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Cancer Epidemiology, Biomarkers & Prevention
Cancer Epidemiology, Biomarkers & Prevention
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Research Articles

Dietary and Circulating Fatty Acids and Ovarian Cancer Risk in the European Prospective Investigation into Cancer and Nutrition

Sahar Yammine, Inge Huybrechts, Carine Biessy, Laure Dossus, Elom K. Aglago, Sabine Naudin, Pietro Ferrari, Elisabete Weiderpass, Anne Tjønneland, Louise Hansen, Kim Overvad, Francesca R. Mancini, Marie-Christine Boutron-Ruault, Marina Kvaskoff, Renée T. Fortner, Rudolf Kaaks, Matthias B. Schulze, Heiner Boeing, Antonia Trichopoulou, Anna Karakatsani, Carlo La Vecchia, Vassiliki Benetou, Giovanna Masala, Vittorio Krogh, Amalia Mattiello, Alessandra Macciotta, Inger T. Gram, Guri Skeie, Jose R. Quirós, Antonio Agudo, Maria-José Sánchez, Maria-Dolores Chirlaque, Eva Ardanaz, Leire Gil, Hanna Sartor, Isabel Drake, Annika Idahl, Eva Lundin, Dagfinn Aune, Heather Ward, Melissa A. Merritt, Naomi E. Allen, Marc J. Gunter and Véronique Chajès
Sahar Yammine
1International Agency for Research on Cancer, World Health Organization, Lyon, France.
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Inge Huybrechts
1International Agency for Research on Cancer, World Health Organization, Lyon, France.
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Carine Biessy
1International Agency for Research on Cancer, World Health Organization, Lyon, France.
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Laure Dossus
1International Agency for Research on Cancer, World Health Organization, Lyon, France.
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Elom K. Aglago
1International Agency for Research on Cancer, World Health Organization, Lyon, France.
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Sabine Naudin
1International Agency for Research on Cancer, World Health Organization, Lyon, France.
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Pietro Ferrari
1International Agency for Research on Cancer, World Health Organization, Lyon, France.
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Elisabete Weiderpass
1International Agency for Research on Cancer, World Health Organization, Lyon, France.
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Anne Tjønneland
2Diet, Genes and Environment, Danish Cancer Society Research Center, Copenhagen, Denmark.
3Department of Public Health, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark.
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Louise Hansen
2Diet, Genes and Environment, Danish Cancer Society Research Center, Copenhagen, Denmark.
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Kim Overvad
4Denmark Department of Public Health, Aarhus University, Aarhus, Denmark.
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Francesca R. Mancini
5CESP, Faculté de Médecine-Université Paris-Sud, Faculté de Médecine-UVSQ, INSERM, Université Paris-Saclay, Villejuif, France.
6Gustave Roussy, Villejuif, France.
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Marie-Christine Boutron-Ruault
5CESP, Faculté de Médecine-Université Paris-Sud, Faculté de Médecine-UVSQ, INSERM, Université Paris-Saclay, Villejuif, France.
6Gustave Roussy, Villejuif, France.
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Marina Kvaskoff
5CESP, Faculté de Médecine-Université Paris-Sud, Faculté de Médecine-UVSQ, INSERM, Université Paris-Saclay, Villejuif, France.
6Gustave Roussy, Villejuif, France.
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Renée T. Fortner
7The German Cancer Research Center (DKFZ), Heidelberg, Germany.
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Rudolf Kaaks
7The German Cancer Research Center (DKFZ), Heidelberg, Germany.
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Matthias B. Schulze
8German Institute of Human Nutrition Potsdam-Rehbruecke, Nuthetal, Germany.
9Institute of Nutrition Science, University of Potsdam, Nuthetal, Germany.
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Heiner Boeing
8German Institute of Human Nutrition Potsdam-Rehbruecke, Nuthetal, Germany.
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Antonia Trichopoulou
10Hellenic Health Foundation, Athens, Greece.
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Anna Karakatsani
10Hellenic Health Foundation, Athens, Greece.
112nd Pulmonary Medicine Department, School of Medicine, National and Kapodistrian University of Athens, “ATTIKON” University Hospital, Haidari, Greece.
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Carlo La Vecchia
10Hellenic Health Foundation, Athens, Greece.
12Department of Clinical Sciences and Community Health Università degli Studi di Milano, Milan, Italy.
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Vassiliki Benetou
13Department of Hygiene, Epidemiology and Medical Statistics, School of Medicine, National and Kapodistrian University of Athens, Athens, Greece.
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Giovanna Masala
14Cancer Risk Factors and Lifestyle Epidemiology Unit, Institute for Cancer Research, Prevention and Clinical Network, ISPRO, Florence, Italy.
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Vittorio Krogh
15Epidemiology and Prevention Unit, Fondazione IRCCS Istituto Nazionale dei Tumori di Milano, Milan, Italy.
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Amalia Mattiello
16Dipartimento di Medicina Clinica e Chirurgia, University of Naples Federico II, Naples, Italy.
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Alessandra Macciotta
17Department of Clinical and Biological Sciences, University of Turin, Turin, Italy.
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Inger T. Gram
18Faculty of Health Sciences, Department of Community Medicine, University of Tromsø, The Artic University of Norway, Tromsø, Norway.
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Guri Skeie
18Faculty of Health Sciences, Department of Community Medicine, University of Tromsø, The Artic University of Norway, Tromsø, Norway.
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Jose R. Quirós
19Public Health Directorate, Asturias, Spain.
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Antonio Agudo
20Unit of Nutrition and Cancer, Cancer Epidemiology Research Program, Catalan Institute of Oncology - ICO, Group of Research on Nutrition and Cancer, Bellvitge Biomedical Research Institute - IDIBELL, L'Hospitalet of Llobregat, Barcelona, Spain.
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Maria-José Sánchez
21Andalusian School of Public Health (EASP), Granada, Spain.
22Instituto de Investigación Biosanitaria de Granada (ibs. Granada), Granada, Spain.
23CIBER of Epidemiology and Public Health (CIBERESP), Madrid, Spain.
24Universidad de Granada, Granada, Spain.
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Maria-Dolores Chirlaque
23CIBER of Epidemiology and Public Health (CIBERESP), Madrid, Spain.
25Department of Epidemiology, Regional Health Council, IMIB-Arrixaca, Murcia University, Murcia, Spain.
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Eva Ardanaz
23CIBER of Epidemiology and Public Health (CIBERESP), Madrid, Spain.
26Navarra Public Health Institute, Pamplona, Spain.
27IdiSNA, Navarra Institute for Health Research, Pamplona, Spain.
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Leire Gil
28Public Health Division of Gipuzkoa, Biodonostia Health Research Institute, Ministry of Health of the Basque Government, San Sebastian, Spain.
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Hanna Sartor
29Diagnostic Radiology, Department of Translational Medicine, Lund University, Malmö, Sweden.
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Isabel Drake
30Department of Clinical Sciences in Malmö, Lund University, Malmö, Sweden.
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Annika Idahl
31Department of Clinical Sciences, Obstetrics and Gynecology, Umeå, University, Umeå, Sweden.
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Eva Lundin
32Department of Medical Biosciences, Pathology, Umeå University, Umeå, Sweden.
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Dagfinn Aune
33Department of Epidemiology and Biostatistics, School of Public Health, Imperial College London, London, United Kingdom.
34Department of Nutrition, Bjørknes University College, Oslo, Norway.
35Department of Endocrinology, Morbid Obesity and Preventive Medicine, Oslo University Hospital, Oslo, Norway.
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Heather Ward
33Department of Epidemiology and Biostatistics, School of Public Health, Imperial College London, London, United Kingdom.
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Melissa A. Merritt
33Department of Epidemiology and Biostatistics, School of Public Health, Imperial College London, London, United Kingdom.
36University of Hawaii Cancer Center, Population Sciences in the Pacific Program, Honolulu, Hawaii.
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Naomi E. Allen
37Clinical Trial Service Unit and Epidemiological Studies Unit, Nuffield Department of Population Health, University of Oxford, Oxford, United Kingdom.
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Marc J. Gunter
1International Agency for Research on Cancer, World Health Organization, Lyon, France.
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Véronique Chajès
1International Agency for Research on Cancer, World Health Organization, Lyon, France.
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  • For correspondence: chajesv@iarc.fr
DOI: 10.1158/1055-9965.EPI-19-1477 Published September 2020
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Abstract

Background: Fatty acids impact obesity, estrogens, and inflammation, which are risk factors for ovarian cancer. Few epidemiologic studies have investigated the association of fatty acids with ovarian cancer.

Methods: Within the European Prospective Investigation into Cancer and Nutrition (EPIC), 1,486 incident ovarian cancer cases were identified. Cox proportional hazard models with adjustment for ovarian cancer risk factors were used to estimate HRs of ovarian cancer across quintiles of intake of fatty acids. False discovery rate was computed to control for multiple testing. Multivariable conditional logistic regression models were used to estimate ORs of ovarian cancer across tertiles of plasma fatty acids among 633 cases and two matched controls in a nested case–control analysis.

Results: A positive association was found between ovarian cancer and intake of industrial trans elaidic acid [HR comparing fifth with first quintileQ5-Q1 = 1.29; 95% confidence interval (CI) = 1.03–1.62; Ptrend = 0.02, q-value = 0.06]. Dietary intakes of n-6 linoleic acid (HRQ5-Q1 = 1.10; 95% CI = 1.01–1.21; Ptrend = 0.03) and n-3 α-linolenic acid (HRQ5-Q1 = 1.18; 95% CI = 1.05–1.34; Ptrend = 0.007) from deep-frying fats were also positively associated with ovarian cancer. Suggestive associations were reported for circulating elaidic (OR comparing third with first tertileT3-T1 = 1.39; 95% CI = 0.99–1.94; Ptrend = 0.06) and α-linolenic acids (ORT3-T1 = 1.30; 95% CI = 0.98–1.72; Ptrend = 0.06).

Conclusions: Our results suggest that higher intakes and circulating levels of industrial trans elaidic acid, and higher intakes of linoleic acid and α-linolenic acid from deep-frying fat, may be associated with greater risk of ovarian cancer.

Impact: If causal, eliminating industrial trans-fatty acids could offer a straightforward public health action for reducing ovarian cancer risk.

This article is featured in Highlights of This Issue, p. 1697

Footnotes

  • Cancer Epidemiol Biomarkers Prev 2020;29:1739–49

  • Received November 26, 2019.
  • Revision received March 3, 2020.
  • Accepted June 1, 2020.
  • Published first July 2, 2020.
  • ©2020 American Association for Cancer Research.
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Cancer Epidemiology Biomarkers & Prevention: 29 (9)
September 2020
Volume 29, Issue 9
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Dietary and Circulating Fatty Acids and Ovarian Cancer Risk in the European Prospective Investigation into Cancer and Nutrition
Sahar Yammine, Inge Huybrechts, Carine Biessy, Laure Dossus, Elom K. Aglago, Sabine Naudin, Pietro Ferrari, Elisabete Weiderpass, Anne Tjønneland, Louise Hansen, Kim Overvad, Francesca R. Mancini, Marie-Christine Boutron-Ruault, Marina Kvaskoff, Renée T. Fortner, Rudolf Kaaks, Matthias B. Schulze, Heiner Boeing, Antonia Trichopoulou, Anna Karakatsani, Carlo La Vecchia, Vassiliki Benetou, Giovanna Masala, Vittorio Krogh, Amalia Mattiello, Alessandra Macciotta, Inger T. Gram, Guri Skeie, Jose R. Quirós, Antonio Agudo, Maria-José Sánchez, Maria-Dolores Chirlaque, Eva Ardanaz, Leire Gil, Hanna Sartor, Isabel Drake, Annika Idahl, Eva Lundin, Dagfinn Aune, Heather Ward, Melissa A. Merritt, Naomi E. Allen, Marc J. Gunter and Véronique Chajès
Cancer Epidemiol Biomarkers Prev September 1 2020 (29) (9) 1739-1749; DOI: 10.1158/1055-9965.EPI-19-1477

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Dietary and Circulating Fatty Acids and Ovarian Cancer Risk in the European Prospective Investigation into Cancer and Nutrition
Sahar Yammine, Inge Huybrechts, Carine Biessy, Laure Dossus, Elom K. Aglago, Sabine Naudin, Pietro Ferrari, Elisabete Weiderpass, Anne Tjønneland, Louise Hansen, Kim Overvad, Francesca R. Mancini, Marie-Christine Boutron-Ruault, Marina Kvaskoff, Renée T. Fortner, Rudolf Kaaks, Matthias B. Schulze, Heiner Boeing, Antonia Trichopoulou, Anna Karakatsani, Carlo La Vecchia, Vassiliki Benetou, Giovanna Masala, Vittorio Krogh, Amalia Mattiello, Alessandra Macciotta, Inger T. Gram, Guri Skeie, Jose R. Quirós, Antonio Agudo, Maria-José Sánchez, Maria-Dolores Chirlaque, Eva Ardanaz, Leire Gil, Hanna Sartor, Isabel Drake, Annika Idahl, Eva Lundin, Dagfinn Aune, Heather Ward, Melissa A. Merritt, Naomi E. Allen, Marc J. Gunter and Véronique Chajès
Cancer Epidemiol Biomarkers Prev September 1 2020 (29) (9) 1739-1749; DOI: 10.1158/1055-9965.EPI-19-1477
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