Skip to main content

Advertisement

SpringerLink
Log in

Saturated, mono- and polyunsaturated fatty acid intake and cancer risk: results from the French prospective cohort NutriNet-Santé

  • Original Contribution
  • Published:
European Journal of Nutrition Aims and scope Submit manuscript

Abstract

Purpose

Lipid intakes such as saturated (SFA), monounsaturated (MUFA) and polyunsaturated (PUFA) fatty acids have been widely studied regarding cardiovascular health, but their relevance to cancer is unclear. Inconsistent epidemiological results may be explained by varied mechanisms involving PUFAs and redox balance, inflammatory status and cell signalling, along with interactions with other dietary components such as antioxidants, dietary fibre and more generally fruits and vegetable intakes. Therefore, this study aimed to investigate the associations between lipid intakes and cancer risk, and their potential modulation by vitamin C, vitamin E, dietary fibre and fruit and vegetable intakes.

Methods

This prospective study included 44,039 participants aged ≥ 45 years from the NutriNet-Santé cohort (2009–2017). Dietary data were collected using repeated 24 h-dietary records. Multivariable Cox models were performed to characterize associations.

Results

SFA intake was associated with increased overall [n = 1722 cases, HRQ5vsQ1 = 1.44 (1.10–1.87), p-trend = 0.008] and breast [n = 545 cases, HRQ5vsQ1 = 1.98 (1.24–3.17), p-trend = 0.01] cancer risks. n-6 PUFA [HRQ5vsQ1 = 0.56 (0.32–0.97), p-trend = 0.01] and MUFA (HRQ5vsQ1 = 0.41 [0.18-0.0.95), p-trend = 0.009] intakes were associated with a decreased risk of digestive cancers (n = 190 cases). Associations between n-6 PUFA, eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA) intakes and digestive cancer risk were modulated by dietary fibre, vitamin C and fruit and vegetable intakes.

Conclusion

These findings suggested that SFA intake could increase overall and breast cancer risks while some unsaturated fatty acids could decrease digestive cancer risk. However, in line with mechanistic hypotheses, our results suggest that intakes of fruits and vegetables and their constituents (antioxidants, fibre) may interact with PUFAs to modulate these associations.

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

Similar content being viewed by others

Abbreviations

DHA:

Docosahexaenoic acid

DPA:

Docosapentaenoic acid

EPA:

Eicosapentaenoic acid

PUFAs:

Polyunsaturated fatty acids

MUFAs:

Monounsaturated fatty acids

SFAs:

Saturated fatty acids

HR:

Hazard ratio

CI:

Confidence interval

References

  1. WHO, IARC (2012) All Cancers: Estimated Cancer Incidence, Mortality and Prevalence Worldwide in 2012. Geneva, Switzerland

    Google Scholar 

  2. Bray F, Jemal A, Grey N et al (2012) Global cancer transitions according to the Human Development Index (2008–2030): a population-based study. Lancet Oncol 13:790–801. https://doi.org/10.1016/S1470-2045(12)70211-5

    Article  Google Scholar 

  3. World Cancer Research Fund, American Institute for Cancer Research (2007) Food, nutrition, physical activity, and the prevention of cancer: a global perspective. AICR, Washington DC

    Google Scholar 

  4. WCRF/AICR (2017) Continuous Update Project findings and reports

  5. Sieri S, Chiodini P, Agnoli C et al (2014) Dietary fat intake and development of specific breast cancer subtypes. J Natl Cancer Inst. https://doi.org/10.1093/jnci/dju068

    Article  PubMed  PubMed Central  Google Scholar 

  6. Gonzalez CA, Riboli E (2010) Diet and cancer prevention: contributions from the European Prospective Investigation into Cancer and Nutrition (EPIC) study. Eur J Cancer Oxf Engl 1990 46:2555–2562. https://doi.org/10.1016/j.ejca.2010.07.025

    Article  Google Scholar 

  7. Zheng J-S, Hu X-J, Zhao Y-M et al (2013) Intake of fish and marine n-3 polyunsaturated fatty acids and risk of breast cancer: meta-analysis of data from 21 independent prospective cohort studies. BMJ 346:f3706

    Article  PubMed  Google Scholar 

  8. Yang B, Ren X-L, Fu Y-Q et al (2014) Ratio of n-3/n-6 PUFAs and risk of breast cancer: a meta-analysis of 274135 adult females from 11 independent prospective studies. BMC Cancer 14:105. https://doi.org/10.1186/1471-2407-14-105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Kiyabu GY, Inoue M, Saito E et al (2015) Fish, n-3 polyunsaturated fatty acids and n-6 polyunsaturated fatty acids intake and breast cancer risk: the Japan Public Health Center-based prospective study. Int J Cancer 137:2915–2926. https://doi.org/10.1002/ijc.29672

    Article  CAS  PubMed  Google Scholar 

  10. Bassett JK, Hodge AM, English DR et al (2016) Plasma phospholipids fatty acids, dietary fatty acids, and breast cancer risk. Cancer Causes Control CCC 27:759–773. https://doi.org/10.1007/s10552-016-0753-2

    Article  PubMed  Google Scholar 

  11. Fu Y-Q, Zheng J-S, Yang B, Li D (2015) Effect of individual omega-3 fatty acids on the risk of prostate cancer: a systematic review and dose-response meta-analysis of prospective cohort studies. J Epidemiol 25:261–274. https://doi.org/10.2188/jea.JE20140120

    Article  PubMed  PubMed Central  Google Scholar 

  12. Vieira AR, Abar L, Chan D et al (2017) Foods and beverages and colorectal cancer risk: a systematic review and meta-analysis of cohort studies, an update of the evidence of the WCRF-AICR continuous update project. Ann Oncol Off J Eur Soc Med Oncol. https://doi.org/10.1093/annonc/mdx171

    Article  Google Scholar 

  13. Bartsch H, Nair J, Owen RW (1999) Dietary polyunsaturated fatty acids and cancers of the breast and colorectum: emerging evidence for their role as risk modifiers. Carcinogenesis 20:2209–2218

    Article  CAS  PubMed  Google Scholar 

  14. Richard D, Kefi K, Barbe U et al (2008) Polyunsaturated fatty acids as antioxidants. Pharmacol Res 57:451–455. https://doi.org/10.1016/j.phrs.2008.05.002

    Article  CAS  PubMed  Google Scholar 

  15. Marion-Letellier R, Savoye G, Ghosh S (2015) Polyunsaturated fatty acids and inflammation. IUBMB Life 67:659–667. https://doi.org/10.1002/iub.1428

    Article  CAS  PubMed  Google Scholar 

  16. Latino-Martel P, Cottet V, Druesne-Pecollo N et al (2016) Alcoholic beverages, obesity, physical activity and other nutritional factors, and cancer risk: a review of the evidence. Crit Rev Oncol Hematol 99:308–323. https://doi.org/10.1016/j.critrevonc.2016.01.002

    Article  PubMed  Google Scholar 

  17. Narayanankutty A, Kottekkat A, Mathew SE et al (2017) Vitamin E supplementation modulates the biological effects of omega-3 fatty acids in naturally aged rats. Toxicol Mech Methods 27:207–214. https://doi.org/10.1080/15376516.2016.1273431

    Article  CAS  PubMed  Google Scholar 

  18. Vulcain E, Goupy P, Caris-Veyrat C, Dangles O (2005) Inhibition of the metmyoglobin-induced peroxidation of linoleic acid by dietary antioxidants: action in the aqueous vs. lipid phase. Free Radic Res 39:547–563. https://doi.org/10.1080/10715760500073865

    Article  CAS  PubMed  Google Scholar 

  19. Bo L, Jiang S, Xie Y et al (2016) Effect of vitamin E and omega-3 fatty acids on protecting ambient PM2.5-induced inflammatory response and oxidative stress in vascular endothelial cells. PLoS One 11:e0152216. https://doi.org/10.1371/journal.pone.0152216

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Pouchieu C, Chajès V, Laporte F et al (2014) Prospective associations between plasma saturated, monounsaturated and polyunsaturated fatty acids and overall and breast cancer risk—modulation by antioxidants: a nested case-control study. PLoS One 9:e90442. https://doi.org/10.1371/journal.pone.0090442

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Männistö S, Pietinen P, Virtanen MJ et al (2003) Fatty acids and risk of prostate cancer in a nested case–control study in male smokers. Cancer Epidemiol Prev Biomark 12:1422–1428

    Google Scholar 

  22. Pierre FHF, Martin OCB, Santarelli RL et al (2013) Calcium and α-tocopherol suppress cured-meat promotion of chemically induced colon carcinogenesis in rats and reduce associated biomarkers in human volunteers. Am J Clin Nutr 98:1255–1262. https://doi.org/10.3945/ajcn.113.061069

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Chang WC, Chapkin RS, Lupton JR (1997) Predictive value of proliferation, differentiation and apoptosis as intermediate markers for colon tumorigenesis. Carcinogenesis 18:721–730

    Article  CAS  PubMed  Google Scholar 

  24. Navarro SL, Neuhouser ML, Cheng T-YD et al (2016) The interaction between dietary fiber and fat and risk of colorectal cancer in the women’s health initiative. Nutrients. https://doi.org/10.3390/nu8120779

    Article  PubMed  PubMed Central  Google Scholar 

  25. Kraja B, Muka T, Ruiter R et al (2015) Dietary fiber intake modifies the positive association between n-3 PUFA intake and colorectal cancer risk in a caucasian population. J Nutr 145:1709–1716. https://doi.org/10.3945/jn.114.208462

    Article  CAS  PubMed  Google Scholar 

  26. de Sousa Moraes LF, Sun X, Peluzio M, do CG, Zhu M-J (2017) Anthocyanins/anthocyanidins and colorectal cancer: what is behind the scenes?. Crit Rev Food Sci Nutr 1–13. https://doi.org/10.1080/10408398.2017.1357533

  27. Chen H-M, Yu Y-N, Wang J-L et al (2013) Decreased dietary fiber intake and structural alteration of gut microbiota in patients with advanced colorectal adenoma. Am J Clin Nutr 97:1044–1052. https://doi.org/10.3945/ajcn.112.046607

    Article  CAS  PubMed  Google Scholar 

  28. Hercberg S, Castetbon K, Czernichow S et al (2010) The Nutrinet-Santé Study: a web-based prospective study on the relationship between nutrition and health and determinants of dietary patterns and nutritional status. BMC Public Health 10:242. https://doi.org/10.1186/1471-2458-10-242

    Article  PubMed  PubMed Central  Google Scholar 

  29. Vergnaud A-C, Touvier M, Méjean C et al (2011) Agreement between web-based and paper versions of a socio-demographic questionnaire in the NutriNet-Santé study. Int J Public Health 56:407–417. https://doi.org/10.1007/s00038-011-0257-5

    Article  PubMed  Google Scholar 

  30. Lassale C, Péneau S, Touvier M et al (2013) Validity of web-based self-reported weight and height: results of the Nutrinet-Santé study. J Med Internet Res 15:e152. https://doi.org/10.2196/jmir.2575

    Article  PubMed  PubMed Central  Google Scholar 

  31. Touvier M, Méjean C, Kesse-Guyot E et al (2010) Comparison between web-based and paper versions of a self-administered anthropometric questionnaire. Eur J Epidemiol 25:287–296. https://doi.org/10.1007/s10654-010-9433-9

    Article  PubMed  Google Scholar 

  32. The IPAQ Group (2005) Guidelines for data processing and analysis of the International Physical Activity Questionnaire. http://www.ipaq.ki.se

  33. Touvier M, Kesse-Guyot E, Méjean C et al (2011) Comparison between an interactive web-based self-administered 24 h dietary record and an interview by a dietitian for large-scale epidemiological studies. Br J Nutr 105:1055–1064. https://doi.org/10.1017/S0007114510004617

    Article  CAS  PubMed  Google Scholar 

  34. Lassale C, Castetbon K, Laporte F et al (2015) Validation of a Web-based, self-administered, non-consecutive-day dietary record tool against urinary biomarkers. Br J Nutr 113:953–962. https://doi.org/10.1017/S0007114515000057

    Article  CAS  PubMed  Google Scholar 

  35. Lassale C, Castetbon K, Laporte F et al (2016) Correlations between fruit, vegetables, fish, vitamins, and fatty acids estimated by web-based nonconsecutive dietary records and respective biomarkers of nutritional status. J Acad Nutr Diet 116:427–438.e5. https://doi.org/10.1016/j.jand.2015.09.017

    Article  PubMed  Google Scholar 

  36. Le Moullec N, Deheeger M, Preziosi P et al (1996) Validation du manuel photo utilisé pour l’enquête alimentaire de l’étude SU.VI.MAX (Validation of the food portion size booklet used in the SU.VI.MAX study). Cah Nutr Diététique 31:158–164

    Google Scholar 

  37. Arnault N, Caillot L, Castetbon K et al (2013) Table De composition des aliments, étude NutriNet-Santé. [Food composition table, NutriNet-Santé study]. Les éditions INSERM/Economica, Paris (in French)

    Google Scholar 

  38. Black AE (2000) Critical evaluation of energy intake using the Goldberg cut-off for energy intake:basal metabolic rate. A practical guide to its calculation, use and limitations. Int J Obes Relat Metab Disord J Int Assoc Study Obes 24:1119–1130

    Article  CAS  Google Scholar 

  39. Pouchieu C, Andreeva VA, Péneau S et al (2013) Sociodemographic, lifestyle and dietary correlates of dietary supplement use in a large sample of French adults: results from the NutriNet-Santé cohort study. Br J Nutr 110:1480–1491. https://doi.org/10.1017/S0007114513000615

    Article  CAS  PubMed  Google Scholar 

  40. INCa (2016) Les cancers en France. [Cancers in France]. http://www.e-cancer.fr/ressources/cancers_en_france/ (in French)

  41. Magaki M, Ishii H, Yamasaki A et al (2017) A high-fat diet increases the incidence of mammary cancer inc-Ha-ras proto-oncogene transgenic rats. J Toxicol Pathol 30:145–152. https://doi.org/10.1293/tox.2016-0052

    Article  CAS  PubMed  Google Scholar 

  42. Han J, Jiang Y, Liu X et al (2015) Dietary fat intake and risk of gastric cancer: a meta-analysis of observational studies. PLoS One 10:e0138580. https://doi.org/10.1371/journal.pone.0138580

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Yao X, Tian Z (2015) Saturated, monounsaturated and polyunsaturated fatty acids intake and risk of pancreatic cancer: evidence from observational studies. PLoS One 10:e0130870. https://doi.org/10.1371/journal.pone.0130870

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Koh W-P, Dan YY, Goh GB-B et al (2016) Dietary fatty acids and risk of hepatocellular carcinoma in the Singapore Chinese health study. Liver Int Off J Int Assoc Study Liver 36:893–901. https://doi.org/10.1111/liv.12978

    Article  CAS  Google Scholar 

  45. Duarte-Salles T, Fedirko V, Stepien M et al (2015) Dietary fat, fat subtypes and hepatocellular carcinoma in a large European cohort. Int J Cancer 137:2715–2728. https://doi.org/10.1002/ijc.29643

    Article  CAS  PubMed  Google Scholar 

  46. Hodge AM, Williamson EJ, Bassett JK et al (2015) Dietary and biomarker estimates of fatty acids and risk of colorectal cancer. Int J Cancer 137:1224–1234. https://doi.org/10.1002/ijc.29479

    Article  CAS  PubMed  Google Scholar 

  47. Bamia C, Lagiou P, Buckland G et al (2013) Mediterranean diet and colorectal cancer risk: results from a European cohort. Eur J Epidemiol 28:317–328. https://doi.org/10.1007/s10654-013-9795-x

    Article  CAS  PubMed  Google Scholar 

  48. Arem H, Mayne ST, Sampson J et al (2013) Dietary fat intake and risk of pancreatic cancer in the prostate, lung, colorectal and ovarian cancer screening trial. Ann Epidemiol 23:571–575. https://doi.org/10.1016/j.annepidem.2013.06.006

    Article  PubMed  PubMed Central  Google Scholar 

  49. Lu X, He G, Yu H et al (2010) Colorectal cancer cell growth inhibition by linoleic acid is related to fatty acid composition changes. J Zhejiang Univ Sci B 11:923–930. https://doi.org/10.1631/jzus.B1000125

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Zhang C, Yu H, Ni X et al (2015) Growth inhibitory effect of polyunsaturated fatty acids (PUFAs) on colon cancer cells via their growth inhibitory metabolites and fatty acid composition changes. PLoS One 10:e0123256. https://doi.org/10.1371/journal.pone.0123256

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Thiébaut ACM, Chajès V, Gerber M et al (2009) Dietary intakes of omega-6 and omega-3 polyunsaturated fatty acids and the risk of breast cancer. Int J Cancer 124:924–931. https://doi.org/10.1002/ijc.23980

    Article  CAS  PubMed  Google Scholar 

  52. Shen W, Gaskins HR, McIntosh MK (2014) Influence of dietary fat on intestinal microbes, inflammation, barrier function and metabolic outcomes. J Nutr Biochem 25:270–280. https://doi.org/10.1016/j.jnutbio.2013.09.009

    Article  CAS  Google Scholar 

  53. Andreeva VA, Salanave B, Castetbon K et al (2015) Comparison of the sociodemographic characteristics of the large NutriNet-Santé e-cohort with French census data: the issue of volunteer bias revisited. J Epidemiol Community Health 69:893–898. https://doi.org/10.1136/jech-2014-205263

    Article  PubMed  Google Scholar 

  54. ANSES, Comité d’Experts Spécialisé Nutrition Humaine, Groupe de travail ANC acides gras (2011) Actualisation des apports nutritionnels conseillés pour les acides gras, rapport d’expertise collective. [Update of recommended dietary fatty acid intakes, collective expert report]. Anses editions (in French)

Download references

Acknowledgements

The authors thank all the volunteers of the NutriNet-Santé cohort. We also thank Frédéric Coffinieres, Thi Hong Van Duong, Younes Esseddik (IT manager), Paul Flanzy, Régis Gatibelza, Jagatjit Mohinder and Maithyly Sivapalan (computer scientists); and Julien Allegre, Nathalie Arnault, Laurent Bourhis, Véronique Gourlet, PhD and Fabien Szabo de Edelenyi, PhD (manager) (data-manager/biostatisticians) for their technical contribution to the NutriNet-Santé study and Nathalie Druesne-Pecollo, PhD (operational coordination).

Funding

The NutriNet-Santé study was supported by the following public institutions: Ministère de la Santé, Institut de Veille Sanitaire (InVS), Institut National de la Prévention et de l’Education pour la Santé (INPES), Région Ile-de-France (CORDDIM), Institut National de la Santé et de la Recherche Médicale (INSERM), Institut National de la Recherche Agronomique (INRA), Conservatoire National des Arts et Métiers (CNAM) and Université Paris 13. Mélanie Deschasaux and Philippine Fassier were funded by a PhD Grant from the Cancéropôle Ile de France/Région Ile de France (public funding). Bernard Srour was funded by the French National Cancer Institute (grant number INCa_8085).

Author information

Authors and Affiliations

  1. Sorbonne Paris Cité Epidemiology and Statistics Research Center (CRESS), U1153 Inserm, U1125, Inra, Cnam, Paris 13 University, Nutritional Epidemiology Research Team (EREN), Bobigny, France

    Laury Sellem, Bernard Srour, Emmanuelle Kesse-Guyot, Thibault Fiolet, Céline Lavalette, Manon Egnell, Paule Latino-Martel, Philippine Fassier, Serge Hercberg, Pilar Galan, Mélanie Deschasaux & Mathilde Touvier

  2. INRA UMR1331, TOXALIM (Research Center in Food Toxicology), Université de Toulouse, ENVT, INP, Toulouse, France

    Françoise Guéraud & Fabrice Pierre

Authors
  1. Laury Sellem
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bernard Srour
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Françoise Guéraud
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Fabrice Pierre
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Emmanuelle Kesse-Guyot
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Thibault Fiolet
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Céline Lavalette
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Manon Egnell
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Paule Latino-Martel
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Philippine Fassier
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Serge Hercberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Pilar Galan
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Mélanie Deschasaux
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Mathilde Touvier
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

LS and MT: designed the research; SH, PG, EKG, MT: conducted the research; LS: performed statistical analysis; MT: supervised statistical analysis; LS and MT: wrote the paper; LS, BS, FG, FP, EKG, TF, CL, ME, PLM, PF, SH, PG, MD, and MT: contributed to the data interpretation and revised each draft for important intellectual content. All authors read and approved the final manuscript. MT had primary responsibility for the final content. None of the authors reported a conflict of interest related to the study. The funders had no role in the design, implementation, analysis, or interpretation of the data. This research was performed in the framework of the French network for Nutrition And Cancer Research (NACRe network).

Corresponding author

Correspondence to Bernard Srour.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PPTX 71 KB)

Supplementary material 2 (DOCX 14 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sellem, L., Srour, B., Guéraud, F. et al. Saturated, mono- and polyunsaturated fatty acid intake and cancer risk: results from the French prospective cohort NutriNet-Santé. Eur J Nutr 58, 1515–1527 (2019). https://doi.org/10.1007/s00394-018-1682-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00394-018-1682-5

Keywords

Search

Navigation