Cervical cancer screening using a sampling device: efficiency and acceptability
To analyze the data available in the literature on the efficiency of using a self-sampling technique as part of cervical cancer (CC) screening. It is noted that an increase the number of women to be examined and optimization of techniques for high-risk human papillomavirus (hr-HPV) typing are currently considered as main areas for improvement of CC screening programs. Self-sampling shows a high concordance with physician-taken sampling for HPV detection. The possibilities of delivering self-sampling devices directly to women’s homes as part of CC screening programs are considered.There is an urgent need for new approaches to screening with self-sampling devices that are economically affordable, can be easily mailed to the women to be examined, acceptable and convenient to use, technically reliable and compatible with the techniques used to detect hr-HPV.Bashirova L.K., Apolikhina I.A., Pavlovich S.V.
Keywords
cervical cancer
human papillomavirus
cervical intraepithelial neoplasia
screening
cervicovaginal self-sampling
References
- Аполихина И.А., Филиппенкова Е.В., Додова Е.Г., Гасанова Г.Ф., Горбунова Е.А. Современные возможности организованного скрининга рака шейки матки. Акушерство и гинекология. 2016; 9: 12–8. [Apolikhina I.A., Filippenkova E.V., Dodova E.G., Gasanova G.F., Gorbunova E.A. Current possibilities of organized screening for cancer of the cervix uteri. Obstetrics and Gynecology/Akusherstvo i ginekologiya. 2016; (9): 12–8. (in Russian).]. https://dx.doi.org/10.18565/aig.2016.9.12–8.
- Левшин В.Ф., Завельская А.Я. Факторы риска и профилактика рака шейки матки. Вопросы онкологии. 2017; 63(3): 506–16. [Levshin V.F., Zavelskaya A.Ya. Risk factors and prevention of cervical cancer. Problems in Oncology/Voprosy onkologii. 2017; 63(3): 506–16. (in Russian).].
- Andersson S., Belkic K., Demirbuker S.S., Mints M., Ostensson E. Perceived cervical cancer risk among women treated for high-grade cervical intraepithelial neoplasia: The importance of specific knowledge. PLoS One. 2017; 12(12): e0190156. https://dx.doi.org/10.1371/journal.pone.0190156.
- Andrae B., Andersson T.M., Lambert P.C., Kemetli L., Silfverdal L., Strander B. et al. Screening and cervical cancer cure: population based cohort study. BMJ. 2012; 344: e900. https://dx.doi.org/10.1136/bmj.e900.
- Vaccarella S., Franceschi S., Engholm G., Lonnberg S., Khan S., Bray F. 50 years of screening in the Nordic countries: quantifying the effects on cervical cancer incidence. Br. J. Cancer. 2014; 111(5): 965–9. https://dx.doi.org/10.1038/bjc.2014.362.
- Crossley B., Crossley J. A review of the use of human papilloma virus (HPV) in cervical screening. Br. J. Biomed. Sci. 2017; 74(3): 105–9. https://dx.doi.org/10.1080/09674845.2017.1332555.
- Tjalma W.A. The ideal cervical cancer screening recommendation for Belgium, an industrialized country in Europe. Eur. J. Gynaecol. Oncol. 2014; 35(3): 211–8. https://dx.doi.org/10.1016/j.cmi.2017.05.020.
- Saslow D., Solomon D., Lawson H.W., Killackey M., Kulasingam S.L., Cain J. et al. American Cancer Society, American Society for Colposcopy and Cervical Pathology, and American Society for Clinical Pathology screening guidelines for the prevention and early detection of cervical cancer. Am. J. Clin. Pathol. 2012; 137(4): 516–42. https://dx.doi.org/10.1309/AJCPTGD94EVRSJCG.
- Arbyn M., Anttila A., Jordan J., Ronco G., Schenck U., Segnan N. et al. European Guidelines for Quality Assurance in Cervical Cancer Screening: Second edition - summary document. Ann. Oncol. 2010; 21(3): 448–58. https://dx.doi.org/10.1093/annonc/mdp471.
- 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(12): 1839–45. https://dx.doi.org/10.1111/jog.13132.
- Zhou H., Mody R.R., Luna E., Armylagos D., Xu J., Schwartz M.R. et al. Clinical performance of the Food and Drug Administration-Approved high-risk HPV test for the detection of high-grade cervicovaginal lesions. Cancer Cytopathol. 2016; 124(5): 317–23. https://dx.doi.org/10.1002/cncy.21687.
- Kyrgiou M., Kalliala I., Mitra A., Ng K.Y., Raglan O., Fotopoulou C., et al. Immediate referral to colposcopy versus cytological surveillance for low-grade cervical cytological abnormalities in the absence of HPV test: A systematic review and a meta-analysis of the literature. Int. J. Cancer. 2017; 140(1): 216–23. https://dx.doi.org/10.1002/ijc.30419.
- Arbyn M., Ronco G., Anttila A., Meijer C.J., Poljak M., Ogilvie G. et al. Evidence regarding human papillomavirus testing in secondary prevention of cervical cancer. Vaccine. 2012; 30(Suppl. 5): F88–99. https://dx.doi.org/10.1016/j.vaccine.2012.06.095.
- Dillner J., Rebolj M., Birembaut P., Petry K.U., Szarewski A., Munk C. et al.; Joint European Cohort Study. Long term predictive values of cytology and human papillomavirus testing in cervical cancer screening: joint European cohort study. BMJ. 2008; 337: a1754. https://dx.doi.org/10.1136/bmj.a1754.
- Verdoodt F., Jentschke M., Hillemanns P., Racey C.S., Snijders P.J.F., Arbyn M. Reaching women who do not participate in the regular cervical cancer screening programme by offering self-sampling kits: A systematic review and meta-analysis of randomised trials. Eur. J. Cancer. 2015; 51(16): 2375–85. https://dx.doi.org/10.1016/j.ejca.2015.07.006.
- Tamalet C., Le Retraite L., Leandri F.X., Heid P., Garnier H.S., Piana L. et al. Vaginal self-sampling is an adequate means of screening HR-HPV types in women not participating in regular cervical cancer screening. Clin. Microbiol. Infect. 2013; 19(1): 44–50. https://dx.doi.org/10.1111/1469-0691.12063.
- Andersson S., Belkic K., Mints M., Ostensson E. Is self-sampling to test for high-risk papillomavirus an acceptable option among women who have been treated for high-grade cervical intraepithelial neoplasia? PLoS One. 2018; 13(6): e0199038. https://dx.doi.org/10.1371/journal.pone.0199038.
- Аполихина И.А., Баширова Л.К., Горбунова Е.А. Возможности применения теста самозабора материала при скрининге рака шейки матки (обзор литературы). Гинекология. 2018; 20(3): 57–60. [Apolikhina I.A., Bashirova L.K., Gorbunova E.A. Possibilities of the self-sampling method application in the cervical cancer screening (review). Gynecology/Ginekologiya. 2018; 20(3): 57–60. (in Russian).]. https://dx.doi.org/10.26442/2079-5696_2018.3.57-60.
- Arbyn M., Verdoodt F., Snijders P.J., Verhoef V.M., Suonio E., Dillner L. et al. Accuracy of human papillomavirus testing on self-collected versus clinician-collected samples: A meta-analysis. Lancet Oncol. 2014; 15(2): 172–83. https://dx.doi.org/10.1016/S1470-2045(13)70570-9.
- Arbyn M., Castle P. Offering self-sampling kits for HPV testing to reach women who do not attend in the regular cervical cancer screening program. Cancer Epidemiol. Biomarkers Prev. 2015; 24(5): 769–72. https://dx.doi.org/10.1158/1055-9965.EPI-14-1417.
- Nelson E.J., Maynard B.R., Loux T., Fatla J., Gordon R., Arnold L.D. The acceptability of self-sampled screening for HPV DNA: a systematic review and meta-analysis. Sex. Transm. Infect. 2017; 9(1): 56–61. https://dx.doi.org/10.1136/sextrans-2016-052609.
- 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(1): 348. https://dx.doi.org/10.1186/s12879-018-3254-y.
- Schmeink C.E., Bekkers R.L., Massuger L.F., Melchers W.J. The potential role of self-sampling for high-risk human papillomavirus detection in cervical cancer screening. Rev. Med. Virol. 2011; 21(3): 139–53. https://dx.doi.org/10.1002/rmv.686.
- Ketelaars P., Bosgraaf R., Siebers A., Massuger L., van der Linden J., Wauters C. et al. High-risk human papillomavirus detection in self-sampling compared to physiciantaken smear in a responder population of the Dutch cervical screening: results of the VERA study. Prev. Med. 2017; 101: 96–101. https://dx.doi.org/10.1016/j.ypmed.2017.05.021.
- Van Baars R., Bosgraaf R.P., ter Harmsel B.W., Melchers W.J., Quint W.G., Bekkers R.L. 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(12): 3937–43. https://dx.doi.org/10.1128/JCM.01506-12.
- Racey C.S., Withrow D.R., Gesink D. Self-collected HPV testing improves participation in cervical cancer screening: a systematic review and meta-analysis. Can. J. Public Health. 2013; 104(2): e159–66.
- Pathak N., Dodds J., Zamora J., Khan K. Accuracy of urinary human papillomavirus testing for presence of cervical HPV: systematic review and meta-analysis. BMJ. 2014; 349: g5264. https://dx.doi.org/10.1136/bmj.g5264.
- Sahasrabuddhe V.V., Gravitt P.E., Dunn S.T., Brown D., Allen R.A., Eby Y.J. et al. Comparison of human papillomavirus detections in urine, vulvar, and cervical samples from women attending a colposcopy clinic. J. Clin. Microbiol. 2014; 52(1): 187–92. https://dx.doi.org/10.1128/JCM.01623-13.
- Stanczuk G.A., Currie H., Baxter G., Foster A., Gibson L., Graham C., Cuschieri K. Cobas 4800 HPV detection in the cervical, vaginal and urine samples of women with high-grade CIN before and after treatment. J. Clin. Pathol. 2015; 68(7): 567–70. https://dx.doi.org/10.1136/jclinpath-2014-202851.
- Vorsters A., Van den Bergh J., Micalessi I., Biesmans S., Bogers J., Hens A. et al. Optimization of HPV DNA detection in urine by improving collection, storage, and extraction. Eur. J. Clin. Microbiol. Infect. Dis. 2014; 33(11): 2005–14. https://dx.doi.org/10.1007/s10096-014-2147-2.
- Van Keer S., Pattyn J., Tjalma W.A.A., Van Ostade X., Ieven M., Van Damme P., Vorsters A. First-void urine: A potential biomarker source for triage of high-risk human papillomavirus infected women. Eur. J. Obstet. Gynecol. Reprod. Biol. 2017; 216: 1–11. https://dx.doi.org/10.1016/j.ejogrb.2017.06.036.
- Rozemeijer K., de Kok I.M., Naber S.K., van Kemenade F.J., Penning C., van Rosmalen J., van Ballegooijen M. Offering self-sampling to non-attendees of organized primary HPV screening: When do harms outweigh the benefits? Cancer Epidemiol. Biomarkers Prev. 2015; 24(5): 773–82. https://dx.doi.org/10.1158/1055-9965.EPI-14-0998.
- Giorgi Rossi P., Fortunato C., Barbarino P., Boveri S., Caroli S., Del Mistro A. et al. Self-sampling to increase participation in cervical cancer screening: an RCT comparing home mailing, distribution in pharmacies, and recall letter. Br. J. Cancer. 2015; 112(4): 667–75. https://dx.doi.org/10.1038/bjc.2015.11.
- Lam J.U., Rebolj M., Møller Ejegod D., Pedersen H., Rygaard C., Lynge E. et al. Human papillomavirus self-sampling for screening non-attenders: Opt-in pilot implementation with electronic communication platforms. Int. J. Cancer. 2017; 140(11): 2212–9. https://dx.doi.org/10.1002/ijc.30647.
- Giorgi Rossi P., Marsili L.M., Camilloni L., Iossa A., Lattanzi A., Sani C. et al. The effect of self-sampled HPV testing on participation to cervical cancer screening in Italy: a randomised controlled trial (ISRCTN96071600). Br. J. Cancer. 2011; 104(2): 248–54. https://dx.doi.org/10.1038/sj.bjc.6606040.
- Arrossi S., Paolino M., Thouyaret L., Laudi R., Campanera A. Evaluation of scaling-up of HPV self-collection offered by community health workers at home visits to increase screening among socially vulnerable under-screened women in Jujuy Province, Argentina. Implement. Sci. 2017; 12(1): 17. https://dx.doi.org/10.1186/s13012-017-0548-1.
- Leinonen M.K., Schee K., Jonassen C.M., Lie A.K., Nystrand C.F., Rangberg A. 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. 2018; 99-100: 22–30. https://dx.doi.org/10.1016/j.jcv.2017.12.008.
- Tranberg M., Bech B.H., Blaakær J., Jensen J.S., Svanholm H., Andersen B. HPV self-sampling in cervical cancer screening: the effect of different invitation strategies in various socioeconomic groups – a randomized controlled trial. Clin. Epidemiol. 2018; 10: 1027–36. https://dx.doi.org/10.2147/CLEP.S164826. eCollection 2018.
- Ingemann-Hansen O., Lidang M., Niemann I., Dinesen J., Baandrup U., Svanholm H., Petersen L. Screening history of women with cervical cancer: a 6-year study in Aarhus, Denmark. Br. J. Cancer. 2008; 98(7): 1292–4. https://dx.doi.org/10.1038/sj.bjc.6604293.
- Spence A.R., Goggin P., Franco E.L. Process of care failures in invasive cervical cancer: systematic review and meta-analysis. Prev. Med. 2007; 45(2-3): 93–106. https://dx.doi.org/10.1016/j.ypmed.2007.06.007.
- Jensen K.E., Hannibal C.G., Nielsen A., Jensen A., Nøhr B., Munk C., Kjaer S.K. Social inequality and incidence of and survival from cancer of the female genital organs in a population-based study in Denmark, 1994-2003. Eur. J. Cancer. 2008; 44(14): 2003–17. https://dx.doi.org/10.1016/j.ejca.2008.06.014.
- Ronco G., Dillner J., Elfström K.M., Tunesi S., Snijders P.J., Arbyn M. et al. Efficacy of HPV-based screening for prevention of invasive cervical cancer: follow-up of four European randomised controlled trials. Lancet. 2014; 383(9916): 524–32. https://dx.doi.org/10.1016/S0140-6736(13)62218-7.
- Sancho-Garnier H., Tamalet C., Halfon P., Leandri F.X., Le Retraite L., Djoufelkit K. et al. HPV self-sampling or the Pap-smear: a randomized study among cervical screening nonattenders from lower socioeconomic groups in France. Int. J. Cancer. 2013; 133(11): 2681–7. https://dx.doi.org/10.1002/ijc.28283.
- Sultana F., English D.R., Simpson J.A., Drennan K.T., Mullins R., Brotherton J.M. et al. Home-based HPV selfsampling improves participation by never-screened and under-screened women: results from a large randomized trial (iPap) in Australia. Int. J. Cancer. 2016; 139(2): 281–90. https://dx.doi.org/10.1002/ijc.30031.
- Gök M., Heideman D.A., van Kemenade F.J., de Vries A.L., Berkhof J., Rozendaal L. et al. Offering self-sampling for human papillomavirus testing to non-attendees of the cervical screening programme: characteristics of the responders. Eur J Cancer. 2012; 48(12): 1799–808.: https://dx.doi.org/10.1016/j.ejca.2011.11.022.
- Virtanen A., Anttila A., Luostarinen T., Nieminen P. Self-sampling versus reminder letter: effects on cervical cancer screening attendance and coverage in Finland. Int. J. Cancer. 2011; 128(11): 2681–7. https://dx.doi.org/10.1002/ijc.25581.
- Snellenberg S., De Strooper L.M., Hesselink A.T., Meijer C.J., Snijders P.J., Heideman D.A., Steenbergen R.D. Development of a multiplex methylation-specific PCR as candidate triage test for women with an HPV-positive cervical scrape. BMC Cancer. 2012; 12: 551–3. https://dx.doi.org/10.1186/1471-2407-12-551.
Received 27.11.2019
Accepted 29.11.2019
About the Authors
Lala K. Bashirova, postgraduate at the Department of Obstetrics, Gynecology, Perinatology and Reproductology of the First Moscow State Medical University namedafter I.М. Sechenov of the Ministry of Health of the Russian Federation (Sechenov University), e-mail: leyla9296@hotmail.com
Inna A. Apolikhina, Doctor of Medicine, Head of the Department of Aesthetic Gynecology and Rehabilitation of the National Medical Research Center for Obstetrics, Gynecology and Perinatology named after the Academician V.I.Kulakov, Professor of the Department of Obstetrics, Gynecology and Perinatology, First Moscow State Medical University named after I.M. Sechenov of the Ministry of Health of the Russian Federation (Sechenov University), e-mail: i_apolikhina@oparina4.ru
Stanislav V. Pavlovich, MD, scientific secretary in Federal State Budget Institution “National Medical Research Center for Obstetrics, Gynecology and Perinatology named
after Academician V.I. Kulakov” Ministry of Health of Russia; Professor of the Department of Obstetrics, Gynecology and Perinatology, First Moscow State Medical University named after I.M. Sechenov of the Ministry of Health of the Russian Federation (Sechenov University), E-mail: st.pavlovich@mail.ru
For citation: Bashirova L.K., Apolikhina I.A., Pavlovich S.V.
Cervical cancer screening using a sampling device: efficiency and acceptability.
Akusherstvo i Ginekologiya/ Obstetrics and gynecology. 2020;2: 50-61 (In Russian).
https://dx.doi.org/10.18565/aig.2020.2.50-61