Skip to main content

Advertisement

SpringerLink
Log in

Effects of fertility on breast cancer incidence trends: comparing France and US

  • Brief report
  • Published:
Cancer Causes & Control Aims and scope Submit manuscript

Abstract

Purpose

Breast cancer incidence rates are now higher in France than most other European countries as well as the United States (US). Increasing breast cancer incidence rates globally have often been attributed to declining fertility rates.

Methods

We compared temporal trends in breast cancer incidence in France and the US, and examined the extent temporal trends in national fertility rates can explain the temporal trends in breast cancer incidence. This study of temporal trends used estimates of annual percent change (APC) from cancer registry data in France and the US (1978–2016) and national fertility data (1958–2011). We estimated the APCs for all ages (overall APC) and for specific age groups (under 50, 50–64 years, and 65 years and over).

Results

The overall APC was over three times higher in France than the US (France APC = 1.63%, 95% CI 1.43–1.84; US APC = 0.51, 95% CI 0.31–0.72). The overall APCs remained positive and statistically significant after adjusting for fertility trends irrespective of assumptions on fertility lags (France APC = 1.61–0.91 for a 5-year to 20-year lag, respectively; US APC = 0.37–0.36 for a 5-year to 20-year lag, respectively). Similarly, among women under 50, the APC was over 3.5 times higher in France than the US (France APC = 1.22, 95% CI 1.07–1.37; US APC = 0.33, 95% CI 0.22–0.44), and APCs remained positive after adjusting for fertility (France APC = 1.21–1.28 for a 5-year to 20-year lag, respectively; US APC = 0.38–0.26 for a 5-year to 20-year lag, respectively).

Conclusions

Based on these trend analyses, changes in fertility rate trends do not fully explain the increase incidence in breast cancer seen in both France and the US, nor the magnitude of difference between the two countries. This was seen overall and in age-specific groups.

Graphic abstract

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Code availability

All analyses were performed using SAS statistical software version 9.4 (SAS Institute).

References

  1. Torre LA, Siegel RL, Ward EM, Jemal A (2016) Global cancer incidence and mortality rates and trends–an update. Cancer Epidemiol Biomarkers Prev 25(1):16–27

    Article  Google Scholar 

  2. OECD (2020) Non-medical determinants of health (Edition 2020). OECD Health Statistics (database). https://doi.org/10.1787/46da657a-en. Accessed 20 Oct 2020

  3. Leclère BMF, Trétarre B, Stracci F, Daubisse-Marliac L, Colonna M, GRELL Working Group (2013) Trends in incidence of breast cancer among women under 40 in seven European countries: a GRELL cooperative study. Cancer Epidemiol 37:544–549

    Article  Google Scholar 

  4. Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A (2018) Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. Cancer J Clin 68(6):394–424

    Article  Google Scholar 

  5. Defossez G LGPS, Uhry Z, Grosclaude P, Colonna M, Dantony E et al (2019) National estimates of cancer incidence and mortality in metropolitan France between 1990 and 2018. Overview. Saint-Maurice: Santé publique France 20

  6. Dimitrova N, Znaor A, Agius D et al (2017) Breast cancer in South-Eastern European countries since 2000: rising incidence and decreasing mortality at young and middle ages. Eur J Cancer 83:43–55

    Article  Google Scholar 

  7. Kehm RD, Yang W, Tehranifar P, Terry MB (2019) 40 Years of change in age-and stage-specific cancer incidence rates in US women and men. JNCI Cancer Spectr 3(3):pkz038

    Article  Google Scholar 

  8. Oeffinger KC, Fontham ET, Etzioni R et al (2015) Breast cancer screening for women at average risk: 2015 guideline update from the American cancer society. JAMA 314(15):1599–1614

    Article  CAS  Google Scholar 

  9. République Française. Arrêté du 29 septembre 2006 relatif aux programmes de dépistage des cancers. Journal Officiel du 21 Decembre 2006:32002–32047. NOR: SANP0623877A

  10. Freedman DM, Tarone RE, Doody MM et al (2002) Trends in reproductive, smoking, and other chronic disease risk factors by birth cohort and race in a large occupational study population. Ann Epidemiol 12(6):363–369

    Article  Google Scholar 

  11. Kapil U, Bhadoria AS, Sareen N, Singh P, Dwivedi SN (2014) Reproductive factors and risk of breast cancer: a review. Indian J Cancer 51(4):571–576

    Article  CAS  Google Scholar 

  12. Lima SM, Kehm RD, Swett K, Gonsalves L, Terry MB (2020) Trends in parity and breast cancer incidence in US women younger than 40 years from 1935 to 2015. JAMA Netw Open 3(3):e200929–e200929

    Article  Google Scholar 

  13. OECD (2021) Fertility rates (indicator). https://doi.org/10.1787/8272fb01-en. Accessed 20 Apr 2020

  14. Mackay J, Mensah GA (2004) The atlas of heart disease and stroke. World Health Organization

  15. Renaud S, de Lorgeril M (1992) Wine, alcohol, platelets, and the French paradox for coronary heart disease. Lancet 339(8808):1523–1526

    Article  CAS  Google Scholar 

  16. Ferlay J, Colombet M, Bray F (2018) Cancer incidence in five continents, CI5plus: IARC CancerBase No. 9 [Internet]. Lyon, France: International Agency for Research on Cancer. http://ci5.iarc.fr

  17. Loire-Atlantique, Vendée - EPIC-PL Association. Cancer Registry. Accessed Sept 2019. https://www.santepaysdelaloire.com/registre-des-cancers/

  18. Harris JR, Lippman ME, Veronesi U, Willett W (1992) Breast cancer (1). N Engl J Med 327(5):319–328

    Article  CAS  Google Scholar 

  19. Segi M (1960) Cancer mortality for selected sites in 24 countries (1950–57), Sendai, Tohoku University School of Public Health

  20. National Institute of Statistics and Economic Studies (2019) Fertility, retrospective tables. France. https://www.insee.fr/en/statistiques/2382605?sommaire=2382613. Accessed 5 Jan 2019

  21. Siu AL (2016) Screening for breast cancer: US preventive services task force recommendation statement. Ann Intern Med 164(4):279–296

    Article  Google Scholar 

  22. Junod B, Zahl P-H, Kaplan RM, Olsen J, Greenland S (2011) An investigation of the apparent breast cancer epidemic in France: screening and incidence trends in birth cohorts. BMC Cancer 11(1):401

    Article  Google Scholar 

  23. Sante Publique France (2019) Rate of participation in the national organized breast cancer screening program by age and region. https://www.santepubliquefrance.fr/maladies-et-traumatismes/cancers/cancer-du-sein/articles/taux-departicipation-au-programme-national-de-depistage-organise-du-cancer-du-sein-par-age-et-par-region. Accessed 20 May 2019

  24. 2846 Arrêté du 27 septembre 2001 fixant le modèle de la convention type mentionnée à l'article L. 1411–2 du code de la santé publique Journal officiel du 3 octobre 2001. https://www.santepubliquefrance.fr/media/files/01-maladieset-traumatismes/cancers/cancers/cdc; http://www.sante.gouv.fr/fichiers/bo/2001/01-43/a0432846.htm

  25. Lacour AMN, Arnold F, Bazin B, Bohec C, Brégeault A, Chaperon J, Dubuc M, Duru G, Exbrayat C, Fontaine D, Manuel C, Obadia Y, Piette C, San Marco JL, Schaffer P, Trugeon A, Brémond A, Charles R, Cohen M, Cordier B, Dubreuil A, Namer M, Renaud R, Allemand H et al (1997) Mass screening programs for breast cancer in France comparative evaluation. J Gynecol Obstet Biol Reprod 26(5):470–483

    CAS  Google Scholar 

  26. Quintin C, Rogel A (2019) Évaluation du programme de dépistage organisé du cancer du sein: résultats et évolution des indicateurs de performance depuis 2004 en France métropolitaine. Saint-Maurice: Santé publique France. P 48. https://www.santepubliquefrance.fr

  27. Faure S (2016) Traitements hormonaux substitutifs de la ménopause. Actual Pharm 55(552):57–61

    Google Scholar 

  28. Nichols HB, Schoemaker MJ, Cai J et al (2019) Breast cancer risk After recent childbirth: a pooled analysis of 15 prospective studies. Ann Intern Med 170(1):22–30

    Article  Google Scholar 

  29. McDonald JA, Goyal A, Terry MB (2013) Alcohol intake and breast cancer risk: weighing the overall evidence. Curr Breast Cancer Rep 5(3):208–221

    Article  Google Scholar 

  30. OECD (2020) Alcohol consumption (indicator). https://doi.org/10.1787/e6895909-en. Accessed 20 Oct 2020

  31. Mesa-Eguiagaray I, Wild SH, Rosenberg PS et al (2020) Distinct temporal trends in breast cancer incidence from 1997 to 2016 by molecular subtypes: a population-based study of Scottish cancer registry data. Br J Cancer 123(5):852–859

    Article  CAS  Google Scholar 

  32. Cortet M, Bertaut A, Molinié F et al (2018) Trends in molecular subtypes of breast cancer: description of incidence rates between 2007 and 2012 from three French registries. BMC Cancer 18(1):161

    Article  Google Scholar 

  33. Acheampong T, Kehm RD, Terry MB, Argov EL, Tehranifar P (2020) Incidence trends of breast cancer molecular subtypes by age and race/ethnicity in the US from 2010 to 2016. JAMA Netw Open 3(8):e2013226

    Article  Google Scholar 

  34. Picon-Ruiz M, Morata-Tarifa C, Valle-Goffin JJ, Friedman ER, Slingerland JM (2017) Obesity and adverse breast cancer risk and outcome: mechanistic insights and strategies for intervention. Cancer J Clin 67(5):378–397

    Article  Google Scholar 

Download references

Acknowledgments

We would like to acknowledge the Francim network of French Cancer Registries for providing French breast cancer incidence data.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Author information

Author notes

  1. Martine Bellanger and Sarah M. Lima have contributed equally to this paper and co-first authors.

Authors and Affiliations

  1. Institut de Cancerologie de l’Ouest, Nantes, France

    Martine Bellanger

  2. Ecole Des Hautes Etudes en Sante Publique, EA 7348 MOS, Research Unit, Rennes, France

    Martine Bellanger

  3. International Breast Cancer and Nutrition Network, Angers, France

    Martine Bellanger & Mary Beth Terry

  4. Department of Epidemiology, Mailman School of Public Health, Columbia University, 722 West 168th St, New York, NY, USA

    Sarah M. Lima & Mary Beth Terry

  5. Loire-Atlantique/Vendée Cancer Registry, Nantes, France

    Anne Cowppli-Bony & Florence Molinié

  6. SIRIC ILIAD INCa-DGOSInserm_12558, CHU Nantes, Nantes, France

    Anne Cowppli-Bony & Florence Molinié

  7. French Network of Cancer Registries (FRANCIM), Toulouse, France

    Anne Cowppli-Bony & Florence Molinié

  8. Herbert Irving Comprehensive Cancer Center, Columbia University Irving Medical Center, 1130 St Nicholas Ave, New York, NY, USA

    Mary Beth Terry

Authors
  1. Martine Bellanger
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sarah M. Lima
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Anne Cowppli-Bony
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Florence Molinié
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mary Beth Terry
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceptualization: MB, MBT; methodology: SML, MBT; data acquisition: SML, ACB, FM; formal analysis and investigation: SML; writing-original draft preparation: MB, SML; writing-review and editing: all authors (MB, SML, ACB, FM, MBT); supervision: MBT.

Corresponding author

Correspondence to Mary Beth Terry.

Ethics declarations

Conflict of interest

The authors have no conflicts of interest to disclose.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors. This study was exempt from ethical review and informed consent according to Code of Federal Regulations [45 CFR 46.101(b)]. This paper was done in compliance with the STROBE checklist for observational studies. https://www.equator-network.org/wp-content/uploads/2015/10/STROBE_checklist_v4_combined.pdf.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bellanger, M., Lima, S.M., Cowppli-Bony, A. et al. Effects of fertility on breast cancer incidence trends: comparing France and US. Cancer Causes Control 32, 903–910 (2021). https://doi.org/10.1007/s10552-021-01440-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10552-021-01440-2

Keywords

Search

Navigation