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Trends in the incidence of cervical cancer and severe precancerous lesions in Denmark, 1997–2012

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Abstract

Purpose

The incidence of cervical cancer, including squamous cell carcinoma (SCC), has been decreasing in several developed countries since the onset of organized screening programs; in some countries, however, the incidence of adenocarcinoma has increased among young women. We investigated the Danish incidence trends during 1997–2011 when cervical screening coverage was high. Incidences of cervical intraepithelial neoplasia grade 3 (CIN3) and adenocarcinoma in situ (AIS) were also assessed, with the latest part of the study period coinciding with introduction of free-of-charge human papillomavirus (HPV) vaccination.

Methods

Using nationwide registries, we estimated age-specific and age-standardized incidence rates and estimated annual percentage change (EAPC).

Results

The incidence of SCC decreased significantly, especially in women aged ≥45 years [EAPC: −3.1 % (95 % CI −4.3 to −2.5)], whereas the incidence of adenocarcinoma increased significantly, from 2.4 to 3.1/100,000 primarily due to increases in women aged ≤44 years [EAPC: 4.3 % (95 % CI 1.8–6.7)]. The incidences of CIN3 and AIS increased significantly from 94.7 to 156.5/100,000 and 3.3 to 11.3/100,000, respectively, but, importantly, they decreased significantly during 2009–2012 in women aged ≤20 years.

Conclusions

The Danish screening program has successfully reduced the incidence of cervical cancer, especially of SCC in older women; however, the program has not significantly reduced the incidence in young women or the incidence of adenocarcinoma, which is increasing. Decreases in the incidences of CIN3 and AIS in age groups with high HPV vaccine coverage may herald a future decrease in cervical cancer incidence in young Danish women.

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References

  1. Ferlay J, Soerjomataram I, Ervik M et al (2013) GLOBOCAN 2012 v1.0, Cancer incidence and mortality WORLDWIDE: IARC CancerBase No. 11 [Internet].Lyon, France: International Agency for Research on Cancer; 2013. http://globocan.iarc.fr. Accessed August 2014

  2. Seoud M, Tjalma WA, Ronsse V (2011) Cervical adenocarcinoma: moving towards better prevention. Vaccine 29:9148–9158. doi:10.1016/j.vaccine.2011.09.115

    Article  PubMed  Google Scholar 

  3. Adegoke O, Kulasingam S, Virnig B (2012) Cervical cancer trends in the United States: a 35-year population-based analysis. J Womens Health (Larchmt) 21:1031–1037. doi:10.1089/jwh.2011.3385

    Article  Google Scholar 

  4. Bray F, Loos AH, McCarron P et al (2005) Trends in cervical squamous cell carcinoma incidence in 13 European countries: changing risk and the effects of screening. Cancer Epidemiol Biomark Prev 14:677–686

    Article  Google Scholar 

  5. Kyndi M, Frederiksen K, Kruger KS (2006) Cervical cancer incidence in Denmark over six decades (1943–2002). Acta Obstet Gynecol Scand 85:106–111

    Article  PubMed  Google Scholar 

  6. Visioli CB, Zappa M, Ciatto S, Iossa A, Crocetti E (2004) Increasing trends of cervical adenocarcinoma incidence in Central Italy despite extensive screening programme, 1985–2000. Cancer Detect Prev 28:461–464

    Article  PubMed  Google Scholar 

  7. Zhu C, Bassig BA, Zhang Y et al (2014) A birth cohort analysis of the incidence of adenocarcinoma of the uterine cervix in the USA. Eur J Cancer Prev. doi:10.1097/CEJ.0000000000000062

    Google Scholar 

  8. Barnholtz-Sloan J, Patel N, Rollison D, Kortepeter K, Mackinnon J, Giuliano A (2009) Incidence trends of invasive cervical cancer in the United States by combined race and ethnicity. Cancer Causes Control 20:1129–1138. doi:10.1007/s10552-009-9317-z

    Article  PubMed  Google Scholar 

  9. de Kok IM, van der Aa MA, van Ballegooijen M et al (2011) Trends in cervical cancer in the Netherlands until 2007: has the bottom been reached? Int J Cancer 128:2174–2181. doi:10.1002/ijc.25553

    Article  PubMed  Google Scholar 

  10. Howlett RI, Marrett LD, Innes MK, Rosen BP, McLachlin CM (2007) Decreasing incidence of cervical adenocarcinoma in Ontario: this related to improved endocervical Pap test sampling? Int J Cancer 120:362–367

    Article  CAS  PubMed  Google Scholar 

  11. Sigurdsson K (1999) The Icelandic and Nordic cervical screening programs: trends in incidence and mortality rates through 1995. Acta Obstet Gynecol Scand 78:478–485

    Article  CAS  PubMed  Google Scholar 

  12. Lynge E (2002) Cervical cancer screening. Ugeskr Laeger 164:171–173

    PubMed  Google Scholar 

  13. The Danish National Board of Health (2012) Screening for livmoderhalskræft–anbefalinger 2012 https://sundhedsstyrelsen.dk/publ/Publ2012/SYB/Kraeft/ScreenLivmoderhalskrftAnbef.pdf. Accessed October 2014

  14. Stanley M (2010) Pathology and epidemiology of HPV infection in females. Gynecol Oncol 117:S5–S10. doi:10.1016/j.ygyno.2010.01.024

    Article  PubMed  Google Scholar 

  15. Schiffman M, Castle PE, Jeronimo J, Rodriguez AC, Wacholder S (2007) Human papillomavirus and cervical cancer. Lancet 370:890–907

    Article  CAS  PubMed  Google Scholar 

  16. Moscicki AB, Schiffman M, Burchell A et al (2012) Updating the natural history of human papillomavirus and anogenital cancers. Vaccine 30(Suppl 5):F24–F33. doi:10.1016/j.vaccine.2012.05.089

    Article  PubMed Central  PubMed  Google Scholar 

  17. Nøhr B, Frydshou D, Nielsen K, Fuglsang K, Hansen K, et al (2012) DSOG Kliniske Guidelines Udredning, behandling og kontrol af cervikal dysplasi (Danish Society of Obstetrics and Gynaecology). http://gynobsguideline.dk/hindsgavl/Cervixdysplasi2012.pdf. Accessed May 2014

  18. Barken SS, Rebolj M, Andersen ES, Lynge E (2012) Frequency of cervical intraepithelial neoplasia treatment in a well-screened population. Int J Cancer 130:2438–2444. doi:10.1002/ijc.26248

    Article  CAS  PubMed  Google Scholar 

  19. European Medicines Agency (2010) European public assessment report for Gardasil. http://www.emea.europa.eu/ema/index.jsp?curl=pages/medicines/human/medicines/000703/human_med_000805.jsp. Accessed May 2014

  20. Sander BB, Rebolj M, Valentiner-Branth P, Lynge E (2012) Introduction of human papillomavirus vaccination in Nordic Countries. Vaccine 30:1425–1433. doi:10.1016/j.vaccine.2011.11.097

    Article  PubMed  Google Scholar 

  21. Smith JS, Lindsay L, Hoots B 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

    Article  CAS  PubMed  Google Scholar 

  22. Castellsague X, Diaz M, de Sanjosé S et al (2006) Worldwide human papillomavirus etiology of cervical adenocarcinoma and its cofactors: implications for screening and prevention. J Natl Cancer Inst 98:303–315

    Article  PubMed  Google Scholar 

  23. Pimenta JM, Galindo C, Jenkins D, Taylor SM (2013) Estimate of the global burden of cervical adenocarcinoma and potential impact of prophylactic human papillomavirus vaccination. BMC Cancer 13:553. doi:10.1186/1471-2407-13-553

    Article  PubMed Central  PubMed  Google Scholar 

  24. Garland SM, Smith JS (2010) Human papillomavirus vaccines: current status and future prospects. Drugs 70:1079–1098. doi:10.2165/10898580-000000000-00000

    Article  PubMed  Google Scholar 

  25. Kjaer SK, Munk C, Junge J, Iftner T (2014) Carcinogenic HPV prevalence and age-specific type distribution in 40,382 women with normal cervical cytology, ASCUS/LSIL, HSIL, or cervical cancer: what is the potential for prevention? Cancer Causes Control 25:179–189. doi:10.1007/s10552-013-0320-z

    Article  PubMed  Google Scholar 

  26. Statens Serum Institut (2013) EPI-NYT: HPV-vaccination-tilslutning 2012. http://www.ssi.dk/Aktuelt/Nyhedsbreve/EPI-NYT/2013/Uge%2020%20-%202013.aspx?p=1. Accessed May 2014

  27. Statens Serums Institut (2014) Epi-nyt uge 47, Vaccinationstilslutning i det midlertidige HPV-vaccinationsprogram til kvinder født 1985–1992. http://www.ssi.dk/Aktuelt/Nyhedsbreve/EPI-NYT/2014/Uge%2047%20-%202014.aspx. Accessed November 2014

  28. Baldur-Felskov B, Dehlendorff C, Junge J, Munk C, Kjaer SK (2014) Incidence of cervical lesions in Danish women before and after implementation of a national HPV vaccination program. Cancer Causes Control 25:915–922. doi:10.1007/s10552-014-0392-4

    Article  PubMed  Google Scholar 

  29. Baldur-Felskov B, Dehlendorff C, Munk C, Kjaer SK (2014) Early impact of human papillomavirus vaccination on cervical neoplasia–nationwide follow-up of young Danish women. J Natl Cancer Inst 106: djt460. doi: 10.1093/jnci/djt460

  30. Gjerstorff ML (2011) The Danish cancer registry. Scand J Public Health 39:42–45. doi:10.1177/1403494810393562

    Article  PubMed  Google Scholar 

  31. The Danish Pathology Data Bank (2011). http://www.patobank.dk/. Accessed May 2014

  32. Statens Serum Institut (2013) Indberetning og patientregistrering: Patologi. http://www.ssi.dk/Sundhedsdataogit/Indberetning%20og%20patientregistrering/SEI/Patologi.aspx. Accessed November 2013

  33. Dugue PA, Lynge E, Bjerregaard B, Rebolj M (2012) Non-participation in screening: the case of cervical cancer in Denmark. Prev Med 54:266–269. doi:10.1016/j.ypmed.2012.01.012

    Article  PubMed  Google Scholar 

  34. Danske Regioner (2012) Økonomisk vejledning 2008, 2010, 2011 and 2012. http://www.regioner.dk/økonomi/økonomisk+vejledning/baggrundsmappe2007og2008/regionernes+bidrag+til+patobanken+i+2008. Accessed November 2013

  35. Ahmad OB, Boschi-Pinto C, Lopez AD, Murray CJ, Lozano R, Inoue M (2001) Age standardization of rates: A new WHO standard. http://www.who.int/healthinfo/paper31.pdf. Accessed May 2013

  36. R Development Core Team (2012) R: A language and environment for statistical computing. Auckland: R Foundation for Statistical Computing. Vienna, Austria. http://www.R-project.org. Accessed October 2013

  37. Vaccarella S, Franceschi S, Engholm G, Lonnberg S, Khan S, Bray F (2014) 50 years of screening in the Nordic countries: quantifying the effects on cervical cancer incidence. Br J Cancer 111:965–969. doi:10.1038/bjc.2014.362

    Article  CAS  PubMed  Google Scholar 

  38. Fujiwara K, Monk B, Devouassoux-Shisheboran M (2014) Adenocarcinoma of the uterine cervix: why is it different? Curr Oncol Rep 16:416. doi:10.1007/s11912-014-0416-y

    Article  PubMed  Google Scholar 

  39. Nygard M, Hansen BT, Dillner J et al (2014) Targeting human papillomavirus to reduce the burden of cervical, vulvar and vaginal cancer and pre-invasive neoplasia: establishing the baseline for surveillance. PLoS One 9:e88323. doi:10.1371/journal.pone.0088323

    Article  PubMed Central  PubMed  Google Scholar 

  40. Foley G, Alston R, Geraci M, Brabin L, Kitchener H, Birch J (2011) Increasing rates of cervical cancer in young women in England: an analysis of national data 1982–2006. Br J Cancer 105:177–184. doi:10.1038/bjc.2011.196

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  41. Wang SS, Sherman ME, Hildesheim A, Lacey JV Jr, Devesa S (2004) Cervical adenocarcinoma and squamous cell carcinoma incidence trends among white women and black women in the United States for 1976–2000. Cancer 100:1035–1044

    Article  PubMed  Google Scholar 

  42. Dickinson JA, Stankiewicz A, Popadiuk C, Pogany L, Onysko J, Miller AB (2012) Reduced cervical cancer incidence and mortality in Canada: national data from 1932 to 2006. BMC Public Health 12:992. doi:10.1186/1471-2458-12-992

    Article  PubMed Central  PubMed  Google Scholar 

  43. Dillner J (2000) Trends over time in the incidence of cervical neoplasia in comparison to trends over time in human papillomavirus infection. J Clin Virol 19:7–23

    Article  CAS  PubMed  Google Scholar 

  44. 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

    Article  PubMed  Google Scholar 

  45. Bray F, Carstensen B, Moller H et al (2005) Incidence trends of adenocarcinoma of the cervix in 13 European countries. Cancer Epidemiol Biomark Prev 14:2191–2199

    Article  Google Scholar 

  46. Barken SS, Rebolj M, Lynge E, Junge J, Rygaard C (2013) Outcomes in cervical screening using various cytology technologies: what’s age got to do with it? Eur J Cancer Prev 22:367–373. doi:10.1097/CEJ.0b013e328359cbe0

    Article  PubMed  Google Scholar 

  47. Rask J, Lynge E, Franzmann M et al (2014) Impact of technology on cytology outcome in cervical cancer screening of young and older women. Int J Cancer 134:2168–2179. doi:10.1002/ijc.28532

    Article  CAS  PubMed  Google Scholar 

  48. Arbyn M, Bergeron C, Klinkhamer P, Martin-Hirsch P, Siebers AG, Bulten J (2008) Liquid compared with conventional cervical cytology: a systematic review and meta-analysis. Obstet Gynecol 111:167–177. doi:10.1097/01.AOG.0000296488.85807.b3

    Article  PubMed  Google Scholar 

  49. Katki HA, Kinney WK, Fetterman B et al (2011) Cervical cancer risk for women undergoing concurrent testing for human papillomavirus and cervical cytology: a population-based study in routine clinical practice. Lancet Oncol 12:663–672. doi:10.1016/S1470-2045(11)70145-0

    Article  PubMed Central  PubMed  Google Scholar 

  50. Nielsen SL, Daugbjerg SB, Gimbel H, Settnes A (2011) Use of vaginal hysterectomy in Denmark: rates, indications and patient characteristics. Acta Obstet Gynecol Scand 90:978–984. doi:10.1111/j.1600-0412.2011.01199.x

    Article  PubMed  Google Scholar 

  51. Domingo S, Pellicer A (2009) Overview of current trends in hysterectomy. Expert Rev Obstet Gynecol 4 (6): 673–85. doi:10.1586/eog.09.51. http://www.medscape.com/viewarticle/712569. Accessed August 2014

  52. Lam JU, Lynge E, Njor SH, Rebolj M (2015) Hysterectomy and its impact on the calculated incidence of cervical cancer and screening coverage in Denmark. Acta Oncol Mar 24:1–8. doi:10.3109/0284186X.2015.1016625

    Article  Google Scholar 

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Acknowledgments

The study was supported by the Mermaid project (MERMAID II).

Conflict of interest

Birgitte Baldur-Felskov and Christian Munk received travel and speaker’s fees from Sanofi Pasteur MSD. Benny Kirchner has been on the advisory board and received travel fees from GlaxoSmithKline. Jette Junge received advisory board fees from Sanofi Pasteur MSD and consultant fees from Merck. Susanne K. Kjaer received advisory board, speaker’s fees and unrestricted research grants through her institution from Sanofi Pasteur MSD and Merck. Thor Schütt Svane Nielsen, and Christian Dehlendorff report no potential conflicts of interest.

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Correspondence to Susanne K. Kjaer.

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The sponsor of the study had no role in the study design, data collection, data analysis, data interpretation, or writing the report. The corresponding author had full access to all the data and had final responsibility for the decision to submit for publication.

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Baldur-Felskov, B., Munk, C., Nielsen, T.S.S. et al. Trends in the incidence of cervical cancer and severe precancerous lesions in Denmark, 1997–2012. Cancer Causes Control 26, 1105–1116 (2015). https://doi.org/10.1007/s10552-015-0603-7

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