Self-Collection for Cervical Screening Programs: From Research to Reality
Abstract
:1. Introduction
2. Materials and Methods
2.1. PCR-Based Technologies for HPV Testing of Self-Collected Specimens
2.2. Non-PCR-Based Technologies for HPV Testing of Self-Collected Specimens
2.2.1. Hologic Aptima
2.2.2. careHPV
2.3. Self-Collection Devices for HPV Testing
2.3.1. Evalyn Brush
2.3.2. Viba-Brush
2.3.3. Qvintip
2.3.4. Copan FLOQSwab
2.4. Other Considerations for Clinical Testing of Self-Collection Specimens for HPV
2.4.1. Validated Assays
2.4.2. Sample Preparation
2.4.3. Pre-Analytic Considerations
3. Discussion
4. Conclusions
- Self-collection is an attractive mechanism to increase participation in cervical screening worldwide. The current evidence strongly supports the need for PCR-based HPV assays with internal controls, specifically for both sample adequacy and detection of inhibition.
- Whilst there does not appear to be major differences in the sensitivity of different collection devices, their cost, acceptability, and scalability as part of population level screening programs need to be considered.
- This area of clinical testing for HPV as part of organized cervical screening programs will likely be a fast evolving one, with the continued development of new HPV assays, pre-analytic devices, and hopefully, manufacturer-validated claims for the use of self-collection.
Author Contributions
Funding
Conflicts of Interest
References
- Arbyn, M.; Weiderpass, E.; Bruni, L.; de Sanjosé, S.; Saraiya, M.; Ferlay, J.; Bray, F. Estimates of incidence and mortality of cervical cancer in 2018: A worldwide analysis. Lancet. Glob. Health 2020, 8, e191–e203. [Google Scholar] [CrossRef] [Green Version]
- Zucchetto, A.; Ronco, G.; Giorgi Rossi, P.; Zappa, M.; Ferretti, S.; Franzo, A.; Falcini, F.; Visioli, C.B.; Zanetti, R.; Biavati, P.; et al. Screening patterns within organized programs and survival of Italian women with invasive cervical cancer. Prev. Med. 2013, 57, 220–226. [Google Scholar] [CrossRef] [PubMed]
- Ibáñez, R.; Alejo, M.; Combalia, N.; Tarroch, X.; Autonell, J.; Codina, L.; Culubret, M.; Bosch, F.X.; de Sanjosé, S. Underscreened women remain overrepresented in the pool of cervical cancer cases in Spain: A need to rethink the screening interventions. Biomed. Res. Int 2015, 2015, 605375. [Google Scholar] [CrossRef] [PubMed]
- Harder, E.; Juul, K.E.; Jensen, S.M.; Thomsen, L.T.; Frederiksen, K.; Kjaer, S.K. Factors associated with non-participation in cervical cancer screening - a nationwide study of nearly half a million women in Denmark. Prev. Med. 2018, 111, 94–100. [Google Scholar] [CrossRef] [PubMed]
- AIHW. Cervical Screening in Australia; Australian Institute of Health and Welfare: Canberra, Australia, 2018. [Google Scholar]
- Chorley, A.J.; Marlow, L.A.V.; Forster, A.S.; Haddrell, J.B.; Waller, J. Experiences of cervical screening and barriers to participation in the context of an organised programme: A systematic review and thematic synthesis. Psychooncology 2017, 26, 161–172. [Google Scholar] [CrossRef] [PubMed]
- Saville, M.; Hawkes, D.; McLachlan, E.; Anderson, S.; Arabena, K. Self-collection for under-screened women in a national cervical screening program: Pilot study. Current Oncology 2018, 25, e27. [Google Scholar] [CrossRef] [Green Version]
- Birdsong, G.G.; Davey, D.D. Specimen adequacy. In The Bethesda System for Reporting Cervical Cytology, 3rd ed.; Nayar, R., Wilbur, D.C., Eds.; Springer: Berlin/Heidelberg, Germany, 2015. [Google Scholar]
- Cancer Council Australia. Cervical Cancer Screening Guidelines Working Party. National Cervical Screening Program: Guidelines for the management of screen-detected abnormalities, screening in specific populations and investigation of abnormal vaginal bleeding. Cancer Council Australia: Sydney, Australia; Available online: https://wiki.cancer.org.au/australia/Guidelines:Cervical_cancer/Screening (accessed on 21 April 2020).
- Arbyn, M.; Smith, S.B.; Temin, S.; Sultana, F.; Castle, P. Detecting cervical precancer and reaching underscreened women by using HPV testing on self samples: Updated meta-analyses. BMJ 2018, 363, k4823. [Google Scholar] [CrossRef] [Green Version]
- Pedersen, H.N.; Smith, L.W.; Racey, C.S.; Cook, D.; Krajden, M.; van Niekerk, D.; Ogilvie, G.S. Implementation considerations using HPV self-collection to reach women under-screened for cervical cancer in high-income settings. Curr. Oncol. Toronto Ont. 2018, 25, e4–e7. [Google Scholar] [CrossRef] [Green Version]
- Franco, E.L. Self-sampling for cervical cancer screening: Empowering women to lead a paradigm change in cancer control. Curr. Oncol. (Toronto Ont.) 2018, 25, e1–e3. [Google Scholar] [CrossRef] [Green Version]
- Ketelaars, P.J.W.; Bosgraaf, R.P.; Siebers, A.G.; Massuger, L.F.A.G.; van der Linden, J.C.; Wauters, C.A.P.; Rahamat-Langendoen, J.C.; van den Brule, A.J.C.; IntHout, J.; Melchers, W.J.G.; et al. High-risk human papillomavirus detection in self-sampling compared to physician-taken smear in a responder population of the Dutch cervical screening: Results of the Vera study. Prev. Med. 2017, 101, 96–101. [Google Scholar] [CrossRef]
- Tranberg, M.; Jensen, J.S.; Bech, B.H.; Blaakær, J.; Svanholm, H.; Andersen, B. Good concordance of HPV detection between cervico-vaginal self-samples and general practitioner-collected samples using the cobas 4800 HPV DNA test. BMC Infect. Dis. 2018, 18, 348. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Leinonen, M.K.; Schee, K.; Jonassen, C.M.; Lie, A.K.; Nystrand, C.F.; Rangberg, A.; Furre, I.E.; Johansson, M.J.; Tropé, A.; Sjøborg, K.D.; et al. Safety and acceptability of human papillomavirus testing of self-collected specimens: a methodologic study of the impact of collection devices and HPV assays on sensitivity for cervical cancer and high-grade lesions. J. Clin. Virol. Off. Publ. Pan Am. Soc. Clin. Virol. 2018, 99, 22–30. [Google Scholar] [CrossRef] [PubMed]
- Jentschke, M.; Chen, K.; Arbyn, M.; Hertel, B.; Noskowicz, M.; Soergel, P.; Hillemanns, P. Direct comparison of two vaginal self-sampling devices for the detection of human papillomavirus infections. J. Clin. Virol. Off. Publ. Pan Am. Soc. Clin. Virol. 2016, 82, 46–50. [Google Scholar] [CrossRef] [PubMed]
- Chen, K.; Ouyang, Y.; Hillemanns, P.; Jentschke, M. Excellent analytical and clinical performance of a dry self-sampling device for human papillomavirus detection in an urban Chinese referral population. J. Obstet. Gynaecol. Res. 2016, 42, 1839–1845. [Google Scholar] [CrossRef] [PubMed]
- Ejegod, D.M.; Pedersen, H.; Alzua, G.P.; Pedersen, C.; Bonde, J. Time and temperature dependent analytical stability of dry-collected Evalyn HPV self-sampling brush for cervical cancer screening. Papillomavirus Res. Amst. Neth. 2018, 5, 192–200. [Google Scholar] [CrossRef] [PubMed]
- Toliman, P.J.; Kaldor, J.M.; Badman, S.G.; Phillips, S.; Tan, G.; Brotherton, J.M.L.; Saville, M.; Vallely, A.J.; Tabrizi, S.N. Evaluation of self-collected vaginal specimens for the detection of high-risk human papillomavirus infection and the prediction of high-grade cervical intraepithelial lesions in a high-burden, low-resource setting. Clin. Microbiol. Infect. Off. Publ. Eur. Soc. Clin. Microbiol. Infect. Dis. 2019, 25, 496–503. [Google Scholar] [CrossRef] [Green Version]
- Woo, Y.L. The feasibility and acceptability of self-sampling and HPV testing using Cepheid Xpert(®) HPV in a busy primary care facility. J. Virus Erad. 2019, 5, 10–11. [Google Scholar]
- Brisson, M.; Kim, J.J.; Canfell, K.; Drolet, M.; Gingras, G.; Burger, E.A.; Martin, D.; Simms, K.T.; Bénard, É.; Boily, M.-C.; et al. Impact of HPV vaccination and cervical screening on cervical cancer elimination: A comparative modelling analysis in 78 low-income and lower-middle-income countries. Lancet Lond. Engl. 2020, 395, 575–590. [Google Scholar] [CrossRef] [Green Version]
- WHO. Who Director-General Calls for All Countries to Take Action to Help End the Suffering Caused by Cervical Cancer. Available online: https://www.who.int/reproductivehealth/call-to-action-elimination-cervical-cancer/en/ (accessed on 10 February 2020).
- WHO. Draft: Global Strategy Towards Eliminating Cervical Cancer as a Public Health Problem; WHO: Geneva, Switzerland, 2019. [Google Scholar]
- NPAAC. Requirements for Laboratories Reporting Tests for the National Cervical Screening Program, 1st ed.; Australian Government Department of Health: Canberra, Australia, 2017. [Google Scholar]
- Saville, M.; Hawkes, D.; Keung, M.H.; Ip, E.; Silvers, J.; Sultana, F.; Malloy, M.; Velentzis, L.; Canfell, K.; Wrede, C.D.; et al. Analytical performance of HPV assays on vaginal self-collected vs practitioner-collected samples: The SCOPE study. J. Clin. Virol. 2020, in press. [Google Scholar] [CrossRef]
- Arbyn, M.; Verdoodt, F.; Snijders, P.J.; Verhoef, V.M.; Suonio, E.; Dillner, L. Accuracy of human papillomavirus testing on self-collected versus clinician-collected samples: a meta-analysis. Lancet Oncol. 2014, 15, 172–183. [Google Scholar] [CrossRef]
- Chernesky, M.; Jang, D.; Gilchrist, J.; Elit, L.; Lytwyn, A.; Smieja, M.; Dockter, J.; Getman, D.; Reid, J.; Hill, C. Evaluation of a new Aptima specimen collection and transportation kit for high-risk human papillomavirus e6/e7 messenger RNA in cervical and vaginal samples. Sex. Transm Dis. 2014, 41, 365–368. [Google Scholar] [CrossRef] [PubMed]
- Asciutto, K.C.; Ernstson, A.; Forslund, O.; Borgfeldt, C. Self-sampling with HPV mRNA analyses from vagina and urine compared with cervical samples. J. Clin. Virol. 2018, 101, 69–73. [Google Scholar] [CrossRef] [PubMed]
- Nieves, L.; Enerson, C.L.; Belinson, S.; Brainard, J.; Chiesa-Vottero, A.; Nagore, N.; Booth, C.; Perez, A.G.; Chavez-Aviles, M.N.; Belinson, J. Primary cervical cancer screening and triage using an mRNA human papillomavirus assay and visual inspection. Int. J. Gynecol. Cancer Off. J. Int. Gynecol. Cancer Soc. 2013, 23, 513–518. [Google Scholar] [CrossRef] [PubMed]
- Borgfeldt, C.; Forslund, O. Increased HPV detection by the use of a pre-heating step on vaginal self-samples analysed by Aptima HPV assay. J. Virol. Methods 2019, 270, 18–20. [Google Scholar] [CrossRef] [PubMed]
- Cuschieri, K.; Geraets, D.; Cuzick, J.; Cadman, L.; Moore, C.; Vanden Broeck, D.; Padalko, E.; Quint, W.; Arbyn, M. Performance of a cartridge-based assay for detection of clinically significant human papillomavirus (HPV) infection: Lessons from VALGENT (Validation of HPV genotyping tests). J. Clin. Microbiol. 2016, 54, 2337–2342. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Brotherton, J.M.; Hawkes, D.; Sultana, F.; Malloy, M.J.; Machalek, D.A.; Smith, M.A.; Garland, S.M.; Saville, M. Age-specific HPV prevalence among 116,052 women in Australia’s renewed cervical screening program: A new tool for monitoring vaccine impact. Vaccine 2019, 37, 412–416. [Google Scholar] [CrossRef] [PubMed]
- Machalek, D.A.; Roberts, J.M.; Garland, S.M.; Thurloe, J.; Richards, A.; Chambers, I.; Sivertsen, T.; Farnsworth, A. Routine cervical screening by primary HPV testing: Early findings in the renewed national cervical screening program. Med. J. Aust. 2019, 211, 113–119. [Google Scholar] [CrossRef] [Green Version]
- Vassilakos, P.; Catarino, R.; Bougel, S.; Munoz, M.; Benski, C.; Meyer-Hamme, U.; Jinoro, J.; Heriniainasolo, J.L.; Petignat, P. Use of swabs for dry collection of self-samples to detect human papillomavirus among Malagasy women. Infect. Agents Cancer 2016, 11, 13. [Google Scholar] [CrossRef] [Green Version]
- Chen, W.; Jeronimo, J.; Zhao, F.-H.; Qiao, Y.-L.; Valdez, M.; Zhang, X.; Kang, L.-N.; Bansil, P.; Paul, P.; Bai, P.; et al. The concordance of HPV DNA detection by hybrid capture 2 and careHPV on clinician- and self-collected specimens. J. Clin. Virol. 2014, 61, 553–557. [Google Scholar] [CrossRef]
- Obiri-Yeboah, D.; Adu-Sarkodie, Y.; Djigma, F.; Hayfron-Benjamin, A.; Abdul, L.; Simpore, J.; Mayaud, P. Self-collected vaginal sampling for the detection of genital human papillomavirus (HPV) using CareHPV among Ghanaian women. BMC Women’s Health 2017, 17, 1–6. [Google Scholar] [CrossRef] [Green Version]
- Baussano, I.; Tshering, S.; Choden, T.; Lazzarato, F.; Tenet, V.; Plummer, M.; Franceschi, S.; Clifford, G.M.; Tshomo, U. Cervical cancer screening in rural Bhutan with the careHPV test on self-collected samples: An ongoing cross-sectional, population-based study (Reach-Bhutan). BMJ Open 2017, 7. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Swanson, M.; Ibrahim, S.; Blat, C.; Oketch, S.; Olwanda, E.; Maloba, M.; Huchko, M.J. Evaluating a community-based cervical cancer screening strategy in western Kenya: A descriptive study. BMC Womens Health 2018, 18, 116. [Google Scholar] [CrossRef] [PubMed]
- Tin-Oo, C.; Hlaing, H.N.T.; Nandar, C.S.; Aung, T.; Fishbein, D. Why the cost of purchasing the careHPV test in Myanmar was many times greater than that reported in the international literature. J. Glob. Oncol. 2018, 4, 49s. [Google Scholar] [CrossRef]
- Polman, N.J.; Ebisch, R.M.F.; Heideman, D.A.M.; Melchers, W.J.G.; Bekkers, R.L.M.; Molijn, A.C.; Meijer, C.J.L.M.; Quint, W.G.V.; Snijders, P.J.F.; Massuger, L.F.A.G.; et al. Performance of human papillomavirus testing on self-collected versus clinician-collected samples for the detection of cervical intraepithelial neoplasia of grade 2 or worse: A randomised, paired screen-positive, non-inferiority trial. Lancet. Oncol. 2019, 20, 229–238. [Google Scholar] [CrossRef]
- Van Baars, R.; Bosgraaf, R.P.; ter Harmsel, B.W.A.; Melchers, W.J.G.; Quint, W.G.V.; Bekkers, R.L.M. Dry storage and transport of a cervicovaginal self-sample by use of the Evalyn brush, providing reliable human papillomavirus detection combined with comfort for women. J. Clin. Microbiol. 2012, 50, 3937–3943. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Leeman, A.; Del Pino, M.; Molijn, A.; Rodriguez, A.; Torné, A.; de Koning, M.; Ordi, J.; van Kemenade, F.; Jenkins, D.; Quint, W. HPV testing in first-void urine provides sensitivity for CIN2+ detection comparable with a smear taken by a clinician or a brush-based self-sample: Cross-sectional data from a triage population. BJOG Int. J. Obstet. Gynaecol. 2017, 124, 1356–1363. [Google Scholar] [CrossRef]
- Geraets, D.T.; van Baars, R.; Alonso, I.; Ordi, J.; Torné, A.; Melchers, W.J.G.; Meijer, C.J.L.M.; Quint, W.G.V. Clinical evaluation of high-risk HPV detection on self-samples using the indicating FTA-elute solid-carrier cartridge. J. Clin. Virol. Off. Publ. Pan Am. Soc. Clin. Virol. 2013, 57, 125–129. [Google Scholar] [CrossRef]
- Dijkstra, M.G.; Heideman, D.A.M.; van Kemenade, F.J.; Hogewoning, K.J.A.; Hesselink, A.T.; Verkuijten, M.C.G.T.; van Baal, W.M.; Boer, G.M.N.-d.; Snijders, P.J.F.; Meijer, C.J.L.M. Brush-based self-sampling in combination with GP5+/6+-PCR-based HRHPV testing: High concordance with physician-taken cervical scrapes for HPV genotyping and detection of high-grade CIN. J. Clin. Virol. Off. Publ. Pan Am. Soc. Clin. Virol. 2012, 54, 147–151. [Google Scholar] [CrossRef]
- Aiko, K.Y.; Yoko, M.; Saito, O.M.; Ryoko, A.; Yasuyo, M.; Mikiko, A.S.; Takeharu, Y.; Fumiki, H.; Etsuko, M. Accuracy of self-collected human papillomavirus samples from Japanese women with abnormal cervical cytology. J. Obstet. Gynaecol. Res. 2017, 43, 710–717. [Google Scholar] [CrossRef]
- Gyllensten, U.; Sanner, K.; Gustavsson, I.; Lindell, M.; Wikstrom, I.; Wilander, E. Short-time repeat high-risk HPV testing by self-sampling for screening of cervical cancer. Br. J. Cancer 2011, 105, 694–697. [Google Scholar] [CrossRef] [Green Version]
- Sanner, K.; Wikstrom, I.; Strand, A.; Lindell, M.; Wilander, E. Self-sampling of the vaginal fluid at home combined with high-risk HPV testing. Br. J. Cancer 2009, 101, 871–874. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Stenvall, H.; Wikstrom, I.; Wilander, E. High prevalence of oncogenic human papilloma virus in women not attending organized cytological screening. Acta Dermato Venereol. 2007, 87, 243–245. [Google Scholar] [PubMed]
- Wikstrom, I.; Lindell, M.; Sanner, K.; Wilander, E. Self-sampling and HPV testing or ordinary Pap-smear in women not regularly attending screening: A randomised study. Br. J. Cancer 2011, 105, 337–339. [Google Scholar] [CrossRef] [PubMed]
- Aprovix. Qvintip Instructions for Use. 2019, p. 1. Available online: http://www.genoid.net/images/uploads/sy_Qvintip_user_guide_20160531.pdf (accessed on 21 April 2020).
- Viviano, M.; Willame, A.; Cohen, M.; Benski, A.C.; Catarino, R.; Wuillemin, C.; Tran, P.L.; Petignat, P.; Vassilakos, P. A comparison of cotton and flocked swabs for vaginal self-sample collection. Int. J. Womens Health 2018, 10, 229–236. [Google Scholar] [CrossRef] [Green Version]
- Catarino, R.; Vassilakos, P.; Bilancioni, A.; Vanden Eynde, M.; Meyer-Hamme, U.; Menoud, P.-A.; Guerry, F.; Petignat, P. Randomized comparison of two vaginal self-sampling methods for human papillomavirus detection: Dry swab versus FTA cartridge. PLoS ONE 2015, 10, e0143644. [Google Scholar] [CrossRef]
- Meijer, C.J.; Berkhof, J.; Castle, P.E.; Hesselink, A.T.; Franco, E.L.; Ronco, G.; Arbyn, M.; Bosch, F.X.; Cuzick, J.; Dillner, J.; et al. Guidelines for human papillomavirus DNA test requirements for primary cervical cancer screening in women 30 years and older. Int. J. Cancer 2009, 124, 516–520. [Google Scholar] [CrossRef] [Green Version]
- Arbyn, M.; Depuydt, C.; Benoy, I.; Bogers, J.; Cuschieri, K.; Schmitt, M.; Pawlita, M.; Geraets, D.; Heard, I.; Gheit, T.; et al. VALGENT: A protocol for clinical validation of human papillomavirus assays. J. Clin. Virol. 2016, 76 (Suppl. S1), S14–S21. [Google Scholar] [CrossRef]
- Stanczuk, G.; Baxter, G.; Currie, H.; Lawrence, J.; Cuschieri, K.; Wilson, A.; Arbyn, M. Clinical validation of HRHPV testing on vaginal and urine self-samples in primary cervical screening (cross-sectional results from the Papillomavirus Dumfries and Galloway—PAVDAG study). BMJ Open 2016, 6, e010660. [Google Scholar] [CrossRef]
- Asciutto, K.C.; Henningsson, A.J.; Borgfeldt, H.; Darlin, L.; Borgfeldt, C. Vaginal and urine self-sampling compared to cervical sampling for HPV-testing with the cobas 4800 HPV test. Anticancer. Res. 2017, 37, 4183–4187. [Google Scholar]
- Lam, J.U.H.; Rebolj, M.; Ejegod, D.M.; Pedersen, H.; Rygaard, C.; Lynge, E.; Harder, E.; Thomsen, L.T.; Kjaer, S.K.; Bonde, J. Prevalence of human papillomavirus in self-taken samples from screening nonattenders. J. Clin. Microbiol. 2017, 55, 2913–2923. [Google Scholar] [CrossRef] [Green Version]
- Arbyn, M.; Peeters, E.; Benoy, I.; Vanden Broeck, D.; Bogers, J.; De Sutter, P.; Donders, G.; Tjalma, W.; Weyers, S.; Cuschieri, K.; et al. Valhudes: A protocol for validation of human papillomavirus assays and collection devices for HPV testing on self-samples and urine samples. J. Clin. Virol. 2018, 107, 52–56. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pattyn, J.; Van Keer, S.; Téblick, L.; Van Damme, P.; Vorsters, A. HPV DNA detection in urine samples of women: ’An efficacious and accurate alternative to cervical samples?’. Expert Rev. Anti-Infect. Ther. 2019, 17, 755–757. [Google Scholar] [CrossRef] [PubMed]
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Hawkes, D.; Keung, M.H.T.; Huang, Y.; McDermott, T.L.; Romano, J.; Saville, M.; Brotherton, J.M.L. Self-Collection for Cervical Screening Programs: From Research to Reality. Cancers 2020, 12, 1053. https://doi.org/10.3390/cancers12041053
Hawkes D, Keung MHT, Huang Y, McDermott TL, Romano J, Saville M, Brotherton JML. Self-Collection for Cervical Screening Programs: From Research to Reality. Cancers. 2020; 12(4):1053. https://doi.org/10.3390/cancers12041053
Chicago/Turabian StyleHawkes, David, Marco H. T. Keung, Yanping Huang, Tracey L. McDermott, Joanne Romano, Marion Saville, and Julia M. L. Brotherton. 2020. "Self-Collection for Cervical Screening Programs: From Research to Reality" Cancers 12, no. 4: 1053. https://doi.org/10.3390/cancers12041053