Abstract
Purpose
We examined the associations between intake of meat and fish by preparation methods and breast cancer in the Carolina Breast Cancer Study, a racially diverse population-based case–control study.
Methods
African American (AA) and European American (EA) women aged 20–74 years with a first diagnosis of invasive or in situ breast cancers were frequency matched by race and age group to controls identified through the North Carolina Division of Motor Vehicles and Medicare lists [AA: 548 cases, 452 controls; EA: 858 cases, 748 controls]. Participants self-reported meat preparation methods and intake frequencies. Adjusted odds ratios (OR) and 95% confidence intervals (CIs) were calculated using multivariable logistic regression adjusted for age, race, alcohol intake, body mass index, family income, lactation, marital status, use of oral contraceptives, postmenopausal hormone use, smoking status, and offsets.
Results
Positive associations with breast cancer were observed for intakes of grilled/barbecued hamburger (≥ once/week, OR: 1.28; 95% CI 1.01, 1.63), and pan-fried/oven-broiled beef steak (≥ once/week, OR: 1.36; 95% CI 1.08, 1.72). Inverse associations were observed for pan-fried fish (≥ once/week, OR: 0.77; 95% CI 0.60, 0.98), and for grilled/ barbecued pork chops (> 0 time/week OR: 0.81, 95% CI 0.68, 0.97). Associations tended to be stronger among EA women than among AA women.
Conclusion
More frequent consumption of beef prepared with high temperature methods was associated with higher odds of breast cancer while more frequent consumption of pan-fried fish or grilled/barbecued pork chops was associated with lower odds of breast cancer.
Similar content being viewed by others
Data availability
Data from the Carolina Breast Cancer Study can be requested from study investigators at the following: https://unclineberger.org/cbcs/for-researchers/data-sharing/.
Abbreviations
- AA:
-
African American
- BMI:
-
Body mass index
- CBCS:
-
Carolina Breast Cancer Study
- CI:
-
Confidence interval
- CIS:
-
Carcinoma in situ
- DAG:
-
Directed acyclic graph
- DCIS:
-
Ductal carcinoma in situ
- EA:
-
European American
- ER:
-
Estrogen receptor
- HCA:
-
Heterocyclic amines
- HER:
-
Human epidermal growth factor receptor
- IHC:
-
Immunohistochemistry
- LCIS:
-
Lobular carcinoma in situ
- NOCs:
-
N-Nitroso compounds
- OR:
-
Odds ratio
- PAH:
-
Polycyclic aromatic hydrocarbons
- PR:
-
Progesterone receptor
- PUFA:
-
Polyunsaturated fatty acid
References
Siegel RL, Miller KD, Fuchs HE, Jemal A (2021) Cancer statistics. CA Cancer J Clin 71(1):7–33. https://doi.org/10.3322/caac.21654
Boldo E, Castello A, Aragones N, Amiano P, Perez-Gomez B, Castano-Vinyals G, Martin V, Guevara M, Urtiaga C, Dierssen-Sotos T, Fernandez-Tardon G, Moreno V, Solans M, Peiro R, Capelo R, Gomez-Acebo I, Castilla J, Molina AJ, Castells X, Altzibar JM, Lope V, Kogevinas M, Romieu I, Pollan M (2018) Meat intake, methods and degrees of cooking and breast cancer risk in the MCC-Spain study. Maturitas 110:62–70. https://doi.org/10.1016/j.maturitas.2018.01.020
Wu J, Zeng R, Huang J, Li X, Zhang J, Ho JC, Zheng Y (2016) Dietary protein sources and Incidence of Breast Cancer: A Dose-Response Meta-Analysis of Prospective Studies. Nutrients. https://doi.org/10.3390/nu8110730
International Agency for Research on Cancer (2018) Red meat and processed meat. For more information contact publications@iarc.fr. International Agency for Research on Cancer, Lyon
Papaioannou MD, Koufaris C, Gooderham NJ (2014) The cooked meat-derived mammary carcinogen 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP) elicits estrogenic-like microRNA responses in breast cancer cells. Toxicol Lett 229(1):9–16. https://doi.org/10.1016/j.toxlet.2014.05.021
White AJ, Bradshaw PT, Herring AH, Teitelbaum SL, Beyea J, Stellman SD, Steck SE, Mordukhovich I, Eng SM, Engel LS, Conway K, Hatch M, Neugut AI, Santella RM, Gammon MD (2016) Exposure to multiple sources of polycyclic aromatic hydrocarbons and breast cancer incidence. Environ Int 89–90:185–192. https://doi.org/10.1016/j.envint.2016.02.009
Clarke RE, Dordevic AL, Tan SM, Ryan L, Coughlan MT (2016) Dietary Advanced Glycation End Products and Risk Factors for Chronic Disease: A Systematic Review of Randomised Controlled Trials. Nutrients 8(3):125. https://doi.org/10.3390/nu8030125
Uribarri J, Cai W, Sandu O, Peppa M, Goldberg T, Vlassara H (2005) Diet-derived advanced glycation end products are major contributors to the body’s AGE pool and induce inflammation in healthy subjects. Ann N Y Acad Sci 1043:461–466. https://doi.org/10.1196/annals.1333.052
Omofuma OO, Turner DP, Peterson LL, Merchant AT, Zhang J, Steck SE (2020) Dietary Advanced Glycation End-products (AGE) and Risk of Breast Cancer in the Prostate, Lung, Colorectal and Ovarian Cancer Screening Trial (PLCO). Cancer Prev Res (Phila) 13(7):601–610. https://doi.org/10.1158/1940-6207.CAPR-19-0457
Peterson LL, Park S, Park Y, Colditz GA, Anbardar N, Turner DP (2020) Dietary advanced glycation end products and the risk of postmenopausal breast cancer in the National Institutes of Health-AARP Diet and Health Study. Cancer 126(11):2648–2657. https://doi.org/10.1002/cncr.32798
Inoue-Choi M, Sinha R, Gierach GL, Ward MH (2016) Red and processed meat, nitrite, and heme iron intakes and postmenopausal breast cancer risk in the NIH-AARP Diet and Health Study. Int J Cancer 138(7):1609–1618. https://doi.org/10.1002/ijc.29901
Lo JJ, Park YM, Sinha R, Sandler DP (2020) Association between meat consumption and risk of breast cancer: Findings from the Sister Study. Int J Cancer 146(8):2156–2165. https://doi.org/10.1002/ijc.32547
Fu Z, Deming SL, Fair AM, Shrubsole MJ, Wujcik DM, Shu XO, Kelley M, Zheng W (2011) Well-done meat intake and meat-derived mutagen exposures in relation to breast cancer risk: the Nashville Breast Health Study. Breast Cancer Res Treat 129(3):919–928. https://doi.org/10.1007/s10549-011-1538-7
Guo J, Wei W, Zhan L (2015) Red and processed meat intake and risk of breast cancer: a meta-analysis of prospective studies. Breast Cancer Res Treat 151(1):191–198. https://doi.org/10.1007/s10549-015-3380-9
Steck SE, Gaudet MM, Eng SM, Britton JA, Teitelbaum SL, Neugut AI, Santella RM, Gammon MD (2007) Cooked meat and risk of breast cancer–lifetime versus recent dietary intake. Epidemiology 18(3):373–382. https://doi.org/10.1097/01.ede.0000259968.11151.06
Wu K, Sinha R, Holmes MD, Giovannucci E, Willett W, Cho E (2010) Meat mutagens and breast cancer in postmenopausal women–a cohort analysis. Cancer Epidemiol Biomark Prev 19(5):1301–1310. https://doi.org/10.1158/1055-9965.epi-10-0002
Alexander DD, Morimoto LM, Mink PJ, Cushing CA (2010) A review and meta-analysis of red and processed meat consumption and breast cancer. Nutr Res Rev 23(2):349–365. https://doi.org/10.1017/s0954422410000235
Farvid MS, Stern MC, Norat T, Sasazuki S, Vineis P, Weijenberg MP, Wolk A, Wu K, Stewart BW, Cho E (2018) Consumption of red and processed meat and breast cancer incidence: a systematic review and meta-analysis of prospective studies. Int J Cancer 143(11):2787–2799. https://doi.org/10.1002/ijc.31848
Wang Y, Beydoun MA, Caballero B, Gary TL, Lawrence R (2010) Trends and correlates in meat consumption patterns in the US adult population. Public Health Nutr 13(9):1333–1345. https://doi.org/10.1017/s1368980010000224
Chandran U, Zirpoli G, Ciupak G, McCann SE, Gong Z, Pawlish K, Lin Y, Demissie K, Ambrosone CB, Bandera EV (2013) Racial disparities in red meat and poultry intake and breast cancer risk. Cancer Causes Control 24(12):2217–2229. https://doi.org/10.1007/s10552-013-0299-5
Larsson SC, Bergkvist L, Wolk A (2009) Long-term meat intake and risk of breast cancer by oestrogen and progesterone receptor status in a cohort of Swedish women. Eur J Cancer (Oxf, Engl 1990) 45(17):3042–3046. https://doi.org/10.1016/j.ejca.2009.04.035
Newman B, Moorman PG, Millikan R, Qaqish BF, Geradts J, Aldrich TE, Liu ET (1995) The Carolina Breast Cancer Study: integrating population-based epidemiology and molecular biology. Breast Cancer Res Treat 35(1):51–60
Weinberg CR, Wacholder S (1990) The design and analysis of case-control studies with biased sampling. Biometrics 46(4):963–975
Weinberg CR, Sandler DP (1991) Randomized recruitment in case-control studies. Am J Epidemiol 134(4):421–432
Carey LA, Perou CM, Livasy CA, Dressler LG, Cowan D, Conway K, Karaca G, Troester MA, Tse CK, Edmiston S, Deming SL, Geradts J, Cheang MC, Nielsen TO, Moorman PG, Earp HS, Millikan RC (2006) Race, breast cancer subtypes, and survival in the Carolina Breast Cancer Study. JAMA 295(21):2492–2502. https://doi.org/10.1001/jama.295.21.2492
Anderson JJ, Darwis NDM, Mackay DF, Celis-Morales CA, Lyall DM, Sattar N, Gill JMR, Pell JP (2018) Red and processed meat consumption and breast cancer: UK Biobank cohort study and meta-analysis. Eur J Cancer (Oxf, Engl 1990) 90:73–82. https://doi.org/10.1016/j.ejca.2017.11.022
Genkinger JM, Makambi KH, Palmer JR, Rosenberg L, Adams-Campbell LL (2013) Consumption of dairy and meat in relation to breast cancer risk in the Black Women’s Health Study. Cancer Causes Control (CCC) 24(4):675–684. https://doi.org/10.1007/s10552-013-0146-8
Holmes MD, Colditz GA, Hunter DJ, Hankinson SE, Rosner B, Speizer FE, Willett WC (2003) Meat, fish and egg intake and risk of breast cancer. Int J Cancer 104(2):221–227. https://doi.org/10.1002/ijc.10910
Diallo A, Deschasaux M, Latino-Martel P, Hercberg S, Galan P, Fassier P, Alles B, Gueraud F, Pierre FH, Touvier M (2018) Red and processed meat intake and cancer risk: results from the prospective NutriNet-Sante cohort study. Int J Cancer 142(2):230–237. https://doi.org/10.1002/ijc.31046
Han MA, Zeraatkar D, Guyatt GH, Vernooij RWM, El Dib R, Zhang Y, Algarni A, Leung G, Storman D, Valli C, Rabassa M, Rehman N, Parvizian MK, Zworth M, Bartoszko JJ, Lopes LC, Sit D, Bala MM, Alonso-Coello P, Johnston BC (2019) Reduction of red and processed meat intake and cancer mortality and incidence: a systematic review and meta-analysis of cohort studies. Ann Intern Med 171(10):711–720. https://doi.org/10.7326/M19-0699
Dai Q, Shu XO, Jin F, Gao YT, Ruan ZX, Zheng W (2002) Consumption of animal foods, cooking methods, and risk of breast cancer. Cancer Epidemiol Biomark Prev 11(9):801–808
Delfino RJ, Sinha R, Smith C, West J, White E, Lin HJ, Liao SY, Gim JS, Ma HL, Butler J, Anton-Culver H (2000) Breast cancer, heterocyclic aromatic amines from meat and N-acetyltransferase 2 genotype. Carcinogenesis 21(4):607–615. https://doi.org/10.1093/carcin/21.4.607
Zheng W, Gustafson DR, Sinha R, Cerhan JR, Moore D, Hong CP, Anderson KE, Kushi LH, Sellers TA, Folsom AR (1998) Well-done meat intake and the risk of breast cancer. J Natl Cancer Inst 90(22):1724–1729. https://doi.org/10.1093/jnci/90.22.1724
Pala V, Krogh V, Berrino F, Sieri S, Grioni S, Tjonneland A, Olsen A, Jakobsen MU, Overvad K, Clavel-Chapelon F, Boutron-Ruault MC, Romieu I, Linseisen J, Rohrmann S, Boeing H, Steffen A, Trichopoulou A, Benetou V, Naska A, Vineis P, Tumino R, Panico S, Masala G, Agnoli C, Engeset D, Skeie G, Lund E, Ardanaz E, Navarro C, Sanchez MJ, Amiano P, Svatetz CA, Rodriguez L, Wirfalt E, Manjer J, Lenner P, Hallmans G, Peeters PH, van Gils CH, Bueno-de-Mesquita HB, van Duijnhoven FJ, Key TJ, Spencer E, Bingham S, Khaw KT, Ferrari P, Byrnes G, Rinaldi S, Norat T, Michaud DS, Riboli E (2009) Meat, eggs, dairy products, and risk of breast cancer in the European Prospective Investigation into Cancer and Nutrition (EPIC) cohort. Am J Clin Nutr 90(3):602–612. https://doi.org/10.3945/ajcn.2008.27173
Gertig DM, Hankinson SE, Hough H, Spiegelman D, Colditz GA, Willett WC, Kelsey KT, Hunter DJ (1999) N-acetyl transferase 2 genotypes, meat intake and breast cancer risk. Int J Cancer 80(1):13–17
Kim J, Lim SY, Shin A, Sung MK, Ro J, Kang HS, Lee KS, Kim SW, Lee ES (2009) Fatty fish and fish omega-3 fatty acid intakes decrease the breast cancer risk: a case-control study. BMC Cancer 9:216. https://doi.org/10.1186/1471-2407-9-216
Zheng JS, Hu XJ, Zhao YM, Yang J, Li D (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 (Clin Res Ed) 346:f3706. https://doi.org/10.1136/bmj.f3706
Smith JS, Ameri F, Gadgil P (2008) Effect of marinades on the formation of heterocyclic amines in grilled beef steaks. J Food Sci 73(6):T100-105
Viegas O, Yebra-Pimentel I, Martinez-Carballo E, Simal-Gandara J, Ferreira IM (2014) Effect of beer marinades on formation of polycyclic aromatic hydrocarbons in charcoal-grilled pork. J Agric Food Chem 62(12):2638–2643. https://doi.org/10.1021/jf404966w
Nerurkar PV, Le Marchand L, Cooney RV (1999) Effects of marinating with Asian marinades or western barbecue sauce on PhIP and MeIQx formation in barbecued beef. Nutr Cancer 34(2):147–152. https://doi.org/10.1207/s15327914nc3402_4
Newman LA, Kaljee LM (2017) Health disparities and triple-negative breast cancer in African American women: a review. JAMA Surg 152(5):485–493. https://doi.org/10.1001/jamasurg.2017.0005
Rebbeck TR (1997) Molecular epidemiology of the human glutathione S-transferase genotypes GSTM1 and GSTT1 in cancer susceptibility. Cancer Epidemiol Biomark Prev 6(9):733–743
Cotton SC, Sharp L, Little J, Brockton N (2000) Glutathione S-transferase polymorphisms and colorectal cancer: a HuGE review. Am J Epidemiol 151(1):7–32. https://doi.org/10.1093/oxfordjournals.aje.a010124
Sinha R, Rothman N, Salmon CP, Knize MG, Brown ED, Swanson CA, Rhodes D, Rossi S, Felton JS, Levander OA (1998) Heterocyclic amine content in beef cooked by different methods to varying degrees of doneness and gravy made from meat drippings. Food Chem Toxicol 36(4):279–287
Skog K, Steineck G, Augustsson K, Jagerstad M (1995) Effect of cooking temperature on the formation of heterocyclic amines in fried meat products and pan residues. Carcinogenesis 16(4):861–867. https://doi.org/10.1093/carcin/16.4.861
Larsson BK (1986) Formation of polycyclic aromatic hydrocarbons during the smoking and grilling of food. Prog Clin Biol Res 206:169–180
Cross AJ, Pollock JR, Bingham SA (2003) Haem, not protein or inorganic iron, is responsible for endogenous intestinal N-nitrosation arising from red meat. Cancer Res 63(10):2358–2360
Joosen AM, Kuhnle GG, Aspinall SM, Barrow TM, Lecommandeur E, Azqueta A, Collins AR, Bingham SA (2009) Effect of processed and red meat on endogenous nitrosation and DNA damage. Carcinogenesis 30(8):1402–1407. https://doi.org/10.1093/carcin/bgp130
Kuhnle GG, Story GW, Reda T, Mani AR, Moore KP, Lunn JC, Bingham SA (2007) Diet-induced endogenous formation of nitroso compounds in the GI tract. Free Radic Biol Med 43(7):1040–1047. https://doi.org/10.1016/j.freeradbiomed.2007.03.011
Sinha R, Rothman N (1997) Exposure assessment of heterocyclic amines (HCAs) in epidemiologic studies. Mutat Res 376(1–2):195–202
Acknowledgements
We are grateful to CBCS participants and study staff.
Funding
This work was supported by a Susan G. Komen Graduate Training in Disparities Research Grant (GTDR17500160; SES, OOO) and a Cancer Prevention Research Fellowship from the American Society of Preventive Oncology and the Prevent Cancer Foundation (SES); This research was supported by a grant from UNC Lineberger Comprehensive Cancer Center, which is funded by the University Cancer Research Fund of North Carolina, the Susan G Komen Foundation, the National Cancer Institute of the National Institutes of Health (P01CA151135), and the National Cancer Institute Specialized Program of Research Excellence (SPORE) in Breast Cancer (NIH/NCI P50-CA58223). This research recruited participants and/or obtained data with the assistance of Rapid Case Ascertainment, a collaboration between the North Carolina Central Cancer Registry and UNC Lineberger. RCA is supported by a grant from the National Cancer Institute of the National Institutes of Health (P30CA016086). We are grateful to CBCS participants and study staff.
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Data analysis was performed by Omonefe Omofuma. The first draft of the manuscript was written by Omonefe Omofuma and all authors commented on subsequent versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no relevant financial or non-financial interests to disclose.
Ethical approval
This study was conducted according to the guidelines laid down in the Declaration of Helsinki and all procedures involving research study participants were approved by the Institutional Review Board at the University of North Carolina at Chapel Hill (UNC IRB#92-0410). The current analyses of deidentified existing data were reviewed by the University of South Carolina Institutional Review Board and declared not human subjects research (#PR00074227).
Consent to participate
Informed consent was obtained from all individual participants included in the study.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Omofuma, O.O., Steck, S.E., Olshan, A.F. et al. The association between meat and fish intake by preparation methods and breast cancer in the Carolina Breast Cancer Study (CBCS). Breast Cancer Res Treat 193, 187–201 (2022). https://doi.org/10.1007/s10549-022-06555-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10549-022-06555-x