sample adequacy controls, is necessary to mitigate barriers to adoption for cervical cancer screening.

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          Most cited references31

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          Rethinking Covid-19 Test Sensitivity — A Strategy for Containment

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            Cervical cancer screening for individuals at average risk: 2020 guideline update from the American Cancer Society

            The American Cancer Society (ACS) recommends that individuals with a cervix initiate cervical cancer screening at age 25 years and undergo primary human papillomavirus (HPV) testing every 5 years through age 65 years (preferred); if primary HPV testing is not available, then individuals aged 25 to 65 years should be screened with cotesting (HPV testing in combination with cytology) every 5 years or cytology alone every 3 years (acceptable) (strong recommendation). The ACS recommends that individuals aged >65 years who have no history of cervical intraepithelial neoplasia grade 2 or more severe disease within the past 25 years, and who have documented adequate negative prior screening in the prior 10 years, discontinue all cervical cancer screening (qualified recommendation). These new screening recommendations differ in 4 important respects compared with the 2012 recommendations: 1) The preferred screening strategy is primary HPV testing every 5 years, with cotesting and cytology alone acceptable where access to US Food and Drug Administration-approved primary HPV testing is not yet available; 2) the recommended age to start screening is 25 years rather than 21 years; 3) primary HPV testing, as well as cotesting or cytology alone when primary testing is not available, is recommended starting at age 25 years rather than age 30 years; and 4) the guideline is transitional, ie, options for screening with cotesting or cytology alone are provided but should be phased out once full access to primary HPV testing for cervical cancer screening is available without barriers. Evidence related to other relevant issues was reviewed, and no changes were made to recommendations for screening intervals, age or criteria for screening cessation, screening based on vaccination status, or screening after hysterectomy. Follow-up for individuals who screen positive for HPV and/or cytology should be in accordance with the 2019 American Society for Colposcopy and Cervical Pathology risk-based management consensus guidelines for abnormal cervical cancer screening tests and cancer precursors.
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              Self-sampling for human papillomavirus (HPV) testing: a systematic review and meta-analysis

              Introduction Human papillomavirus (HPV) self-sampling test kits may increase screening for and early detection of cervical cancer and reduce its burden globally. To inform WHO self-care guidelines, we conducted a systematic review and meta-analysis of HPV self-sampling among adult women on cervical (pre-)cancer screening uptake, screening frequency, social harms/adverse events and linkage to clinical assessment/treatment. Methods The included studies compared women using cervical cancer screening services with HPV self-sampling with women using standard of care, measured at least one outcome, and were published in a peer-reviewed journal. We searched PubMed, the Cumulative Index to Nursing and Allied Health Literature (CNIAHL), Latin American and Caribbean Health Sciences Literature (LILACS) and Embase through October 2018. Risk of bias was assessed using the Cochrane tool for randomised controlled trials (RCTs) and the Evidence Project tool for non-randomised studies. Meta-analysis was conducted using random-effects models to generate pooled estimates of relative risk (RR). Results 33 studies in 34 articles with 369 017 total participants met the inclusion criteria: 29 RCTs and 4 observational studies. All studies examined HPV self-sampling; comparison groups were standard of care (eg, Pap smear, visual inspection with acetic acid, clinician-collected HPV testing). 93% of participants were from high-income countries. All 33 studies measured cervical cancer screening uptake. Meta-analysis found greater screening uptake among HPV self-sampling participants compared with control (RR: 2.13, 95% CI 1.89 to 2.40). Effect size varied by HPV test kit dissemination method, whether mailed directly to home (RR: 2.27, 95% CI 1.89 to 2.71), offered door-to-door (RR: 2.37, 95% CI 1.12 to 5.03) or requested on demand (RR: 1.28, 95% CI 0.90 to 1.82). Meta-analysis showed no statistically significant difference in linkage to clinical assessment/treatment between arms (RR: 1.12, 95% CI 0.80 to 1.57). No studies measured screening frequency or social harms/adverse events. Conclusion A growing evidence base, mainly from high-income countries and with significant heterogeneity, suggests HPV self-sampling can increase cervical cancer screening uptake compared with standard of care, with a marginal effect on linkage to clinical assessment/treatment. Systematic review registration number PROSPERO CRD42018114871.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: SupervisionRole: Writing – original draftRole: Writing – review & editing
                Role: Formal analysisRole: InvestigationRole: MethodologyRole: Writing – original draftRole: Writing – review & editing
                Role: Data curationRole: Writing – original draftRole: Writing – review & editing
                Role: Project administrationRole: Writing – original draftRole: Writing – review & editing
                Role: SupervisionRole: Writing – review & editing
                Role: SupervisionRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS One
                plos
                PLOS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                9 March 2023
                2023
                9 March 2023
                : 18
                : 3
                : e0282853
                Affiliations
                [1 ] Department of Public Health, College of Health and Human Sciences, Purdue University, West Lafayette, Indiana, United States of America
                [2 ] Weldon School of Biomedical Engineering, College of Engineering, Purdue University, West Lafayette, Indiana, United States of America
                [3 ] Indiana University Simon Comprehensive Cancer Center, Cancer Prevention and Control Program, Indianapolis, Indiana, United States of America
                [4 ] Formerly at Department of Nutrition Science, College of Health and Human Sciences, Purdue University, West Lafayette, Indiana, United States of America
                University of Macerata: Universita degli Studi di Macerata, ITALY
                Author notes

                Competing Interests: I have read the journal’s policy and the authors of this manuscript have the following competing interests: NMR holds a US patent (US11136620B2) for a platform device that combines nucleic acid extraction, amplification, and detection to enable rapid testing with visual readout. The remaining authors declare no competing interests. This does not alter our adherence to PLOS ONE policies on sharing data and materials.

                Author information
                https://orcid.org/0000-0002-2633-4397
                https://orcid.org/0000-0002-5616-7913
                https://orcid.org/0000-0002-6153-0713
                Article
                PONE-D-22-30688
                10.1371/journal.pone.0282853
                9997915
                36893182
                339522ca-70c4-4a8b-8440-281a5ba0b194
                © 2023 Rodriguez et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 7 November 2022
                : 24 February 2023
                Page count
                Figures: 2, Tables: 2, Pages: 16
                Funding
                Funded by: National Cancer Institute
                Award ID: K01CA241073
                Award Recipient :
                This work was supported by Grant Number K01CA241073 from the National Institutes of Health, National Cancer Institute, cancer.gov, (Principal Investigator: NMR). The funder had no role in the study, design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
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                Custom metadata
                The full dataset cannot be shared publicly because of potentially sensitive information disclosed by participants. The deidentified data underlying the results presented in the study are available from Dr. Natalia Rodriguez at natalia@ 123456purdue.edu or from Purdue University's Institutional Review Board at irb@ 123456purdue.edu .
                COVID-19

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