Abstract
The objective of this work was to detail the incidence and mortality trends of invasive and in situ breast cancer (BC) in France, especially regarding the development of screening, over the 1990–2008 period. Data issued from nine population-based cancer registries were studied. The incidence of invasive BC increased annually by 0.8 % from 1990 to 1996 and more markedly by 3.2 % from 1996 to 2003, and then sharply decreased until 2006 (−2.3 % per year), especially among women aged 50–69 years (−4.9 % per year). This trend was similar whatever the introduction date of the organized screening (OS) program in the different areas. The incidence of ductal carcinoma in situ steadily increased between 1990 and 2005, particularly among women aged 50–69 years and 70 and older. At the same time, the mortality from BC decreased annually by 1.1 % over the entire study period. This decrease was more pronounced in women aged 40–49 and 50–69 and, during the 1990–1999 period, in the areas where OS began in 1989–1991. The similarity in the incidence trends for all periods of implementation of OS in the different areas was striking. This suggests that OS alone does not explain the changes observed in incidence rate. Our study highlights the importance of closely monitoring the changes in incidence and mortality indicators, and of better understanding the factors causing variation.
Similar content being viewed by others
References
Forouzanfar MH, Foreman KJ, Delossantos AM et al (2011) Breast and cervical cancer in 187 countries between 1980 and 2010: a systematic analysis. Lancet 378:1461–1484. doi:10.1016/S0140-6736(11)61351-2
Glass AG, Lacey JV Jr, Carreon JD, Hoover RN (2007) Breast cancer incidence, 1980–2006: combined roles of menopausal hormone therapy, screening mammography, and estrogen receptor status. J Natl Cancer Inst 99:1152–1161. doi:10.1093/jnci/djm059
Weedon-Fekjær H, Bakken K, Vatten LJ, Tretli S (2012) Understanding recent trends in incidence of invasive breast cancer in Norway: age-period-cohort analysis based on registry data on mammography screening and hormone treatment use. BMJ 344:e299
Key TJ, Verkasalo PK, Banks E (2001) Epidemiology of breast cancer. Lancet Oncol 2:133–140. doi:10.1016/S1470-2045(00)00254-0
Bulletin Officiel No. 2001-43. http://www.sante.gouv.fr/fichiers/bo/2001/01-43/a0432846.htm. Accessed Nov 25 2013
Duport N (2012) Characteristics of women using organized or opportunistic breast cancer screening in France. Analysis of the 2006 French Health, Health Care and Insurance Survey. Rev Epidémiol Sante Publique 60:421–430. doi:10.1016/j.respe.2012.05.006
European Network of Cancer Registries, Tyczyński JE, Démaret E, et al (2003) Standards and guidelines for cancer registration in Europe: the ENCR recommendations: volume I. International Agency for Research on Cancer, Lyon
R Development Core Team (2010) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Belot A, Grosclaude P, Bossard N et al (2008) Cancer incidence and mortality in France over the period 1980–2005. Rev Epidémiologie Santé Publique 56:159–175. doi:10.1016/j.respe.2008.03.117
Lacour A, Mamelle N, Arnold F et al (1997) Mass screening programs for breast cancer in France. Comparative evaluation. J Gynécologie Obstétrique Biol Reprod 26:470–483
Puliti D, Duffy SW, Miccinesi G et al (2012) Overdiagnosis in mammographic screening for breast cancer in Europe: a literature review. J Med Screen 19(Suppl 1):42–56. doi:10.1258/jms.2012.012082
Marmot MG (2013) Sorting through the arguments on breast screening. JAMA 309:2553–2554. doi:10.1001/jama.2013.6822
Wu D, Pérez A (2011) A limited review of over diagnosis methods and long term effects in breast cancer screening. Oncol Rev 5:143–147. doi:10.1007/s12156-011-0077-0
De Gelder R, Heijnsdijk EAM, van Ravesteyn NT et al (2011) Interpreting overdiagnosis estimates in population-based mammography screening. Epidemiol Rev 33:111–121. doi:10.1093/epirev/mxr009
Daubisse-Marliac L, Delafosse P, Boitard JB et al (2011) Breast cancer incidence and time trend in France from 1990 to 2007: a population-based study from two French cancer registries. Ann Oncol 22:329–334. doi:10.1093/annonc/mdq396
Ravdin PM, Cronin KA, Howlader N et al (2007) The decrease in breast-cancer incidence in 2003 in the United States. N Engl J Med 356:1670–1674. doi:10.1056/NEJMsr070105
Zbuk K, Anand SS (2012) Declining incidence of breast cancer after decreased use of hormone-replacement therapy: magnitude and time lags in different countries. J Epidemiol Community Health 66:1–7. doi:10.1136/jech.2008.083774
Gompel A, Plu-Bureau G (2010) Is the decrease in breast cancer incidence related to a decrease in postmenopausal hormone therapy? Ann N Y Acad Sci 1205:268–276. doi:10.1111/j.1749-6632.2010.05664.x
Jemal A, Ward E, Thun MJ (2007) Recent trends in breast cancer incidence rates by age and tumor characteristics among U.S. women. Breast Cancer Res 9:R28. doi:10.1186/bcr1672
Séradour B, Allemand H, Weill A, Ricordeau P (2009) Changes by age in breast cancer incidence, mammography screening and hormone therapy use in France from 2000 to 2006. Bull Cancer 96:E1–E6. doi:10.1684/bdc.2009.0869
Dietel M, Lewis MA, Shapiro S (2005) Hormone replacement therapy: pathobiological aspects of hormone-sensitive cancers in women relevant to epidemiological studies on HRT: a mini-review. Hum Reprod (Oxford, England) 20:2052–2060. doi:10.1093/humrep/dei043
Hill C, Laplanche A (2010) La consommation d’alcool est trop élevée en France. Presse Médicale 39:e158–e164. doi:10.1016/j.lpm.2009.12.010
Leclère B, Molinié F, Trétarre B et al (2013) Trends in incidence of breast cancer among women under 40 in seven European countries: a GRELL cooperative study. Cancer Epidemiol 37:544–549. doi:10.1016/j.canep.2013.05.001
Sørum R, Hofvind S, Skaane P, Haldorsen T (2010) Trends in incidence of ductal carcinoma in situ: the effect of a population-based screening programme. Breast (Edinburgh, Scotland) 19:499–505. doi:10.1016/j.breast.2010.05.014
Virnig BA, Wang S-Y, Shamilyan T et al (2010) Ductal carcinoma in situ: risk factors and impact of screening. JNCI Monogr 2010:113–116. doi:10.1093/jncimonographs/lgq024
Toriola AT, Colditz GA (2013) Trends in breast cancer incidence and mortality in the United States: implications for prevention. Breast Cancer Res Treat 138:665–673. doi:10.1007/s10549-013-2500-7
Kumar AS, Bhatia V, Henderson IC (2005) Overdiagnosis and overtreatment of breast cancer: rates of ductal carcinoma in situ: a US perspective. Breast Cancer Res 7:271–275. doi:10.1186/bcr1346
Autier P, Boniol M, La Vecchia C et al (2010) Disparities in breast cancer mortality trends between 30 European countries: retrospective trend analysis of WHO mortality database. BMJ 341:c3620. doi:10.1136/bmj.c3620
Broeders M, Moss S, Nyström L et al (2012) The impact of mammographic screening on breast cancer mortality in Europe: a review of observational studies. J Med Screen 19(Suppl 1):14–25. doi:10.1258/jms.2012.012078
Independent UK Panel (2012) The benefits and harms of breast cancer screening: an independent review. Lancet 380:1778–1786. doi:10.1016/S0140-6736(12)61611-0
Gøtzsche PC, Nielsen M (2011) Screening for breast cancer with mammography. Cochrane Database Syst Rev (1):CD001877. doi:10.1002/14651858.CD001877.pub4
Kalager M, Zelen M, Langmark F, Adami H-O (2010) Effect of screening mammography on breast-cancer mortality in Norway. N Engl J Med 363:1203–1210. doi:10.1056/NEJMoa1000727
Blanks RG, Moss SM, McGahan CE et al (2000) Effect of NHS breast screening programme on mortality from breast cancer in England and Wales, 1990–8: comparison of observed with predicted mortality. BMJ 321:665–669
Olsen AH, Njor SH, Lynge E (2007) Estimating the benefits of mammography screening: the impact of study design. Epidemiology (Cambridge, Mass.) 18:487–492. doi:10.1097/EDE.0b013e318060cbbd
Moss SM, Nyström L, Jonsson H et al (2012) The impact of mammographic screening on breast cancer mortality in Europe: a review of trend studies. J Med Screen 19(Suppl 1):26–32. doi:10.1258/jms.2012.012079
Hanley JA (2011) Measuring mortality reductions in cancer screening trials. Epidemiol Rev 33:36–45. doi:10.1093/epirev/mxq021
Berry DA, Cronin KA, Plevritis SK et al (2005) Effect of screening and adjuvant therapy on mortality from breast cancer. N Engl J Med 353:1784–1792. doi:10.1056/NEJMoa050518
Vilaprinyo E, Puig T, Rue M (2012) Contribution of early detection and adjuvant treatments to breast cancer mortality reduction in Catalonia, Spain. PLoS One 7:e30157. doi:10.1371/journal.pone.0030157
Lee S, Zelen M (2006) A stochastic model for predicting the mortality of breast cancer. J Natl Cancer Inst Monogr (36):79–86. doi:10.1093/jncimonographs/lgj011
Mandelblatt J, Schechter CB, Lawrence W, et al (2006) The SPECTRUM population model of the impact of screening and treatment on U.S. breast cancer trends from 1975 to 2000: principles and practice of the model methods. J Natl Cancer Inst Monogr (36):47–55. doi:10.1093/jncimonographs/lgj008
Youlden DR, Cramb SM, Dunn NAM et al (2012) The descriptive epidemiology of female breast cancer: an international comparison of screening, incidence, survival and mortality. Cancer Epidemiol 36:237–248. doi:10.1016/j.canep.2012.02.007
Uhry Z, Hédelin G, Colonna M et al (2011) Modelling the effect of breast cancer screening on related mortality using French data. Cancer Epidemiol 35:235–242. doi:10.1016/j.canep.2010.10.009
Sprague BL, Trentham-Dietz A, Remington PL (2011) The contribution of postmenopausal hormone use cessation to the declining incidence of breast cancer. Cancer Causes Control CCC 22:125–134. doi:10.1007/s10552-010-9682-7
Ringa V, Fournier A (2008) Did the decrease in use of menopausal hormone therapy induce a decrease in the incidence of breast cancer in France (and elsewhere)? Rev Epidémiologie Santé Publique 56:297–301. doi:10.1016/j.respe.2008.07.085
Acknowledgments
Grant sponsor: National Cancer Institute (INCa), French Institute for Public Health Surveillance (InVS). We are grateful for the generous assistance given by the pathologists, oncologists, Departments of Medical Data Processing of public and private hospitals, and medical practitioners, regarding access to medical records.
Conflict of interest
None.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Molinié, F., Vanier, A., Woronoff, A.S. et al. Trends in breast cancer incidence and mortality in France 1990–2008. Breast Cancer Res Treat 147, 167–175 (2014). https://doi.org/10.1007/s10549-014-3073-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10549-014-3073-9