Omega-3 fatty acids for breast cancer prevention and survivorship

Breast Cancer Research

Volumn 17, Issue 1, 2015, Pages

  Fabian, Carol J ^a   Kimler, Bruce F ^b   Hursting, Stephen D ^c  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

^c University of North Carolina at Chapel Hill   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOCOSAHEXAENOIC ACID; ICOSAPENTAENOIC ACID; OMEGA 3 FATTY ACID; OMEGA 6 FATTY ACID;

BREAST CANCER; CANCER MODEL; CANCER PREVENTION; CANCER RECURRENCE; CANCER RISK; CANCER SURVIVAL; CANCER SURVIVOR; CASE CONTROL STUDY; COGNITION; COHORT ANALYSIS; DIETARY REFERENCE INTAKE; FAT INTAKE; FATTY ACID METABOLISM; HEART DISEASE; HUMAN; INSULIN RESISTANCE; INTERVENTION STUDY; PHARMACODYNAMICS; PRIMARY PREVENTION; PROSPECTIVE STUDY; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; WEIGHT GAIN; ANIMAL; BREAST NEOPLASMS; DIETARY SUPPLEMENT; DISEASE MODEL; FEMALE; METABOLISM; MORTALITY; PRECLINICAL STUDY; RISK; SURVIVOR;

ANIMALS; BREAST NEOPLASMS; DIETARY SUPPLEMENTS; DISEASE MODELS, ANIMAL; DOCOSAHEXAENOIC ACIDS; DRUG EVALUATION, PRECLINICAL; EICOSAPENTAENOIC ACID; FATTY ACIDS, OMEGA-3; FATTY ACIDS, OMEGA-6; FEMALE; HUMANS; RISK; SURVIVORS;

EID: 84929154245     PISSN: 14655411     EISSN: 1465542X     Source Type: Journal    
DOI: 10.1186/s13058-015-0571-6     Document Type: Review

References (95)

1. Howe LR, Subbaramaiah K, Hudis CA, Dannenberg AJ. Molecular pathways: adipose inflammation as a mediator of obesity-associated cancer. Clin Cancer Res. 2013;19:6074-83.
2. Baumgarten SC, Minireview FJ. Inflammation: an instigator of more aggressive estrogen receptor (ER) positive breast cancers. Mol Endocrinol. 2012;26:360-71.
3. Hussein MR, Hassan HI. Analysis of the mononuclear inflammatory cell infiltrate in the normal breast, benign proliferative breast disease, in situ and infiltrating ductal breast carcinomas: preliminary observations. J Clin Pathol. 2006;59:972-7.
4. Pollard J. Macrophages define the invasive microenvironment in breast cancer. J Leukoc Biol. 2008;84:623-30.
5. McDermott RS, Beuvon F, Pauly M, Pallud C, Vincent-Salomon A, Mosseri V, et al. Tumor antigens and antigen-presenting capacity in breast cancer. Pathobiology. 2002;70:324-9.
6. Greenberg AS, Obin MS. Obesity and the role of adipose tissue in inflammation and metabolism. Am J Clin Nutr. 2006;83:461S-5S.
7. Weylandt KH, Chiu CY, Gomolka B, Waechter SF, Wiedenmann B. Omega-3 fatty acids and their lipid mediators: towards an understanding of resolvin and protectin formation. Prostaglandins Other Lipid Mediat. 2012;97:73-82.
8. Turk HF, Chapkin RS. Membrane lipid raft organization is uniquely modified by n-3 polyunsaturated fatty acids. Prostaglandins Leukot Essent Fatty Acids. 2013;88:43-7.
9. Calder PC. n-3 fatty acids, inflammation and immunity: new mechanisms to explain old actions. Proc Nutr Soc. 2013;72:326-36.
10. Ravacci GR, Brentani MM, Tortelli Jr T, Torrinhas RS, Saldanha T, Torres EA, et al. Lipid raft disruption by docosahexaenoic acid induces apoptosis in transformed human mammary luminal epithelial cells harboring HER-2 overexpression. J Nutr Biochem. 2013;24:505-15.
11. Lee EJ, Yun UJ, Koo KH, Sung JY, Shim J, Ye SK, et al. Down-regulation of lipid raft-associated onco-proteins via cholesterol-dependent lipid raft internalization in docosahexaenoic acid-induced apoptosis. Biochim Biophys Acta. 1841;2014:190-203.
12. Rogers KR, Kikawa KD, Mouradian M, Hernandez K, McKinnon KM, Ahwah SM, et al. Docosahexaenoic acid alters epidermal growth factor receptor-related signaling by disrupting its lipid raft association. Carcinogenesis. 2010;31:1523-30.
13. Calder PC. Fatty acids and inflammation: the cutting edge between food and pharma. Eur J Pharmacol. 2011;668:S50-8.
14. Wen ZH, Su YC, Lai PL, Zhang Y, Xu YF, Zhao A, et al. Critical role of arachidonic acid-activated mTOR signaling in breast carcinogenesis and angiogenesis. Oncogene. 2013;32:160-70.
15. Yates CM, Calder PC, Ed RG. Pharmacology and therapeutics of omega-3 polyunsaturated fatty acids in chronic inflammatory disease. Pharmacol Ther. 2014;141:272-81.
16. Simopoulos AP. Evolutionary aspects of diet, the omega-6/omega-3 ratio and genetic variation: nutritional implications for chronic diseases. Biomed Pharmacother. 2006;60:502-7.
17. Friborg JT, Melbye M. Cancer patterns in Inuit populations. Lancet Oncol. 2008;9:892-900.
18. Su H-M. Mechanisms of n-3 fatty acid-mediated development and maintenance of learning memory performance neuroprotection. J Nutr Biochem. 2010;21:364-73.
19. Cole GM, Ma QL, Frautschy SA. Omega-3 fatty acids and dementia. Prostaglandins Leukot Essent Fatty Acids. 2009;81:213-21.
20. Simopoulos AP. Evolutionary aspects of omega-3 fatty acids in the food supply. Prostaglandins Leukot Essent Fatty Acids. 1999;60:421-9.
21. Blasbalg TL, Hibbeln JR, Ramsden CE, Majchrzak SF, Rawlings RR. Changes in consumption of omega-3 and omega-6 fatty acids in the United States during the 20th century. Am J Clin Nutr. 2011;93:950-62.
22. Rose D, Connolly J. Omega-3 fatty acids as cancer chemopreventive agents. Pharmacol Ther. 1999;83:217-44.
23. Simonsen N, van't Veer P, Strain JJ, Martin-Moreno JM, Huttunen JK, Navajas JF, et al. EURAMIC study. European Community Multicenter Study on Antioxidants, Myocardial Infarction, and Breast Cancer. Am J Epidemiol. 1998;147:342-52.
24. Russo GL. Dietary n-6 and n-3 polyunsaturated fatty acids: from biochemistry to clinical implications in cardiovascular prevention. Biochem Pharmacol. 2009;77:937-46.
25. Brenna JT, Salem Jr N, Sinclair AJ, Cunnane SC. International Society for the Study of Fatty Acids and Lipids, ISSFAL, alpha-linolenic acid supplementation and conversion to n-3 long-chain polyunsaturated fatty acids in humans. Prostaglandins Leukot Essent Fatty Acids. 2009;80:85-91.
26. Calder PC. Omega-3 polyunsaturated fatty acids and inflammatory processes: nutrition or pharmacology? Br J Clin Pharmacol. 2013;75:645-62.
27. Flock MR, Harris WS, Kris-Etherton PM. Long-chain omega-3 fatty acids: time to establish a dietary reference intake. Nutr Rev. 2013;71:692-707.
28. Arterburn LM, Hall EB, Oken H. Distribution, interconversion, and dose response of n-3 fatty acids in humans. Am J Clin Nutr. 2006;83:1467S-76S.
29. Browning LM, Walker CG, Mander AP, West AL, Madden J, Gambell JM, et al. Incorporation of eicosapentaenoic and docosahexaenoic acids into lipid pools when given as supplements providing doses equivalent to typical intakes of oily fish. Am J Clin Nutr. 2012;96:748-58.
30. European Food Safety Authority. Scientific Opinion on the Tolerable Upper Intake Level of eicosapentaenoic acid (EPA), docosahexaenoic acid (DHA) and docosapentaenoic acid (DPA). EFSA J. 2012;10:2815-82.
31. Addendum A. EPA and DHA Content of Fish Species. United States Department of Agriculture. 2004. www.health.gov/dietaryguidelines/dga2005/report/HTML/G2_Analyses.htm # omegafish. Accessed 10 Mar 2015.
32. Jiang W, Zhu Z, McGinley JN, El Bayoumy K, Manni A, Thompson HJ. Identification of a molecular signature underlying inhibition of mammary carcinoma growth by dietary N-3 fatty acids. Cancer Res. 2012;72:3795-806.
33. Manni A, Richie Jr JP, Xu H, Washington S, Aliaga C, Cooper TK, et al. Effects of fish oil and tamoxifen on preneoplastic lesion development and biomarkers of oxidative stress in the early stages of N-methyl-N-nitrosourea-induced rat mammary carcinogenesis. Int J Oncol. 2011;39:1153-64.
34. Manna S, Janarthan M, Ghosh B, Rana B, Rana A, Chatterjee M. Fish oil regulates cell proliferation, protect DNA damages and decrease HER-2/neu and c-Myc protein expression in rat mammary carcinogenesis. Clin Nutr. 2010;29:531-7.
35. Yee LD, Agarwal D, Rosol TJ, Lehman A, Tian M, Hatton J, et al. The inhibition of early stages of HER-2/neu-mediated mammary carcinogenesis by dietary n-3 PUFAs. Mol Nutr Food Res. 2013;57:320-7.
36. Bernard-Gallon D, Vissac-Sabatier C, Antoine-Vincent D, Rio PG, Maurizis JC, Fustier P, et al. Differential effects of n-3 and n-6 polyunsaturated fatty acids on BRCA1 and BRCA2 gene expression in breast cell lines. Br J Nutr. 2002;87:281-9.
37. Jourdan M-L, Mahéo K, Barascu A, Goupille C, De Latour MP, Bougnoux P, et al. Increased BRCA1 protein in mammary tumours of rats fed marine ω-3 fatty acids. Oncol Rep. 2007;17:713-9.
38. Signori C, El-Bayoumy K, Russo J, Thompson HJ, Richie JP, Hartman TJ, et al. Chemoprevention of breast cancer by fish oil in preclinical models: trials and tribulations. Cancer Res. 2011;71:6091-6.
39. MacLennan MB. Mammary tumor development is directly inhibited by lifelong n-3 polyunsaturated fatty acids. J Nutr Biochem. 2013;24:388-95.
40. Yee LD, Young DC, Rosol TJ, VanBuskirk AM, Clinton SK. Dietary (n-3) polyunsaturated fatty acids inhibit HER-2/neu induced breast cancer in mice independently of the PPARγ ligand rosiglitazone. J Nutr. 2005;135:983-8.
41. Chatterjee M, Janarthan M, Manivannan R, Rana A, Chatterjee M. Combinatorial effect of fish oil (Maxepa) and 1alpha,25-dihydroxyvitamin D(3) in the chemoprevention of DMBA-induced mammary carcinogenesis in rats. Chem Biol Interact. 2010;188:102-10.
42. Negi AK, Kansal S, Bhatnagar A, Agnihotri N. Alteration in apoptosis and cell cycle by celecoxib and/or fish oil in 7,12-dimethyl benzene (α) anthracene-induced mammary carcinogenesis. Tumour Biol. 2013;34:3753-64.
43. Manni A, Richie Jr JP, Xu H, Washington S, Aliaga C, Bruggeman R, et al. Influence of omega-3 fatty acids on tamoxifen-induced suppression of rat mammary carcinogenesis. Int J Cancer. 2014;134:1549-57.
44. Katan MB, Deslypere JP, van Birgelen AP, Penders M, Zegwaard M. Kinetics of the incorporation of dietary fatty acids into serum cholesteryl esters, erythrocyte membranes, and adipose tissue: an 18-month controlled study. J Lipid Res. 1997;38:2012-22.
45. Walker CG, Browning LM, Mander AP, Madden J, West AL, Calder PC, et al. Age and sex differences in the incorporation of EPA and DHA into plasma fractions, cells and adipose tissue in humans. Br J Nutr. 2014;111:679-89.
46. Kopecky J, Rossmeisl M, Flachs P, Kuda O, Brauner P, Jilkova Z, et al. n-3 PUFA: bioavailability and modulation of adipose tissue function. Proc Nutr Soc. 2009;68:361-9.
47. Browning LM, Walker CG, Mander AP, West AL, Gambell J, Madden J, et al. Compared with daily, weekly n-3 PUFA intake affects the incorporation of eicosapentaenoic acid and docosahexaenoic acid into platelets and mononuclear cells in humans. J Nutr. 2014;144:667-72.
48. Terry PD, Rohan TE, Wolk A. Intakes of fish and marine fatty acids and the risks of cancers of the breast and prostate and of other hormone-related cancers: a review of the epidemiologic evidence. Am J Clin Nutr. 2003;77:532-43.
49. Yang B, Ren XL, Fu YQ, Gao JL, Li D. 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. 2014;14:105.
50. Chajès V, Torres-Mejía G, Biessy C, Ortega-Olvera C, Angeles-Llerenas A, Ferrari P, et al. ω-3 and ω-6 polyunsaturated fatty acid intakes and the risk of breast cancer in Mexican women: impact of obesity status. Cancer Epidemiol Biomarkers Prev. 2012;21:319-26.
51. Goodstine SL, Zheng T, Holford TR, Ward BA, Carter D, Owens PH, et al. Dietary (n-3)/(n-6) fatty acid ratio: possible relationship to premenopausal but not postmenopausal breast cancer risk in U.S. women. J Nutr. 2003;133:1409-14.
52. Shannon J, King IB, Moshofsky R, Lampe JW, Gao DL, Ray RM, et al. Erythrocyte fatty acids and breast cancer risk: a case-control study in Shanghai. China Am J Clin Nutr. 2007;85:1090-7.
53. Shannon J, King IB, Lampe JW, Gao DL, Ray RM, Lin MG, et al. Erythrocyte fatty acids and risk of proliferative and nonproliferative fibrocystic disease in women in Shanghai. China Am J Clin Nutr. 2009;89:265-76.
54. Kuriki K, Hirose K, Wakai K, Matsuo K, Ito H, Suzuki T, et al. Breast cancer risk and erythrocyte compositions of n-3 highly unsaturated fatty acids in Japanese. Int J Cancer. 2007;121:377-85.
55. Bagga D, Anders KH, Wang HJ, Glaspy JA. Long-chain n-3-to-n-6 polyunsaturated fatty acid ratios in breast adipose tissue from women with and without breast cancer. Nutr Cancer. 2002;42:180-5.
56. Hudson AG, Reeves KW, Modugno F, Wilson JW, Evans RW, Vogel VG, et al. Erythrocyte omega-6 and omega-3 fatty acids and mammographic breast density. Nutr Cancer. 2013;65:410-6.
57. Zheng JS, Hu XJ, Zhao YM, Yang J, Li D. 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. 2013;346:f3706.
58. Gago-Dominguez M, Yuan JM, Sun CL, Lee HP, Yu MC. Opposing effects of dietary n-3 and n-6 fatty acids on mammary carcinogenesis: the Singapore Chinese Health Study. Br J Cancer. 2003;89:1686-92.
59. Wakai K, Tamakoshi K, Date C, Fukui M, Suzuki S, Lin Y, et al. Dietary intakes of fat and fatty acids and risk of breast cancer: a prospective study in Japan. Cancer Sci. 2005;96:590-9.
60. Brasky TM, Lampe JW, Potter JD, Patterson RE, White E. Specialty supplements and breast cancer risk in the VITamins And Lifestyle (VITAL) Cohort. Cancer Epidemiol Biomarkers Prev. 2010;19:1696-708.
61. Kris-Etherton PM, Grieger JA, Etherton TD. Dietary reference intakes for DHA and EPA. Prostaglandins Leukot Essent Fatty Acids. 2009;81:99-104.
62. Yee LD, Lester JL, Cole RM, Richardson JR, Hsu JC, Li Y, et al. Omega-3 fatty acid supplements in women at high risk of breast cancer have dose-dependent effects on breast adipose tissue fatty acid composition. Am J Clin Nutr. 2010;91:1185-94.
63. Flock MR, Skulas-Ray AC, Harris WS, Gaugler TL, Fleming JA, Kris-Etherton PM. Effects of supplemental long-chain omega-3 fatty acids and erythrocyte membrane fatty acid content on circulating inflammatory markers in a randomized controlled trial of healthy adults. Prostaglandins Leukot Essent Fatty Acids. 2014;91:161-8.
64. Yusof HM, Cawood AL, Ding R, Williams JA, Napper FL, Shearman CP, et al. Limited impact of 2 g/day omega-3 fatty acid ethyl esters (Omacor®) on plasma lipids and inflammatory markers in patients awaiting carotid endarterectomy. Mar Drugs. 2013;11:3569-81.
65. Sijben JW, Calder PC. Differential immunomodulation with long-chain n-3 PUFA in health and chronic disease. Proc Nutr Soc. 2007;66:237-59.
66. Signori C, DuBrock C, Richie JP, Prokopczyk B, Demers LM, Hamilton C, et al. Administration of omega-3 fatty acids and raloxifene to women at high risk of breast cancer: interim feasibility and biomarkers analysis from a clinical trial. Eur J Clin Nutr. 2012;66:878-84.
67. Fabian CJ, Kimler BF, Petroff BK, Zalles CM, Metheny T, Nydegger JL, et al. High dose omega-3 fatty acid supplementation modulates breast tissue biomarkers in post-menopausal women at high risk for development of breast cancer [abstract]. Cancer Res. 2013;73:P4-10-01. doi:10.1158/0008-5472.SABCS13-P4-10-01.
68. Fabian CF, Kimler BF, Petroff BK, Zalles CM, Metheny T, Box JA, et al. High dose omega-3 fatty acid (FA) supplementation modulates breast tissue biomarkers in pre-menopausal women at high risk for development of breast cancer [abstract]. J Clin Oncol. 2013;31 Suppl:abstract 1515.
69. Patterson RE. Marine fatty acid intake is associated with breast cancer prognosis. J Nutr. 2011;141:201-6.
70. Kang KS, Wang P, Yamabe N, Fukui M, Jay T, Zhu BT. Docosahexaenoic acid induces apoptosis in MCF-7 cells in vitro and in vivo via reactive oxygen species formation and caspase 8 activation. PLoS One. 2010;5, e10296.
71. Colas S, Mahéo K, Denis F, Goupille C, Hoinard C, Champeroux P, et al. Sensitization by dietary docosahexaenoic acid of rat mammary carcinoma to anthracycline: a role for tumor vascularization. Clin Cancer Res. 2006;12:5879-86.
72. Ewaschuk JB, Newell M, Field CJ. Docosahexanoic acid improves chemotherapy efficacy by inducing CD95 translocation to lipid rafts in ER(-) breast cancer cells. Lipids. 2012;47:1019-30.
73. Bougnoux P, Hajjaji N, Ferrasson MN, Giraudeau B, Couet C, Le Floch O. Improving outcome of chemotherapy of metastatic breast cancer by docosahexaenoic acid: a phase II trial. Br J Cancer. 2009;101:1978-85.
74. Germain E, Bonnet P, Aubourg L, Grangeponte MC, Chajès V, Bougnoux P. Anthracycline-induced cardiac toxicity is not increased by dietary omega-3 fatty acids. Pharmacol Res. 2003;47:111-7.
75. Calder PC, Yaqoob P. Marine omega-3 fatty acids and coronary heart disease. Curr Opin Cardiol. 2012;27:412-9.
76. Baum SJ, Kris-Etherton PM, Willett WC, Lichtenstein AH, Rudel LL, Maki KC, et al. Fatty acids in cardiovascular health and disease: a comprehensive update. J Clin Lipidol. 2012;6:216-34.
77. Bays H. Clinical overview of omacor: a concentrated formulation of omega-3 polyunsaturated fatty acids. Am J Cardiol. 2006;98:71i-6i.
78. ORIGIN Trial Investigators, Bosch J, Gerstein HC, Dagenais GR, Díaz R, Dyal L, et al. n-3 fatty acids and cardiovascular outcomes in patients with dysglycemia. N Engl J Med. 2012;367:309-18.
79. Rizos EC, Ntzani EE, Bika E, Kostapanos MS, Elisaf MS. Association between omega-3 fatty acid supplementation and risk of major cardiovascular disease events: a systematic review and meta-analysis. JAMA. 2012;308:1024-33.
80. Harris WS, Shearer GC. Omega-6 fatty acids and cardiovascular disease: friend or foe? Circulation. 2014;130:1562-4.
81. Bonnet N, Somm E, Rosen CJ. Diet and gene interactions influence the skeletal response to polyunsaturated fatty acids. Bone. 2014;68C:100-7.
82. Hutchins-Wiese HL, Picho K, Watkins BA, Li Y, Tannenbaum S, Claffey K, et al. High-dose eicosapentaenoic acid and docosahexaenoic acid supplementation reduces bone resorption in postmenopausal breast cancer survivors on aromatase inhibitors: a pilot study. Nutr Cancer. 2014;66:68-76.
83. Hershman DL, Unger JM, Crew KD, Dakhil SR, Awad D, Greenlee H, et al. Omega-3 fatty acids for aromatase inhibitor-induced musculoskeletal symptoms in women with early-stage breast cancer (SWOG S0927) [abstract]. J Clin Oncol. 2014;32:5 s Suppl: abstract 9532.
84. Ghoreishi Z, Esfahani A, Djazayeri A, Djalali M, Golestan B, Ayromlou H, et al. Omega-3 fatty acids are protective against paclitaxel-induced peripheral neuropathy: a randomized double-blind placebo controlled trial. BMC Cancer. 2012;12:355.
85. Flock MR, Rogers CJ, Prabhu KS, Kris-Etherton PM. Immunometabolic role of long-chain omega-3 fatty acids in obesity-induced inflammation. Diabetes Metab Res Rev. 2013;29:431-45.
86. Fedor D, Kelley DS. Prevention of insulin resistance by n-3 polyunsaturated fatty acids. Curr Opin Clin Nutr Metab Care. 2009;12:138-46.
87. Buckley JD, Howe PRC. Long-chain omega-3 polyunsaturated fatty acids may be beneficial for reducing obesity - a review. Nutrients. 2010;2:1212-30.
88. Di Girolamo FG, Situlin R, Mazzucco S, Valentini R, Toigo G, Biolo G. Omega-3 fatty acids and protein metabolism: enhancement of anabolic interventions for sarcopenia. Curr Opin Clin Nutr Metab Care. 2014;17:145-50.
89. McDonald C, Bauer J, Capra S, Coll J. The muscle mass, omega-3, diet, exercise and lifestyle (MODEL) study - a randomised controlled trial for women who have completed breast cancer treatment. BMC Cancer. 2014;14:264.
90. Wefel JS, Saleeba AK, Buzdar AU, Meyers CA. Acute and late onset cognitive dysfunction associated with chemotherapy in women with breast cancer. Cancer. 2010;116:3348-56.
91. Janelsins MC, Kesler SR, Ahles TA, Morrow GR. Prevalence, mechanisms, and management of cancer-related cognitive impairment. Int Rev Psychiatry. 2014;26:102-13.
92. Yurko-Mauro K, McCarthy D, Rom D, Nelson EB, Ryan AS, Blackwell A, et al. Beneficial effects of docosahexaenoic acid on cognition in age-related cognitive decline. Alzheimers Dement. 2010;6:456-64.
93. Mazereeuw G, Lanctôt KL, Chau SA, Swardfager W, Herrmann N. Effects of ω-3 fatty acids on cognitive performance: a meta-analysis. Neurobiol Aging. 2012;33:1482.e17-29.
94. Ye S, Tan L, Ma J, Shi Q, Li J. Polyunsaturated docosahexaenoic acid suppresses oxidative stress induced endothelial cell calcium influx by altering lipid composition in membrane caveolar rafts. Prostaglandins Leukot Essent Fatty Acids. 2010;83:37-43.
95. Chalon S. Omega-3 fatty acids and monoamine neurotransmission. Prostaglandins Leukot Essent Fatty Acids. 2006;75:259-69.