Hostname: page-component-8448b6f56d-42gr6 Total loading time: 0 Render date: 2024-04-25T05:48:49.698Z Has data issue: false hasContentIssue false
  • English
  • Français

Serum levels of n-3 PUFA and colorectal cancer risk in Chinese population

Published online by Cambridge University Press:  07 February 2023

Dan-Dan Shi ,
Yu-Jing Fang ,
Yi-Ling Jiang ,
Ting Dong ,
Zhuo-Lin Zhang ,
Ting Ma ,
Ruo-Lin Zhou ,
Qing-Jian Ou  and
Cai-Xia Zhang Open the ORCID record for Cai-Xia Zhang [Opens in a new window]
Dan-Dan Shi
Affiliation:
Department of Epidemiology, School of Public Health, Sun Yat-sen University, Guangzhou 510080, People’s Republic of China
Yu-Jing Fang
Affiliation:
Department of Experimental Research, Sun Yat-sen University Cancer Center, State Key Laboratory of Oncology in South China, Collaborative Innovation Center for Cancer Medicine, 651 Dongfeng Road East, Guangzhou 510060, People’s Republic of China
Yi-Ling Jiang
Affiliation:
Department of Epidemiology, School of Public Health, Sun Yat-sen University, Guangzhou 510080, People’s Republic of China
Ting Dong
Affiliation:
Department of Epidemiology, School of Public Health, Sun Yat-sen University, Guangzhou 510080, People’s Republic of China
Zhuo-Lin Zhang
Affiliation:
Department of Epidemiology, School of Public Health, Sun Yat-sen University, Guangzhou 510080, People’s Republic of China
Ting Ma
Affiliation:
Department of Epidemiology, School of Public Health, Sun Yat-sen University, Guangzhou 510080, People’s Republic of China
Ruo-Lin Zhou
Affiliation:
Department of Epidemiology, School of Public Health, Sun Yat-sen University, Guangzhou 510080, People’s Republic of China
Qing-Jian Ou
Affiliation:
Department of Experimental Research, Sun Yat-sen University Cancer Center, State Key Laboratory of Oncology in South China, Collaborative Innovation Center for Cancer Medicine, 651 Dongfeng Road East, Guangzhou 510060, People’s Republic of China
Cai-Xia Zhang*
Affiliation:
Department of Epidemiology, School of Public Health, Sun Yat-sen University, Guangzhou 510080, People’s Republic of China
*
*Corresponding author: Cai-Xia Zhang, email zhangcx3@mail.sysu.edu.cn
Get access Rights & Permissions [Opens in a new window]

Abstract

Circulating n-3 PUFA, which integrate endogenous and exogenous n-3 PUFA, can be better used to investigate the relationship between n-3 PUFA and disease. However, studies examining the associations between circulating n-3 PUFA and colorectal cancer (CRC) risk were limited, and the results remained inconclusive. This case–control study aimed to examine the association between serum n-3 PUFA and CRC risk in Chinese population. A total of 680 CRC cases and 680 sex- and age-matched (5-year interval) controls were included. Fatty acids were assayed by GC. OR and 95 % CI were calculated using multivariable logistic regression after adjustment for potential confounders. Higher level of serum α-linolenic acid (ALA), docosapentaenoic acid (DPA), DHA, long-chain n-3 PUFA and total n-3 PUFA were associated with lower odds of CRC. The adjusted OR and 95 % CI were 0·34 (0·24, 0·49, Pfor trend < 0·001) for ALA, 0·57 (0·40, 0·80, Pfor trend < 0·001) for DPA, 0·48 (0·34, 0·68, Pfor trend < 0·001) for DHA, 0·39 (0·27, 0·56, Pfor trend < 0·001) for long-chain n-3 PUFA and 0·31 (0·22, 0·45, Pfor trend < 0·001) for total n-3 PUFA comparing the highest with the lowest quartile. However, there was no statistically significant association between EPA and odds of CRC. Analysis stratified by sex showed that ALA, DHA, long-chain n-3 PUFA and total n-3 PUFA were inversely associated with odds of CRC in both sexes. This study indicated that serum ALA, DPA, DHA, long-chain n-3 PUFA and total n-3 PUFA were inversely associated with odds of having CRC in Chinese population.

Keywords

DHAn-3 PUFABiomarkerSerumColorectal cancer
Type
Research Article
Information
British Journal of Nutrition , Volume 130 , Issue 7 , 14 October 2023 , pp. 1239 - 1249
Check for updates
Copyright
© The Author(s), 2023. Published by Cambridge University Press on behalf of The Nutrition Society

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

†

These authors contributed equally to this work.

References

Siegel, RL, Miller, KD, Fuchs, HE, et al. (2022) Cancer statistics, 2022. CA: Cancer J Clin 72, 7–33.Google Scholar
Cao, W, Chen, HD, Yu, YW, et al. (2021) Changing profiles of cancer burden worldwide and in China: a secondary analysis of the global cancer statistics 2020. Chin Med J 134, 783–791.CrossRefGoogle Scholar
International WCRF (2022) Diet, Activity and Cancer-Cancer Risk Factors. https://www.wcrf.org/diet-activity-and-cancer/risk-factors/ (accessed February 2022).Google Scholar
Larsson, SC, Kumlin, M, Ingelman-Sundberg, M, et al. (2004) Dietary long-chain n-3 fatty acids for the prevention of cancer: a review of potential mechanisms. Am J Clin Nutr 79, 935–945.CrossRefGoogle Scholar
Giovannucci, E & Goldin, B (1997) The role of fat, fatty acids, and total energy intake in the etiology of human colon cancer. Am J Clin Nutr 66, 1564s–1571s.CrossRefGoogle ScholarPubMed
Rose, DP & Connolly, JM (1999) n-3 fatty acids as cancer chemopreventive agents. Pharmacol Ther 83, 217–244.CrossRefGoogle ScholarPubMed
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. Carcinog 20, 2209–2218.CrossRefGoogle ScholarPubMed
Guertin, DA & Sabatini, DM (2007) Defining the role of mTOR in cancer. Cancer Cell 12, 9–22.CrossRefGoogle ScholarPubMed
Zhang, YJ, Dai, Q, Sun, DF, et al. (2009) mTOR signaling pathway is a target for the treatment of colorectal cancer. Ann Surg Oncol 16, 2617–2628.CrossRefGoogle ScholarPubMed
Zhong, X, Fang, YJ, Pan, ZZ, et al. (2013) Dietary fat, fatty acid intakes and colorectal cancer risk in Chinese adults: a case-control study. Eur J Cancer Prev 22, 438–447.CrossRefGoogle ScholarPubMed
Song, M, Chan, AT, Fuchs, CS, et al. (2014) Dietary intake of fish, ω-3 and ω-6 fatty acids and risk of colorectal cancer: a prospective study in U.S. men and women. Int J Cancer 135, 2413–2423.CrossRefGoogle ScholarPubMed
Chen, GC, Qin, LQ, Lu, DB, et al. (2015) n-3 polyunsaturated fatty acids intake and risk of colorectal cancer: meta-analysis of prospective studies. Cancer Causes Control 26, 133–141.CrossRefGoogle ScholarPubMed
Shin, A, Cho, S, Sandin, S, et al. (2020) n-3 and -6 fatty acid intake and colorectal cancer risk in Swedish Women’s lifestyle and health cohort. Cancer Res Treat 52, 848–854.CrossRefGoogle Scholar
Goris, AH, Westerterp-Plantenga, MS & Westerterp, KR (2000) Undereating and underrecording of habitual food intake in obese men: selective underreporting of fat intake. Am J Clin Nutr 71, 130–134.CrossRefGoogle ScholarPubMed
Shahidi, F & Ambigaipalan, P (2018) n-3 polyunsaturated fatty acids and their health benefits. Annu Rev Food Sci Technol 9, 345–381.CrossRefGoogle Scholar
Pakiet, A, Kobiela, J, Stepnowski, P, et al. (2019) Changes in lipids composition and metabolism in colorectal cancer: a review. Lipids Health Dis 18, 29.CrossRefGoogle ScholarPubMed
Kojima, M, Wakai, K, Tokudome, S, et al. (2005) Serum levels of polyunsaturated fatty acids and risk of colorectal cancer: a prospective study. Am J Epidemiol 161, 462–471.CrossRefGoogle ScholarPubMed
Hall, MN, Campos, H, Li, H, et al. (2007) Blood levels of long-chain polyunsaturated fatty acids, aspirin, and the risk of colorectal cancer. Cancer Epidemiol Biomarkers Prev 16, 314–321.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Aglago, EK, Huybrechts, I, Murphy, N, et al. (2020) Consumption of fish and long-chain n-3 polyunsaturated fatty acids is associated with reduced risk of colorectal cancer in a large european cohort. Clin Gastroenterol Hepatol 18, 654–666.e656.CrossRefGoogle Scholar
Kuriki, K, Wakai, K, Hirose, K, et al. (2006) Risk of colorectal cancer is linked to erythrocyte compositions of fatty acids as biomarkers for dietary intakes of fish, fat, and fatty acids. Cancer Epidemiol Biomarkers Prev 15, 1791–1798.CrossRefGoogle ScholarPubMed
Butler, LM, Yuan, JM, Huang, JY, et al. (2017) Plasma fatty acids and risk of colon and rectal cancers in the Singapore Chinese Health Study. NPJ Precis Oncol 1, 38.CrossRefGoogle ScholarPubMed
Linseisen, J, Grundmann, N, Zoller, D, et al. (2021) Red blood cell fatty acids and risk of colorectal cancer in the European Prospective Investigation into Cancer and Nutrition (EPIC). Cancer Epidemiol Biomarkers Prev 30, 874–885.CrossRefGoogle ScholarPubMed
Kim, Y & Kim, J (2020) Intake or blood levels of n-3 polyunsaturated fatty acids and risk of colorectal cancer: a systematic review and meta-analysis of prospective studies. Cancer Epidemiol Biomarkers Prev 29, 288–299.CrossRefGoogle ScholarPubMed
Ainsworth, BE, Haskell, WL, Whitt, MC, et al. (2000) Compendium of physical activities: an update of activity codes and MET intensities. Med Sci Sports Exerc 32, S498–S504.CrossRefGoogle ScholarPubMed
Ainsworth, BE, Haskell, WL, Herrmann, SD, et al. (2011) 2011 compendium of physical activities: a second update of codes and MET values. Med Sci Sports Exerc 43, 1575–1581.CrossRefGoogle ScholarPubMed
Zhang, CX & Ho, SC (2009) Validity and reproducibility of a food frequency questionnaire among Chinese women in Guangdong province. Asia Pac J Clin Nutr 18, 240–250.Google ScholarPubMed
Yang, YX, Wang, GY & Pan, XC (2002) China Food Composition Table. Beijing: Peking University Medical Press.Google Scholar
Huang, CY, Abulimiti, A, Zhang, X, et al. (2020) Dietary B vitamin and methionine intakes and risk for colorectal cancer: a case-control study in China. Br J Nutr 123, 1277–1289.CrossRefGoogle ScholarPubMed
Folch, J, Lees, M & Sloane Stanley, GH (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226, 497–509.CrossRefGoogle ScholarPubMed
Willett, WC, Howe, GR & Kushi, LH (1997) Adjustment for total energy intake in epidemiologic studies. Am J Clin Nutr 65, 1220S–1228S; discussion 1229S–1231S.CrossRefGoogle ScholarPubMed
Mika, A, Kobiela, J, Czumaj, A, et al. (2017) Hyper-elongation in colorectal cancer tissue - cerotic acid is a potential novel serum metabolic marker of colorectal malignancies. Cell Physiol Biochem 41, 722–730.CrossRefGoogle ScholarPubMed
Zhu, J, Djukovic, D, Deng, L, et al. (2014) Colorectal cancer detection using targeted serum metabolic profiling. J Proteome Res 13, 4120–4130.CrossRefGoogle ScholarPubMed
Okuno, M, Hamazaki, K, Ogura, T, et al. (2013) Abnormalities in fatty acids in plasma, erythrocytes and adipose tissue in Japanese patients with colorectal cancer. In Vivo 27, 203–210.Google ScholarPubMed
Khankari, NK, Banbury, BL, Borges, MC, et al. (2020) Mendelian randomization of circulating polyunsaturated fatty acids and colorectal cancer risk. Cancer Epidemiol Biomarkers Prev 29, 860–870.CrossRefGoogle ScholarPubMed
Muramatsu, T, Yatsuya, H, Toyoshima, H, et al. (2010) Higher dietary intake of α-linolenic acid is associated with lower insulin resistance in middle-aged Japanese. Prev Med 50, 272–276.CrossRefGoogle ScholarPubMed
Sekikawa, A, Steingrimsdottir, L, Ueshima, H, et al. (2012) Serum levels of marine-derived n-3 fatty acids in Icelanders, Japanese, Koreans, and Americans--a descriptive epidemiologic study. Prostaglandins Leukot Essent Fatty Acids 87, 11–16.CrossRefGoogle ScholarPubMed
Xu, M, Fang, YJ, Chen, YM, et al. (2015) Higher freshwater fish and sea fish intake is inversely associated with colorectal cancer risk among Chinese population: a case-control study. Sci Rep 5, 12976.CrossRefGoogle ScholarPubMed
Black, LJ, Zhao, Y, Peng, YC, et al. (2020) Higher fish consumption and lower risk of central nervous system demyelination. Eur J Clin Nutr 74, 818–824.CrossRefGoogle ScholarPubMed
Anti, M, Armelao, F, Marra, G, et al. (1994) Effects of different doses of fish oil on rectal cell proliferation in patients with sporadic colonic adenomas. Gastroenterology 107, 1709–1718.CrossRefGoogle ScholarPubMed
Reddy, BS (2004) n-3 fatty acids in colorectal cancer prevention. Int J Cancer 112, 1–7.CrossRefGoogle ScholarPubMed
Huang, Q, Wen, J, Chen, G, et al. (2016) n-3 polyunsaturated fatty acids inhibited tumor growth via preventing the decrease of genomic DNA methylation in colorectal cancer rats. Nutr Cancer 68, 113–119.CrossRefGoogle Scholar
Wang, W, Yang, J, Nimiya, Y, et al. (2017) ω-3 polyunsaturated fatty acids and their cytochrome P450-derived metabolites suppress colorectal tumor development in mice. J Nutr Biochem 48, 29–35.CrossRefGoogle ScholarPubMed
Francipane, MG & Lagasse, E (2014) mTOR pathway in colorectal cancer: an update. Oncotarget 5, 49–66.CrossRefGoogle ScholarPubMed
D’Angelo, L, Piazzi, G, Pacilli, A, et al. (2014) A combination of eicosapentaenoic acid-free fatty acid, epigallocatechin-3-gallate and proanthocyanidins has a strong effect on mTOR signaling in colorectal cancer cells. Carcinog 35, 2314–2320.CrossRefGoogle Scholar
Tang, FY, Cho, HJ, Pai, MH, et al. (2009) Concomitant supplementation of lycopene and eicosapentaenoic acid inhibits the proliferation of human colon cancer cells. J Nutr Biochem 20, 426–434.CrossRefGoogle ScholarPubMed
Liu, M, Zhou, L, Zhang, B, et al. (2016) Elevation of n-3/n-6 PUFAs ratio suppresses mTORC1 and prevents colorectal carcinogenesis associated with APC mutation. Oncotarget 7, 76944–76954.CrossRefGoogle ScholarPubMed
Aoki, K, Tamai, Y, Horiike, S, et al. (2003) Colonic polyposis caused by mTOR-mediated chromosomal instability in Apc+/Delta716 Cdx2+/– compound mutant mice. Nat Genet 35, 323–330.CrossRefGoogle ScholarPubMed
Gulhati, P, Cai, Q, Li, J, et al. (2009) Targeted inhibition of mammalian target of rapamycin signaling inhibits tumorigenesis of colorectal cancer. Clin Cancer Res 15, 7207–7216.CrossRefGoogle ScholarPubMed
Roulin, D, Cerantola, Y, Dormond-Meuwly, A, et al. (2010) Targeting mTORC2 inhibits colon cancer cell proliferation in vitro and tumor formation in vivo . Mol Cancer 9, 57.CrossRefGoogle ScholarPubMed
McMichael, AJ & Potter, JD (1980) Reproduction, endogenous and exogenous sex hormones, and colon cancer: a review and hypothesis. J Natl Cancer Inst 65, 1201–1207.Google ScholarPubMed
Tamakoshi, K, Wakai, K, Kojima, M, et al. (2004) A prospective study on the possible association between having children and colon cancer risk: findings from the JACC Study. Cancer Sci 95, 243–247.CrossRefGoogle ScholarPubMed
Burdge, GC & Calder, PC (2005) Conversion of α-linolenic acid to longer-chain polyunsaturated fatty acids in human adults. Reprod Nutr Dev 45, 581–597.CrossRefGoogle ScholarPubMed
Giltay, EJ, Gooren, LJ, Toorians, AW, et al. (2004) Docosahexaenoic acid concentrations are higher in women than in men because of estrogenic effects. Am J Clin Nutr 80, 1167–1174.CrossRefGoogle ScholarPubMed
Burdge, GC, Jones, AE & Wootton, SA (2002) Eicosapentaenoic and docosapentaenoic acids are the principal products of α-linolenic acid metabolism in young men. Br J Nutr 88, 355–363.CrossRefGoogle ScholarPubMed
Burdge, GC & Wootton, SA (2002) Conversion of α-linolenic acid to eicosapentaenoic, docosapentaenoic and docosahexaenoic acids in young women. Br J Nutr 88, 411–420.CrossRefGoogle ScholarPubMed
Salem, N Jr, Wegher, B, Mena, P, et al. (1996) Arachidonic and docosahexaenoic acids are biosynthesized from their 18-carbon precursors in human infants. Proc Natl Acad Sci U S A 93, 49–54.CrossRefGoogle ScholarPubMed
Inoue, M, Tajima, K, Hirose, K, et al. (1995) Subsite-specific risk factors for colorectal cancer: a hospital-based case-control study in Japan. Cancer Causes Control 6, 14–22.CrossRefGoogle ScholarPubMed
Potter, JD (1996) Nutrition and colorectal cancer. Cancer Causes Control 7, 127–146.CrossRefGoogle ScholarPubMed
Arab, L & Akbar, J (2002) Biomarkers and the measurement of fatty acids. Public Health Nutr 5, 865–871.CrossRefGoogle ScholarPubMed
Xu, AG, Jiang, B, Zhong, XH, et al. (2006) The trend of clinical characteristics of colorectal cancer during the past 20 years in Guangdong province. Natl Med J China 86, 272–275.Google ScholarPubMed
Li, ZF, Huang, HY, Shi, JF, et al. (2017) A systematic review of worldwide natural history models of colorectal cancer: classification, transition rate and a recommendation for developing Chinese population-specific model. Chin J Epidemiol 38, 253–260.Google Scholar
Iso, H, Sato, S, Umemura, U, et al. (2002) Linoleic acid, other fatty acids, and the risk of stroke. Stroke 33, 2086–2093.CrossRefGoogle ScholarPubMed
Yanagisawa, N, Shimada, K, Miyazaki, T, et al. (2010) Polyunsaturated fatty acid levels of serum and red blood cells in apparently healthy Japanese subjects living in an urban area. J Atheroscler Thromb 17, 285–294.CrossRefGoogle Scholar
Ritchie, SA, Heath, D, Yamazaki, Y, et al. (2010) Reduction of novel circulating long-chain fatty acids in colorectal cancer patients is independent of tumor burden and correlates with age. BMC Gastroenterol 10, 140.CrossRefGoogle ScholarPubMed