Effect of Fee on Cervical Cancer Screening Attendance--ScreenFee, a Swedish Population-Based Randomised Trial

Emilia Alfonzo, Agneta Andersson Ellström, Szilard Nemes, Björn Strander, Emilia Alfonzo, Agneta Andersson Ellström, Szilard Nemes, Björn Strander

Abstract

Background: Attendance in the cervical cancer screening programme is one of the most important factors to lower the risk of contracting the disease. Attendance rates are often low in areas with low socioeconomic status. Charging a fee for screening might possibly decrease attendance in this population. Screening programme coverage is low in low socio-economic status areas in Gothenburg, Sweden, but has increased slightly after multiple interventions in recent years. For many years, women in the region have paid a fee for screening. We studied the effect of abolishing this fee in a trial emanating from the regular cervical cancer screening programme.

Method: Individually randomised controlled trial. All 3 124 women in three low-resource areas in Gothenburg, due for screening during the study period, were randomised to receive an offer of a free test or the standard invitation stating the regular fee of 100 SEK (≈11 €). The study was conducted during the first six months of 2013. Attendance was defined as a registered Pap smear within 90 days from the date the invitation was sent out.

Results: Attendance did not differ significantly between women who were charged and those offered free screening (RR 0.93; CI 0.85-1.02). No differences were found within the districts or as an effect of age, attendance after the most recent previous invitation or previous experience of smear taking.

Conclusion: Abolishment of a modest screening fee in socially disadvantaged urban districts with low coverage, after previous multiple systematic interventions, does not increase attendance in the short term. Other interventions might be more important for increasing attendance in low socio-economic status areas.

Trial registration: ClinicalTrials.gov NCT02378324.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Fig 1. Flow chart of the study.
Fig 1. Flow chart of the study.
There were no exclusions and no protocol violations.
Fig 2. Attendance 2011–2013 in the districts…
Fig 2. Attendance 2011–2013 in the districts included in the study.
Attendance rate is calculated as smears taken within 90 days after sending invitation. Yearly re-invitations to non-participants are not included in the denominators.
Fig 3. Comparison of age between the…
Fig 3. Comparison of age between the intervention and control arm.
The central middle line is the median age. The boxes contain 50% of the data, the arms 25 and 25% of the remaining data. No outliers were found.
Fig 4. Attendance between the intervention and…
Fig 4. Attendance between the intervention and control group within the districts with 95% confidence intervals.

References

    1. World Health Organization. World Cancer Report 2008 (Internet) Lyon: International Agency for research on Cancer 2008 [updated December 27th 2014]. Available:
    1. Broberg G, Jonasson JM, Ellis J, Gyrd-Hansen D, Anjemark B, Glantz A, et al. Increasing participation in cervical cancer screening: telephone contact with long-term non-attendees in Sweden. Results from RACOMIP, a randomized controlled trial. International journal of cancer Journal international du cancer. 2013;133(1):164–71. Epub 2012/12/13. 10.1002/ijc.27985 .
    1. NORDCAN. Mortality in Cervical cancer in Sweden 1970–2013 [September 2015]. Available: .
    1. Andrae B, Kemetli L, Sparen P, Silfverdal L, Strander B, Ryd W, et al. Screening-preventable cervical cancer risks: evidence from a nationwide audit in Sweden. J Natl Cancer Inst. 2008;100(9):622–9. Epub 2008/05/01. doi: djn099 [pii] 10.1093/jnci/djn099 .
    1. Segnan N, Senore C, Giordano L, Ponti A, Ronco G. Promoting participation in a population screening program for breast and cervical cancer: a randomized trial of different invitation strategies. Tumori. 1998;84(3):348–53. .
    1. Eaker S, Adami HO, Granath F, Wilander E, Sparen P. A large population-based randomized controlled trial to increase attendance at screening for cervical cancer. Cancer Epidemiol Biomarkers Prev. 2004;13(3):346–54. .
    1. Broberg G, Gyrd-Hansen D, Miao Jonasson J, Ryd ML, Holtenman M, Milsom I, et al. Increasing participation in cervical cancer screening: offering a HPV self-test to long-term non-attendees as part of RACOMIP, a Swedish randomized controlled trial. International journal of cancer Journal international du cancer. 2014;134(9):2223–30. Epub 2013/10/16.\ 10.1002/ijc.28545 .
    1. 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. British journal of cancer. 2011;105(3):337–9. Epub 2011/07/07. 10.1038/bjc.2011.236 ; PubMed Central PMCID: PMCPmc3172898.
    1. Virtanen A, Nieminen P, Luostarinen T, Anttila A. Self-sample HPV tests as an intervention for nonattendees of cervical cancer screening in Finland: a randomized trial. Cancer epidemiology, biomarkers & prevention: a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology. 2011;20(9):1960–9. Epub 2011/07/15. 10.1158/1055-9965.epi-11-0307 .
    1. Idestrom M, Milsom I, Andersson-Ellstrom A. Knowledge and attitudes about the Pap-smear screening program: a population-based study of women aged 20–59 years. Acta obstetricia et gynecologica Scandinavica. 2002;81(10):962–7. Epub 2002/10/09. .
    1. Eaker S, Adami HO, Sparen P. Reasons women do not attend screening for cervical cancer: a population-based study in Sweden. Prev Med. 2001;32(6):482–91. .
    1. Fylan F. Screening for cervical cancer: a review of women's attitudes, knowledge, and behaviour. The British journal of general practice: the journal of the Royal College of General Practitioners. 1998;48(433):1509–14. Epub 1999/02/20. ; PubMed Central PMCID: PMCPmc1313202.
    1. Everett T, Bryant A, Griffin MF, Martin-Hirsch PP, Forbes CA, Jepson RG. Interventions targeted at women to encourage the uptake of cervical screening. The Cochrane database of systematic reviews. 2011;(5):Cd002834 Epub 2011/05/13. 10.1002/14651858.CD002834.pub2 ; PubMed Central PMCID: PMCPmc4163962.
    1. Anhang Price R, Zapka J, Edwards H, Taplin SH. Organizational factors and the cancer screening process. Journal of the National Cancer Institute Monographs. 2010;2010(40):38–57. Epub 2010/04/14. 10.1093/jncimonographs/lgq008 ; PubMed Central PMCID: PMCPmc3731433.
    1. Patnick J. Cervical cancer screening in England. European journal of cancer. 2000;36(17):2205–8. Epub 2000/11/10. .
    1. Stone EG, Morton SC, Hulscher ME, Maglione MA, Roth EA, Grimshaw JM, et al. Interventions that increase use of adult immunization and cancer screening services: a meta-analysis. Annals of internal medicine. 2002;136(9):641–51. Epub 2002/05/07. .
    1. Kuroki H. Survey on the trends in uterine cervical cancer screening in Japanese women: the efficacy of free coupons in the screening. The journal of obstetrics and gynaecology research. 2012;38(1):35–9. Epub 2011/10/15. 10.1111/j.1447-0756.2011.01672.x .
    1. Tornberg S, Lidbrink E, Henriksson R. Free of charge mammography gets more people to the examination. Study in Stockholm County shows good efficacy in socioeconomically disadvantaged areas. Lakartidningen. 2014;111(7):278–81. Epub 2014/03/29. .
    1. Nationellt kvalitetsregister för cervixcancerprevention. Förebyggande av livmoderhalscancer I Sverige. Årsrapport 2013 (Prevention av cervical cancer in Sweden. Annual report 2013) [September 2015]. Available:
    1. Göteborgs stad, stadsledningskontoret, Samhällsanalys och statistik. Statistik "Göteborgsbladet" 2014 (Statistics Gothenburg CIty) [September 2015]. Available: .
    1. Västra Götalandsregionen. Slutrapport Ta med en vän-ett projekt för att öka cellprovtagningen i nordöstra Göteborg (Final report Bring a friend- a project to increase taken pap smears in North-eastern Gothenburg) 2012 [September 2015]. Available:
    1. Regionalt Cancer Centrum Väst. Sammanställning av några kvalitetsdata från 2014 gällande cervixcancerprevention i Västra Sverige (Compilation of data regarding prevention of Cervical cancer in West Sweden) [September 2015]. Available:
    1. R Core Team. A Language and Environment for Statistical Computing. R Foundation for Statistical Computing Vienna, Austria [September 2015]. Available: .
    1. Azerkan F, Zendehdel K, Tillgren P, Faxelid E, Sparen P. Risk of cervical cancer among immigrants by age at immigration and follow-up time in Sweden, from 1968 to 2004. International journal of cancer Journal international du cancer. 2008;123(11):2664–70. Epub 2008/09/05. 10.1002/ijc.23843 .
    1. Raghubir P. Free gift with purchase- Promoting or Discounting the brand?. Journal of consumer economy 2004;14 (1&2) 181–6.
    1. Bonfill X, Marzo M, Pladevall M, Marti J, Emparanza JI. Strategies for increasing women participation in community breast cancer screening. The Cochrane database of systematic reviews. 2001;(1):Cd002943 Epub 2001/05/02. 10.1002/14651858.cd002943 .
    1. Immonen-Raiha P, Kauhava L, Parvinen I, Helenius H, Klemi P. Customer fee and participation in breast-cancer screening. Lancet. 2001;358(9291):1425 Epub 2001/11/14. 10.1016/s0140-6736(01)06520-5 .
    1. Stoner TJ, Dowd B, Carr WP, Maldonado G, Church TR, Mandel J. Do vouchers improve breast cancer screening rates? Results from a randomized trial. Health Serv Res. 1998;33(1):11–28. Epub 1998/05/05. ; PubMed Central PMCID: PMCPmc1070244.

Source: PubMed

3
S'abonner