Abstract
Purpose
Evidence suggests that fish-derived omega-3 polyunsaturated fatty acids inhibit cancer promotion and progression. On the other hand, fish may contain endocrine-disrupting and potentially carcinogenic environmental contaminants. Our objective was to describe cancer incidence among the Finnish professional fishermen and their wives who are presumed to eat a lot of fish, partly from the contaminated Baltic Sea. Additionally, we wanted to see whether occupational characteristics are reflected in the fishermen’s cancer pattern.
Methods
All Finnish fishermen during 1980–2002 were identified from the Professional Fishermen Register (n = 6,410) and their wives from the National Population Information System (n = 4,260). The cohort was linked with the Finnish Cancer Registry data until 2011, and the standardized incidence ratios (SIR) were calculated based on national incidence rates.
Results
The total cancer incidence among the fishermen and their wives was the same as in the Finnish general population. Among the fishermen, the incidence was increased for lip (SIR 2.17, 95 % confidence interval 1.26–3.47) and testis (2.51, 1.15–4.75) and decreased for colon (0.72, 0.52–0.98) cancers.
Conclusions
We cannot exclude the possibility that the observed excess in testis cancer among the fishermen could reflect life-long high exposure to environmental contaminants. An excess in lip cancer has been repeatedly observed among outdoor workers due to high exposure to ultraviolet radiation, whereas high physical activity during fishing is the most likely explanation for the deficit in colon cancer.
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References
Stephenson JA, Al-Taan O, Arshad A, Morgan B, Metcalfe MS, Dennison AR (2013) The multifaceted effects of omega-3 polyunsaturated Fatty acids on the hallmarks of cancer. J Lipids 2013:261247
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):935–945
Wendel M, Heller AR (2009) Anticancer actions of omega-3 fatty acids-current state and future perspectives. Anti-Cancer Agents Med Chem 9(4):457–470
Spencer L, Mann C, Metcalfe M, Webb M, Pollard C, Spencer D, Berry D, Steward W, Dennison A (2009) The effect of omega-3 FAs on tumour angiogenesis and their therapeutic potential. Eur J Cancer 45(12):2077–2086
MacLean CH, Newberry SJ, Mojica WA, Khanna P, Issa AM, Suttorp MJ, Lim YW, Traina SB, Hilton L, Garland R, Morton SC (2006) Effects of omega-3 fatty acids on cancer risk: a systematic review. JAMA 295(4):403–415
Gerber M (2012) Omega-3 fatty acids and cancers: a systematic update review of epidemiological studies. Br J Nutr 107(Suppl 2):S228–S239
Gerber M (2009) Background review paper on total fat, fatty acid intake and cancers. Ann Nutr Metab 55(1–3):140–161
Calvo MS, Whiting SJ, Barton CN (2005) Vitamin D intake: a global perspective of current status. J Nutr 135(2):310–316
Garland CF, Garland FC, Gorham ED, Lipkin M, Newmark H, Mohr SB, Holick MF (2006) The role of vitamin D in cancer prevention. Am J Public Health 96(2):252–261
Dyck MC, Ma DW, Meckling KA (2011) The anticancer effects of vitamin D and omega-3 PUFAs in combination via cod-liver oil: one plus one may equal more than two. Med Hypotheses 77(3):326–332
International Agency for Research on Cancer (1997) Polychlorinated dibenzo-p-dioxins and polychlorinated dibenzofurans. IARC Monographs on the evaluation of carcinogenic risks to humans, vol 69
Tuomisto J, Vartiainen T, Tuomisto JT (1999) Synopsis on dioxins and PCBs. National Public Health Institute, Kuopio
Lauby-Secretan B, Loomis D, Grosse Y, El Ghissassi F, Bouvard V, Benbrahim-Tallaa L, Guha N, Baan R, Mattock H, Straif K (2013) Carcinogenicity of polychlorinated biphenyls and polybrominated biphenyls. Lancet Oncol 14(4):287–288
Clapp RW, Jacobs MM, Loechler EL (2008) Environmental and occupational causes of cancer: new evidence 2005–2007. Rev Environ Health 23(1):1–37
Ross G (2004) The public health implications of polychlorinated biphenyls (PCBs) in the environment. Ecotoxicol Environ Saf 59(3):275–291
Cole P, Trichopoulos D, Pastides H, Starr T, Mandel JS (2003) Dioxin and cancer: a critical review. Regul Toxicol Pharmacol 38(3):378–388
Boffetta P, Mundt KA, Adami HO, Cole P, Mandel JS (2011) TCDD and cancer: a critical review of epidemiologic studies. Crit Rev Toxicol 41(7):622–636
Golden R, Kimbrough R (2009) Weight of evidence evaluation of potential human cancer risks from exposure to polychlorinated biphenyls: an update based on studies published since 2003. Crit Rev Toxicol 39(4):299–331
Turunen AW, Verkasalo PK, Kiviranta H, Pukkala E, Jula A, Männistö S, Rasanen R, Marniemi J, Vartiainen T (2008) Mortality in a cohort with high fish consumption. Int J Epidemiol 37(5):1008–1017
Turunen AW, Männistö S, Suominen AL, Tiittanen P, Verkasalo PK (2011) Fish consumption in relation to other foods in the diet. Br J Nutr 10(106):1570–1580
Pesatori AC, Consonni D, Rubagotti M, Grillo P, Bertazzi PA (2009) Cancer incidence in the population exposed to dioxin after the “Seveso accident”: twenty years of follow-up. Environ Health 8:39–49
International Agency for Research on Cancer (2012) Radiation. IARC Monogr Eval Carcinog Risks Hum 100:7–303
Boyle T, Keegel T, Bull F, Heyworth J, Fritschi L (2012) Physical activity and risks of proximal and distal colon cancers: a systematic review and meta-analysis. J Natl Cancer Inst 104(20):1548–1561
Teppo L, Pukkala E, Lehtonen M (1994) Data quality and quality control of a population-based cancer registry: experience in Finland. Acta Oncol 33(4):365–369
Pukkala E (2011) Biobanks and registers in epidemiological research on cancer. In: Dillner J (ed) Methods in biobanking. Methods in molecular biology, vol 675. Totowa, Humana Press, pp 127–164
Pukkala E, Martinsen JI, Lynge E, Gunnarsdottir HK, Sparen P, Tryggvadottir L, Weiderpass E, Kjaerheim K (2009) Occupation and cancer - follow-up of 15 million people in five Nordic countries. Acta Oncol 48(5):646–790
Mikoczy Z, Rylander L (2009) Mortality and cancer incidence in cohorts of Swedish fishermen and fishermen’s wives: updated findings. Chemosphere 74(7):938–943
Moore S, Johnson N, Pierce A, Wilson D (1999) The epidemiology of lip cancer: a review of global incidence and aetiology. Oral Dis 5(3):185–195
Laakkonen A, Pukkala E (2008) Cancer incidence among Finnish farmers, 1995–2005. Scand J Work Environ Health 34(1):73–79
Garner MJ, Turner MC, Ghadirian P, Krewski D (2005) Epidemiology of testicular cancer: an overview. Int J Cancer 116(3):331–339
Jorgensen N, Vierula M, Jacobsen R, Pukkala E, Perheentupa A, Virtanen HE, Skakkebaek NE, Toppari J (2011) Recent adverse trends in semen quality and testis cancer incidence among Finnish men. Int J Androl 34(4pt2):e37–e48
Bray F, Richiardi L, Ekbom A, Pukkala E, Cuninkova M, Moller H (2006) Trends in testicular cancer incidence and mortality in 22 European countries: continuing increases in incidence and declines in mortality. Int J Cancer 118(12):3099–3111
McGlynn KA, Trabert B (2012) Adolescent and adult risk factors for testicular cancer. Nat Rev Urol 9(6):339–349
Hardell L, Bavel B, Lindstrom G, Eriksson M, Carlberg M (2006) In utero exposure to persistent organic pollutants in relation to testicular cancer risk. Int J Androl 29(1):228–234
Purdue MP, Engel LS, Langseth H, Needham LL, Andersen A, Barr DB, Blair A, Rothman N, McGlynn KA (2009) Prediagnostic serum concentrations of organochlorine compounds and risk of testicular germ cell tumors. Environ Health Perspect 117(10):1514–1519
Cook MB, Akre O, Forman D, Madigan MP, Richiardi L, McGlynn KA (2010) A systematic review and meta-analysis of perinatal variables in relation to the risk of testicular cancer–experiences of the son. Int J Epidemiol 39(6):1605–1618
Cook MB, Trabert B, McGlynn KA (2011) Organochlorine compounds and testicular dysgenesis syndrome: human data. Int J Androl 34(4 Pt 2):e68–e84 discussion e84–e65
Virtanen HE, Koskenniemi JJ, Sundqvist E, Main KM, Kiviranta H, Tuomisto JT, Tuomisto J, Viluksela M, Vartiainen T, Skakkebaek NE, Toppari J (2012) Associations between congenital cryptorchidism in newborn boys and levels of dioxins and PCBs in placenta. Int J Androl 35(3):283–293
Verta M, Salo S, Korhonen M, Assmuth T, Kiviranta H, Koistinen J, Ruokojarvi P, Isosaari P, Bergqvist PA, Tysklind M, Cato I, Vikelsoe J, Larsen MM (2007) Dioxin concentrations in sediments of the Baltic Sea-a survey of existing data. Chemosphere 67(9):1762–1775
Miller A, Hedman JE, Nyberg E, Haglund P, Cousins IT, Wiberg K, Bignert A (2013) Temporal trends in dioxins (polychlorinated dibenzo-p-dioxin and dibenzofurans) and dioxin-like polychlorinated biphenyls in Baltic herring (Clupea harengus). Mar Pollut Bull 73(1):220–230
Geelen A, Schouten JM, Kamphuis C, Stam BE, Burema J, Renkema JM, Bakker EJ, van’t Veer P, Kampman E (2007) Fish consumption, n-3 fatty acids, and colorectal cancer: a meta-analysis of prospective cohort studies. Am J Epidemiol 166(10):1116–1125
Wu S, Feng B, Li K, Zhu X, Liang S, Liu X, Han S, Wang B, Wu K, Miao D, Liang J, Fan D (2012) Fish consumption and colorectal cancer risk in humans: a systematic review and meta-analysis. Am J Med 125(6):551 e555–559 e555
Tavani A, Franceschi S, Levi F, La Vecchia C (2005) Fish, omega-3 polyunsaturated fat intake and cancer at selected sites. World Rev Nutr Diet 94:166–175
Sasazuki S, Inoue M, Iwasaki M, Sawada N, Shimazu T, Yamaji T, Takachi R, Tsugane S (2011) Intake of n-3 and n-6 polyunsaturated fatty acids and development of colorectal cancer by subsite: Japan Public Health Center-based prospective study. Int J Cancer 129(7):1718–1729
Gonzalez CA, Riboli E (2010) Diet and cancer prevention: contributions from the European Prospective Investigation into cancer and nutrition (EPIC) study. Eur J Cancer 46(14):2555–2562
Sala-Vila A, Calder PC (2011) Update on the relationship of fish intake with prostate, breast, and colorectal cancers. Crit Rev Food Sci Nutr 51(9):855–871
Lund EK, Belshaw NJ, Elliott GO, Johnson IT (2011) Recent advances in understanding the role of diet and obesity in the development of colorectal cancer. Proc Nutr Soc 70(2):194–204
Turunen AW, Jula A, Suominen AL, Mannisto S, Marniemi J, Kiviranta H, Tiittanen P, Karanko H, Moilanen L, Nieminen MS, Kesaniemi YA, Kahonen M, Verkasalo PK (2013) Fish consumption, omega-3 fatty acids, and environmental contaminants in relation to low-grade inflammation and early atherosclerosis. Environ Res 120:43–54
Schwartz GG (1997) Multiple myeloma: clusters, clues, and dioxins. Cancer Epidemiol Biomark Prev 6(1):49–56
Jona A, Szodoray P, Illes A (2013) Immunologic pathomechanism of Hodgkin’s lymphoma. Exp Hematol 41(12):995–1004
Hennessy BT, Hanrahan EO, Daly PA (2004) Non-Hodgkin lymphoma: an update. Lancet Oncol 5(6):341–353
Freeman MD, Kohles SS (2012) Plasma levels of polychlorinated biphenyls, non-Hodgkin lymphoma, and causation. J Environ Public Health 2012:258981
Kramer S, Hikel SM, Adams K, Hinds D, Moon K (2012) Current status of the epidemiologic evidence linking polychlorinated biphenyls and non-hodgkin lymphoma, and the role of immune dysregulation. Environ Health Perspect 120(8):1067–1075
Sawada N, Inoue M, Iwasaki M, Sasazuki S, Shimazu T, Yamaji T, Takachi R, Tanaka Y, Mizokami M, Tsugane S (2012) Consumption of n-3 fatty acids and fish reduces risk of hepatocellular carcinoma. Gastroenterology 142(7):1468–1475
Pilkington SM, Watson RE, Nicolaou A, Rhodes LE (2011) Omega-3 polyunsaturated fatty acids: photoprotective macronutrients. Exp Dermatol 20(7):537–543
Friedrichs W, Ruparel SB, Marciniak RA, deGraffenried L (2011) Omega-3 fatty acid inhibition of prostate cancer progression to hormone independence is associated with suppression of mTOR signaling and androgen receptor expression. Nutr Cancer 63(5):771–777
Signori C, El-Bayoumy K, Russo J, Thompson HJ, Richie JP, Hartman TJ, Manni A (2011) Chemoprevention of breast cancer by fish oil in preclinical models: trials and tribulations. Cancer Res 71(19):6091–6096
Corsetto PA, Montorfano G, Zava S, Jovenitti IE, Cremona A, Berra B, Rizzo AM (2011) Effects of n-3 PUFAs on breast cancer cells through their incorporation in plasma membrane. Lipids Health Dis 10:73
Torfadottir JE, Valdimarsdottir UA, Mucci LA, Kasperzyk JL, Fall K, Tryggvadottir L, Aspelund T, Olafsson O, Harris TB, Jonsson E, Tulinius H, Gudnason V, Adami HO, Stampfer M, Steingrimsdottir L (2013) Consumption of fish products across the lifespan and prostate cancer risk. PloS One 8(4):e59799
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
Heinze VM, Actis AB (2012) Dietary conjugated linoleic acid and long-chain n-3 fatty acids in mammary and prostate cancer protection: a review. Int J Food Sci Nutr 63(1):66–78
Chua ME, Sio MC, Sorongon MC, Dy JS (2012) Relationship of dietary intake of omega-3 and omega-6 Fatty acids with risk of prostate cancer development: a meta-analysis of prospective studies and review of literature. Prostate Cancer 2012:826254
Szymanski KM, Wheeler DC, Mucci LA (2010) Fish consumption and prostate cancer risk: a review and meta-analysis. Am J Clin Nutr 92(5):1223–1233
Acknowledgments
The authors would like to thank Mr. Jan Ivar Martinsen from the Cancer Registry of Norway for re-calculating the results for the NOCCA study. This work was financially supported by the Academy of Finland [Grant Numbers 77008, 205324, 206950, and 124286], the Finnish Cancer Organisations, the Yrjö Jahnsson Foundation, and the Juho Vainio Foundation.
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The authors declare that they have no conflict of interest.
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Turunen, A.W., Suominen, A.L., Kiviranta, H. et al. Cancer incidence in a cohort with high fish consumption. Cancer Causes Control 25, 1595–1602 (2014). https://doi.org/10.1007/s10552-014-0464-5
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DOI: https://doi.org/10.1007/s10552-014-0464-5