Skip to main content
Top
Published in: Cancer Causes & Control 3/2015

01-03-2015 | Original Paper

Fish consumption and n-3 polyunsaturated fatty acids, and risk of hepatocellular carcinoma: systematic review and meta-analysis

Authors: Min Gao, Kai Sun, Mujie Guo, Hang Gao, Kun Liu, Cuicui Yang, Sheng Li, Ning Liu

Published in: Cancer Causes & Control | Issue 3/2015

Login to get access

Abstract

Purpose

To investigate the association between fish consumption and n-3 polyunsaturated fatty acids (n-3 PUFA) and the risk of hepatocellular carcinoma (HCC).

Methods

We identified eligible studies in MEDLINE and EMBASE up to July 2014 and the reference lists of original studies and review articles on this topic. Summary relative risks (SRR) with their 95 % confidence intervals (CI) were calculated with a random effects model.

Results

Eleven studies (three cohort studies, seven retrospective case–control studies, and one nested case–control study) met eligibility criteria. Ten articles investigated fish consumption, two articles investigated n-3 PUFA, and two articles investigated alpha-linolenic acid (ALA). The current data suggest that fish consumption was associated with 35 % reduction in HCC risk (highest vs. lowest category SRRs = 0.65, 95 % CI 0.51–0.79; test for heterogeneity p = 0.057, I 2 = 44.1 %). n-3 PUFA was associated with 51 % reduction in HCC risk (highest vs. lowest category SRRs = 0.49, 95 % CI 0.19–0.79). However, no significant inverse association was found in ALA (SRRs = 0.70, 95 % CI 0.30–1.10).

Conclusion

Our meta-analysis of observational studies provides evidence that fish consumption and n-3 PUFA has inverse association with the risk of HCC.
Literature
2.
go back to reference Beasley RP (1988) Hepatitis B virus. The major etiology of hepatocellular carcinoma. Cancer 61(10):1942–1956CrossRefPubMed Beasley RP (1988) Hepatitis B virus. The major etiology of hepatocellular carcinoma. Cancer 61(10):1942–1956CrossRefPubMed
3.
go back to reference Shiratori Y, Shiina S, Imamura M, Kato N, Kanai F, Okudaira T, Teratani T, Tohgo G, Toda N, Ohashi M, Et A (1995) Characteristic difference of hepatocellular carcinoma between hepatitis B- and C-viral infection in Japan. Hepatology 22(4 Pt 1):1027–1033CrossRefPubMed Shiratori Y, Shiina S, Imamura M, Kato N, Kanai F, Okudaira T, Teratani T, Tohgo G, Toda N, Ohashi M, Et A (1995) Characteristic difference of hepatocellular carcinoma between hepatitis B- and C-viral infection in Japan. Hepatology 22(4 Pt 1):1027–1033CrossRefPubMed
7.
go back to reference Montella M, Polesel J, La Vecchia C, Dal Maso L, Crispo A, Crovatto M, Casarin P, Izzo F, Tommasi LG, Talamini R, Franceschi S (2007) Coffee and tea consumption and risk of hepatocellular carcinoma in Italy. Int J Cancer 120(7):1555–1559. doi:10.1002/ijc.22509 CrossRefPubMed Montella M, Polesel J, La Vecchia C, Dal Maso L, Crispo A, Crovatto M, Casarin P, Izzo F, Tommasi LG, Talamini R, Franceschi S (2007) Coffee and tea consumption and risk of hepatocellular carcinoma in Italy. Int J Cancer 120(7):1555–1559. doi:10.​1002/​ijc.​22509 CrossRefPubMed
9.
go back to reference Fedirko V, Trichopolou A, Bamia C, Duarte-Salles T, Trepo E, Aleksandrova K, Nothlings U, Lukanova A, Lagiou P, Boffetta P, Trichopoulos D, Katzke VA, Overvad K, Tjonneland A, Hansen L, Boutron-Ruault MC, Fagherazzi G, Bastide N, Panico S, Grioni S, Vineis P, Palli D, Tumino R, Bueno-de-Mesquita HB, Peeters PH, Skeie G, Engeset D, Parr CL, Jakszyn P, Sanchez MJ, Barricarte A, Amiano P, Chirlaque M, Quiros JR, Sund M, Werner M, Sonestedt E, Ericson U, Key TJ, Khaw KT, Ferrari P, Romieu I, Riboli E, Jenab M (2013) Consumption of fish and meats and risk of hepatocellular carcinoma: the European Prospective Investigation into Cancer and Nutrition (EPIC). Ann Oncol 24(8):2166–2173. doi:10.1093/annonc/mdt168 CrossRefPubMedCentralPubMed Fedirko V, Trichopolou A, Bamia C, Duarte-Salles T, Trepo E, Aleksandrova K, Nothlings U, Lukanova A, Lagiou P, Boffetta P, Trichopoulos D, Katzke VA, Overvad K, Tjonneland A, Hansen L, Boutron-Ruault MC, Fagherazzi G, Bastide N, Panico S, Grioni S, Vineis P, Palli D, Tumino R, Bueno-de-Mesquita HB, Peeters PH, Skeie G, Engeset D, Parr CL, Jakszyn P, Sanchez MJ, Barricarte A, Amiano P, Chirlaque M, Quiros JR, Sund M, Werner M, Sonestedt E, Ericson U, Key TJ, Khaw KT, Ferrari P, Romieu I, Riboli E, Jenab M (2013) Consumption of fish and meats and risk of hepatocellular carcinoma: the European Prospective Investigation into Cancer and Nutrition (EPIC). Ann Oncol 24(8):2166–2173. doi:10.​1093/​annonc/​mdt168 CrossRefPubMedCentralPubMed
10.
go back to reference Bettinger D, Schultheiss M, Hennecke N, Panther E, Knuppel E, Blum HE, Thimme R, Spangenberg HC (2013) Selenium levels in patients with hepatitis C virus-related chronic hepatitis, liver cirrhosis, and hepatocellular carcinoma: a pilot study. Hepatology 57(6):2543–2544. doi:10.1002/hep.26142 CrossRefPubMed Bettinger D, Schultheiss M, Hennecke N, Panther E, Knuppel E, Blum HE, Thimme R, Spangenberg HC (2013) Selenium levels in patients with hepatitis C virus-related chronic hepatitis, liver cirrhosis, and hepatocellular carcinoma: a pilot study. Hepatology 57(6):2543–2544. doi:10.​1002/​hep.​26142 CrossRefPubMed
11.
go back to reference Fedirko V, Duarte-Salles T, Bamia C, Trichopoulou A, Aleksandrova K, Trichopoulos D, Trepo E, Tjonneland A, Olsen A, Overvad K, Boutron-Ruault MC, Clavel-Chapelon F, Kvaskoff M, Kuhn T, Lukanova A, Boeing H, Buijsse B, Klinaki E, Tsimakidi C, Naccarati A, Tagliabue G, Panico S, Tumino R, Palli D, Bueno-de-Mesquita HB, Siersema PD, Peters PH, Lund E, Brustad M, Standahl OK, Weiderpass VE, Zamora R, Sanchez MJ, Ardanaz E, Amiano P, Navarro C, Quiros JR, Werner M, Sund M, Lindkvist B, Malm J, Travis RC, Khaw KT, Stepien M, Scalbert A, Romieu I, Lagiou P, Riboli E, Jenab M (2014) Pre-diagnostic circulating vitamin D levels and risk of hepatocellular carcinoma in European populations: a nested case–control study. Hepatology. doi:10.1002/hep.27079 PubMedCentral Fedirko V, Duarte-Salles T, Bamia C, Trichopoulou A, Aleksandrova K, Trichopoulos D, Trepo E, Tjonneland A, Olsen A, Overvad K, Boutron-Ruault MC, Clavel-Chapelon F, Kvaskoff M, Kuhn T, Lukanova A, Boeing H, Buijsse B, Klinaki E, Tsimakidi C, Naccarati A, Tagliabue G, Panico S, Tumino R, Palli D, Bueno-de-Mesquita HB, Siersema PD, Peters PH, Lund E, Brustad M, Standahl OK, Weiderpass VE, Zamora R, Sanchez MJ, Ardanaz E, Amiano P, Navarro C, Quiros JR, Werner M, Sund M, Lindkvist B, Malm J, Travis RC, Khaw KT, Stepien M, Scalbert A, Romieu I, Lagiou P, Riboli E, Jenab M (2014) Pre-diagnostic circulating vitamin D levels and risk of hepatocellular carcinoma in European populations: a nested case–control study. Hepatology. doi:10.​1002/​hep.​27079 PubMedCentral
12.
go back to reference Fernandez E, Chatenoud L, La Vecchia C, Negri E, Franceschi S (1999) Fish consumption and cancer risk. Am J Clin Nutr 70(1):85–90PubMed Fernandez E, Chatenoud L, La Vecchia C, Negri E, Franceschi S (1999) Fish consumption and cancer risk. Am J Clin Nutr 70(1):85–90PubMed
13.
go back to reference Rose DP, Connolly JM (1999) Omega-3 fatty acids as cancer chemopreventive agents. Pharmacol Ther 83(3):217–244CrossRefPubMed Rose DP, Connolly JM (1999) Omega-3 fatty acids as cancer chemopreventive agents. Pharmacol Ther 83(3):217–244CrossRefPubMed
17.
go back to reference 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 346:f3706CrossRefPubMed 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 346:f3706CrossRefPubMed
20.
go back to reference Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D, Moher D, Becker BJ, Sipe TA, Thacker SB (2000) Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis of observational studies in epidemiology (MOOSE) group. JAMA 283(15):2008–2012CrossRefPubMed Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D, Moher D, Becker BJ, Sipe TA, Thacker SB (2000) Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis of observational studies in epidemiology (MOOSE) group. JAMA 283(15):2008–2012CrossRefPubMed
21.
go back to reference La Vecchia C, Negri E, Decarli A, D’Avanzo B, Franceschi S (1988) Risk factors for hepatocellular carcinoma in northern Italy. Int J Cancer 42(6):872–876CrossRefPubMed La Vecchia C, Negri E, Decarli A, D’Avanzo B, Franceschi S (1988) Risk factors for hepatocellular carcinoma in northern Italy. Int J Cancer 42(6):872–876CrossRefPubMed
22.
go back to reference Kurozawa Y, Ogimoto I, Shibata A, Nose T, Yoshimura T, Suzuki H, Sakata R, Fujita Y, Ichikawa S, Iwai N, Fukuda K, Tamakoshi A (2004) Dietary habits and risk of death due to hepatocellular carcinoma in a large scale cohort study in Japan. Univariate analysis of JACC study data. Kurume Med J 51(2):141–149CrossRefPubMed Kurozawa Y, Ogimoto I, Shibata A, Nose T, Yoshimura T, Suzuki H, Sakata R, Fujita Y, Ichikawa S, Iwai N, Fukuda K, Tamakoshi A (2004) Dietary habits and risk of death due to hepatocellular carcinoma in a large scale cohort study in Japan. Univariate analysis of JACC study data. Kurume Med J 51(2):141–149CrossRefPubMed
23.
go back to reference Greenland S (1987) Quantitative methods in the review of epidemiologic literature. Epidemiol Rev 9:1–30PubMed Greenland S (1987) Quantitative methods in the review of epidemiologic literature. Epidemiol Rev 9:1–30PubMed
26.
go back to reference Sterne JA, Egger M (2001) Funnel plots for detecting bias in meta-analysis: guidelines on choice of axis. J Clin Epidemiol 54(10):1046–1055CrossRefPubMed Sterne JA, Egger M (2001) Funnel plots for detecting bias in meta-analysis: guidelines on choice of axis. J Clin Epidemiol 54(10):1046–1055CrossRefPubMed
27.
go back to reference Duval S, Tweedie R (2000) Trim and fill: a simple funnel-plot-based method of testing and adjusting for publication bias in meta-analysis. Biometrics 56(2):455–463CrossRefPubMed Duval S, Tweedie R (2000) Trim and fill: a simple funnel-plot-based method of testing and adjusting for publication bias in meta-analysis. Biometrics 56(2):455–463CrossRefPubMed
28.
go back to reference Lu SN, Lin TM, Chen CJ, Chen JS, Liaw YF, Chang WY, Hsu ST (1988) A case–control study of primary hepatocellular carcinoma in Taiwan. Cancer 62(9):2051–2055CrossRefPubMed Lu SN, Lin TM, Chen CJ, Chen JS, Liaw YF, Chang WY, Hsu ST (1988) A case–control study of primary hepatocellular carcinoma in Taiwan. Cancer 62(9):2051–2055CrossRefPubMed
29.
go back to reference Qiu XQ, Tan SK, Yu HP, Zeng XY, Li LQ, Hu L (2008) Synergistic effect of HBV infection, alcohol and raw fish consumption on oncogenisis of primary hepatic carcinoma. Zhonghua Zhong Liu Za Zhi 30(2):113–115PubMed Qiu XQ, Tan SK, Yu HP, Zeng XY, Li LQ, Hu L (2008) Synergistic effect of HBV infection, alcohol and raw fish consumption on oncogenisis of primary hepatic carcinoma. Zhonghua Zhong Liu Za Zhi 30(2):113–115PubMed
30.
go back to reference Tan SK, Qiu XQ, Yu HP, Zeng XY, Xiao ZM, Hu L (2008) Etiologic fraction and interaction of risk factors for primary hepatic carcinoma in Guangxi, China. Zhonghua Yu Fang Yi Xue Za Zhi 42(3):169–172PubMed Tan SK, Qiu XQ, Yu HP, Zeng XY, Xiao ZM, Hu L (2008) Etiologic fraction and interaction of risk factors for primary hepatic carcinoma in Guangxi, China. Zhonghua Yu Fang Yi Xue Za Zhi 42(3):169–172PubMed
32.
33.
35.
go back to reference Kanazir M, Boricic I, Delic D, Tepavcevic DK, Knezevic A, Jovanovic T, Pekmezovic T (2010) Risk factors for hepatocellular carcinoma: a case–control study in Belgrade (Serbia). Tumori 96(6):911–917PubMed Kanazir M, Boricic I, Delic D, Tepavcevic DK, Knezevic A, Jovanovic T, Pekmezovic T (2010) Risk factors for hepatocellular carcinoma: a case–control study in Belgrade (Serbia). Tumori 96(6):911–917PubMed
36.
go back to reference Polesel J, Talamini R, Montella M, Maso LD, Crovatto M, Parpinel M, Izzo F, Tommasi LG, Serraino D, La Vecchia C, Franceschi S (2007) Nutrients intake and the risk of hepatocellular carcinoma in Italy. Eur J Cancer 43(16):2381–2387. doi:10.1016/j.ejca.2007.07.012 CrossRefPubMed Polesel J, Talamini R, Montella M, Maso LD, Crovatto M, Parpinel M, Izzo F, Tommasi LG, Serraino D, La Vecchia C, Franceschi S (2007) Nutrients intake and the risk of hepatocellular carcinoma in Italy. Eur J Cancer 43(16):2381–2387. doi:10.​1016/​j.​ejca.​2007.​07.​012 CrossRefPubMed
37.
go back to reference Talamini R, Polesel J, Montella M, Dal Maso L, Crispo A, Tommasi LG, Izzo F, Crovatto M, La Vecchia C, Franceschi S (2006) Food groups and risk of hepatocellular carcinoma: a multicenter case–control study in Italy. Int J Cancer 119(12):2916–2921. doi:10.1002/ijc.22267 CrossRefPubMed Talamini R, Polesel J, Montella M, Dal Maso L, Crispo A, Tommasi LG, Izzo F, Crovatto M, La Vecchia C, Franceschi S (2006) Food groups and risk of hepatocellular carcinoma: a multicenter case–control study in Italy. Int J Cancer 119(12):2916–2921. doi:10.​1002/​ijc.​22267 CrossRefPubMed
38.
go back to reference Yu SZ, Huang XE, Koide T, Cheng G, Chen GC, Harada K, Ueno Y, Sueoka E, Oda H, Tashiro F, Mizokami M, Ohno T, Xiang J, Tokudome S (2002) Hepatitis B and C viruses infection, lifestyle and genetic polymorphisms as risk factors for hepatocellular carcinoma in Haimen, China. Jpn J Cancer Res 93(12):1287–1292CrossRefPubMed Yu SZ, Huang XE, Koide T, Cheng G, Chen GC, Harada K, Ueno Y, Sueoka E, Oda H, Tashiro F, Mizokami M, Ohno T, Xiang J, Tokudome S (2002) Hepatitis B and C viruses infection, lifestyle and genetic polymorphisms as risk factors for hepatocellular carcinoma in Haimen, China. Jpn J Cancer Res 93(12):1287–1292CrossRefPubMed
39.
go back to reference Metwally NS, Kholeif TE, Ghanem KZ, Farrag AR, Ammar NM, Abdel-Hamid AH (2011) The protective effects of fish oil and artichoke on hepatocellular carcinoma in rats. Eur Rev Med Pharmacol Sci 15(12):1429–1444PubMed Metwally NS, Kholeif TE, Ghanem KZ, Farrag AR, Ammar NM, Abdel-Hamid AH (2011) The protective effects of fish oil and artichoke on hepatocellular carcinoma in rats. Eur Rev Med Pharmacol Sci 15(12):1429–1444PubMed
40.
go back to reference Larsson SC, Kumlin M, Ingelman-Sundberg M, Wolk A (2004) Dietary long-chain n-3 fatty acids for the prevention of cancer: a review of potential mechanisms. Am J Clin Nutr 79(6):935–945PubMed Larsson SC, Kumlin M, Ingelman-Sundberg M, Wolk A (2004) Dietary long-chain n-3 fatty acids for the prevention of cancer: a review of potential mechanisms. Am J Clin Nutr 79(6):935–945PubMed
41.
go back to reference Sanzo JM, Dorronsoro M, Amiano P, Amurrio A, Aguinagalde FX, Azpiri MA (2001) Estimation and validation of mercury intake associated with fish consumption in an EPIC cohort of Spain. Public Health Nutr 4(5):981–988CrossRefPubMed Sanzo JM, Dorronsoro M, Amiano P, Amurrio A, Aguinagalde FX, Azpiri MA (2001) Estimation and validation of mercury intake associated with fish consumption in an EPIC cohort of Spain. Public Health Nutr 4(5):981–988CrossRefPubMed
42.
go back to reference Sjodin A, Hagmar L, Klasson-Wehler E, Bjork J, Bergman A (2000) Influence of the consumption of fatty baltic sea fish on plasma levels of halogenated environmental contaminants in Latvian and Swedish men. Environ Health Perspect 108(11):1035–1041CrossRefPubMedCentralPubMed Sjodin A, Hagmar L, Klasson-Wehler E, Bjork J, Bergman A (2000) Influence of the consumption of fatty baltic sea fish on plasma levels of halogenated environmental contaminants in Latvian and Swedish men. Environ Health Perspect 108(11):1035–1041CrossRefPubMedCentralPubMed
43.
go back to reference Rojas E, Herrera LA, Poirier LA, Ostrosky-Wegman P (1999) Are metals dietary carcinogens? Mutat Res 443(1–2):157–181CrossRefPubMed Rojas E, Herrera LA, Poirier LA, Ostrosky-Wegman P (1999) Are metals dietary carcinogens? Mutat Res 443(1–2):157–181CrossRefPubMed
44.
go back to reference Williams CD, Whitley BM, Hoyo C, Grant DJ, Iraggi JD, Newman KA, Gerber L, Taylor LA, McKeever MG, Freedland SJ (2011) A high ratio of dietary n-6/n-3 polyunsaturated fatty acids is associated with increased risk of prostate cancer. Nutr Res 31(1):1–8. doi:10.1016/j.nutres.2011.01.002 CrossRefPubMed Williams CD, Whitley BM, Hoyo C, Grant DJ, Iraggi JD, Newman KA, Gerber L, Taylor LA, McKeever MG, Freedland SJ (2011) A high ratio of dietary n-6/n-3 polyunsaturated fatty acids is associated with increased risk of prostate cancer. Nutr Res 31(1):1–8. doi:10.​1016/​j.​nutres.​2011.​01.​002 CrossRefPubMed
Metadata
Title
Fish consumption and n-3 polyunsaturated fatty acids, and risk of hepatocellular carcinoma: systematic review and meta-analysis
Authors
Min Gao
Kai Sun
Mujie Guo
Hang Gao
Kun Liu
Cuicui Yang
Sheng Li
Ning Liu
Publication date
01-03-2015
Publisher
Springer International Publishing
Published in
Cancer Causes & Control / Issue 3/2015
Print ISSN: 0957-5243
Electronic ISSN: 1573-7225
DOI
https://doi.org/10.1007/s10552-014-0512-1

Other articles of this Issue 3/2015

Cancer Causes & Control 3/2015 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine