Quality control of cervical cytology using a 3-type HPV mRNA test increases screening program sensitivity of cervical intraepithelial neoplasia grade 2+ in young Norwegian women—A cohort study

English version

Autoři: Bjørn Westre ^aff001; Anita Giske ^aff001; Hilde Guttormsen ^aff001; Sveinung Wergeland Sørbye ^aff002; Finn Egil Skjeldestad ^aff003
Působiště autorů: Department of Pathology, Ålesund Hospital, Møre and Romsdal Health Trust, Ålesund, Norway ^aff001; Department of Clinical Pathology, University Hospital of North Norway, Tromsø, Norway ^aff002; Research Group Epidemiology of Chronic Diseases, Department of Community Medicine, UiT The Arctic University of Norway, Tromsø, Norway ^aff003
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0221546

Souhrn

Within 2021, Norway intends to complete implementation of HPV DNA-based primary screening for cervical cancer for women 34–69 years, while continue cytology-based screening for women 25–33 years. Over the recent years, the incidence of cervical cancer has increased by 30% among women younger than 40 years. In this subset of women, nearly 30% were diagnosed with a normal smear, as most recent smear, prior the cancer diagnosis. This observation demands quality control of normal smears. The aim of this study was to assess increase in program sensitivity of CIN2+ after follow-up of women with false negative Pap-smears testing positive for a 3-type (-16, -18, -45) HPV mRNA test in a cohort design over one screening interval. 521 women, aged 23–39 years, and no prior history of CIN1+ or HSIL, with an ASC-US or worse smear (ASC-US+) and 1444 women with normal screening cytology comprised the study cohorts. The positivity rate for the 3-type HPV mRNA was 1.9% (28/1444). Rescreening revealed 23 women with ASC-US, two women with LSIL, two women with ASC-H, and one woman with AGUS. If the HPV mRNA-positivity rate and histology findings from samples rescreened were applied to all women with normal cytology, an estimated increase in screening sensitivity of 16.4% (95% CI:15.3–17.5) for CIN2+ and 17.3% (95% CI:16.2–18.4) for CIN3+ were achieved. By rescreening less than 2% of women with normal cytology positive for a 3-type HPV mRNA test, we achieved a significant increase in screening program sensitivity.

Klíčová slova:

Human papillomavirus – Cytology – Cancer detection and diagnosis – Cancer screening – Cervical cancer – Lesions – Carcinogenesis – Biopsy

Zdroje

1. Lonnberg S, Hansen BT, Haldorsen T, Campbell S, Schee K, Nygard M (2015) Cervical cancer prevented by screening: Long-term incidence trends by morphology in Norway. Int J Cancer 137: 1758–1764. doi: 10.1002/ijc.29541 25833121

2. Moyer VA (2012) Screening for cervical cancer: U.S. Preventive Services Task Force recommendation statement. Ann Intern Med 156: 880–91, W312. doi: 10.7326/0003-4819-156-12-201206190-00424 22711081

3. Sasieni P, Castanon A, Cuzick J (2009) Effectiveness of cervical screening with age: population based case-control study of prospectively recorded data. BMJ 339: b2968. doi: 10.1136/bmj.b2968 19638651

4. Vaccarella S, Lortet-Tieulent J, Plummer M, Franceschi S, Bray F (2013) Worldwide trends in cervical cancer incidence: impact of screening against changes in disease risk factors. Eur J Cancer 49: 3262–3273. doi: 10.1016/j.ejca.2013.04.024 23751569

5. Engholm G, Ferlay J, Christensen N, Bray F, Gjerstorff ML, Klint A, et al. (2010) NORDCAN—a Nordic tool for cancer information, planning, quality control and research. Acta Oncol 49: 725–736. doi: 10.3109/02841861003782017 20491528

6. Lonnberg S, Anttila A, Luostarinen T, Nieminen P (2012) Age-specific effectiveness of the Finnish cervical cancer screening programme. Cancer Epidemiol Biomarkers Prev 21: 1354–1361. doi: 10.1158/1055-9965.EPI-12-0162 22665576

7. Arbyn M, Ronco G, Anttila A, Meijer CJ, Poljak M, Ogilvie G, et al. (2012) Evidence regarding human papillomavirus testing in secondary prevention of cervical cancer. Vaccine 30 Suppl 5: F88–F99.

8. Kitchener C, Canfell K, Gilham C, Sargent A, Roberts C, Desai M, et al. (2014) The clinical effectiveness and cost-effectiveness of primary human papillomavirus cervical screening in England: extended follow-up of the ARTISTIC randomised trial cohort through three screening rounds. Health Technol Assess 18: 1–196.

9. Ronco G, Dillner J, Elfstrom KM, Tunesi S, Snijders PJ, Arbyn M, et al. (2014) Efficacy of HPV-based screening for prevention of invasive cervical cancer: follow-up of four European randomised controlled trials. Lancet 383: 524–532. doi: 10.1016/S0140-6736(13)62218-7 24192252

10. Naber SK, de Kok IM, Matthijsse SM, van Ballegooijen M (2016) The potential harms of primary human papillomavirus screening in over-screened women: a microsimulation study. Cancer Causes Control 27: 569–581. doi: 10.1007/s10552-016-0732-7 26970740

11. Rebolj M, Bonde J, Ejegod D, Preisler S, Rygaard C, Lynge E (2015) A daunting challenge: Human Papillomavirus assays and cytology in primary cervical screening of women below age 30years. Eur J Cancer 51: 1456–1466. doi: 10.1016/j.ejca.2015.04.012 25979832

12. Ronco G, Giorgi RP, Giubilato P, Del Mistro A, Zappa M, Carozzi F (2015) A first survey of HPV-based screening in routine cervical cancer screening in Italy. Epidemiol Prev 39: 77–83.

13. Arbyn M, Castellsague X, de Sanjose S, Bruni L, Saraiya M, Bray F, et al. (2011) Worldwide burden of cervical cancer in 2008. Ann Oncol 12: 2675–2686.

14. Arbyn M, Tommasino M, Depuydt C, Dillner J (2014) Are 20 human papillomavirus types causing cervical cancer? J Pathol 234: 431–435. doi: 10.1002/path.4424 25124771

15. de Sanjose S, Quint WG, Alemany L, Geraets DT, Klaustermeier JE, Lloveras B, et al. (2010) Human papillomavirus genotype attribution in invasive cervical cancer: a retrospective cross-sectional worldwide study. Lancet Oncol 11: 1048–1056. doi: 10.1016/S1470-2045(10)70230-8 20952254

16. Powell N, Cuschieri K, Cubie H, Hibbitts S, Rosillon D, De Souza SC, et al. (2013) Cervical cancers associated with human papillomavirus types 16, 18 and 45 are diagnosed in younger women than cancers associated with other types: a cross-sectional observational study in Wales and Scotland (UK). J Clin Virol 58: 571–574. doi: 10.1016/j.jcv.2013.08.020 24051043

17. Holl K, Nowakowski AM, Powell N, McCluggage WG, Pirog EC, Collas De S S, et al. (2015) Human papillomavirus prevalence and type-distribution in cervical glandular neoplasias: Results from a European multinational epidemiological study. Int J Cancer 137: 2858–2868. doi: 10.1002/ijc.29651 26096203

18. Tjalma WA, Fiander A, Reich O, Powell N, Nowakowski AM, Kirschner B, et al. (2013) Differences in human papillomavirus type distribution in high-grade cervical intraepithelial neoplasia and invasive cervical cancer in Europe. Int J Cancer 132: 854–867. doi: 10.1002/ijc.27713 22752992

19. Nygard M (2012) Økning i forekomst av livmorhalskreft hos unge. [Increasing incidence of cervical cancer in young women]. https://www.kreftregisteret.no/Generelt/Nyheter/Okning-i-forekomst-av-livmorhalskreft-hos-unge/

20. Castanon A, Ferryman S, Patnick J, Sasieni P (2012) Review of cytology and histopathology as part of the NHS Cervical Screening Programme audit of invasive cervical cancers. Cytopathology 23: 13–22. doi: 10.1111/j.1365-2303.2011.00948.x 22243289

21. Kirschner B, Poll S, Rygaard C, Wahlin A, Junge J (2011) Screening history in women with cervical cancer in a Danish population-based screening program. Gynecol Oncol 120: 68–72. doi: 10.1016/j.ygyno.2010.09.021 21035171

22. Nygard M, Roysland K, Campbell S, Dillner J (2014) Comparative effectiveness study on human papillomavirus detection methods used in the cervical cancer screening programme. BMJ Open 4: e003460. doi: 10.1136/bmjopen-2013-003460 24401720

23. Sorbye SW, Suhrke P, Reva BW, Berland J, Maurseth RJ, Al-Shibli K (2017) Accuracy of cervical cytology: comparison of diagnoses of 100 Pap smears read by four pathologists at three hospitals in Norway. BMC Clin Pathol 17: 18. doi: 10.1186/s12907-017-0058-8 28860942

24. Castanon A, Leung VM, Landy R, Lim AW, Sasieni P (2013) Characteristics and screening history of women diagnosed with cervical cancer aged 20–29 years. Br J Cancer 109: 35–41. doi: 10.1038/bjc.2013.322 23820257

25. Herbert A, Anshu, Culora G, Dunsmore H, Gupta SS, Holdsworth G, et al. (2010) Invasive cervical cancer audit: why cancers developed in a high-risk population with an organised screening programme. BJOG 117: 736–745. doi: 10.1111/j.1471-0528.2010.02511.x 20184570

26. Ibanez R, Alejo M, Combalia N, Tarroch X, Autonell J, Codina L, et al. (2015) Underscreened Women Remain Overrepresented in the Pool of Cervical Cancer Cases in Spain: A Need to Rethink the Screening Interventions. Biomed Res Int 2015: 605375. doi: 10.1155/2015/605375 26180804

27. Smith JS, Lindsay L, Hoots B, Keys J, Franceschi S, Winer R, et al. (2007) Human papillomavirus type distribution in invasive cervical cancer and high-grade cervical lesions: a meta-analysis update. Int J Cancer 121: 621–632. doi: 10.1002/ijc.22527 17405118

28. Ho GY, Einstein MH, Romney SL, Kadish AS, Abadi M, Mikhail M, et al. (2011) Risk factors for persistent cervical intraepithelial neoplasia grades 1 and 2: managed by watchful waiting. J Low Genit Tract Dis 15: 268–275. doi: 10.1097/LGT.0b013e3182216fef 21811178

29. Trottier H, Mahmud SM, Lindsay L, Jenkins D, Quint W, Wieting SL, et al. (2009) Persistence of an incident human papillomavirus infection and timing of cervical lesions in previously unexposed young women. Cancer Epidemiol Biomarkers Prev 18: 854–862. doi: 10.1158/1055-9965.EPI-08-1012 19223559

30. Kjaer SK, Frederiksen K, Munk C, Iftner T (2010) Long-term absolute risk of cervical intraepithelial neoplasia grade 3 or worse following human papillomavirus infection: role of persistence. J Natl Cancer Inst 102: 1478–1488. doi: 10.1093/jnci/djq356 20841605

31. Castle PE, Schiffman M, Wheeler CM, Solomon D (2009) Evidence for frequent regression of cervical intraepithelial neoplasia-grade 2. Obstet Gynecol 113: 18–25. doi: 10.1097/AOG.0b013e31818f5008 19104355

32. Moscicki AB, Ma Y, Wibbelsman C, Darragh TM, Powers A, Farhat S, et al. (2010) Rate of and risks for regression of cervical intraepithelial neoplasia 2 in adolescents and young women. Obstet Gynecol 116: 1373–1380. doi: 10.1097/AOG.0b013e3181fe777f 21099605

33. Ostor AG (1993) Natural history of cervical intraepithelial neoplasia: a critical review. Int J Gynecol Pathol 12: 186–192. 8463044

34. Pedersen K, Lonnberg S, Skare GB, Sorbye SW, Burger EA, Kristiansen IS (2015) Kostnader ved masseundersøkelsen mot livmorhalskreft [Costs of the Norwegian Cervical Cancer Screening Program]. Sykepleien Forsk 62–71.

Quality control of cervical cytology using a 3-type HPV mRNA test increases screening program sensitivity of cervical intraepithelial neoplasia grade 2+ in young Norwegian women—A cohort study

Souhrn

Klíčová slova:

Zdroje

PLOS One

Aktuální možnosti diagnostiky a léčby litiáz