IJE Advance Access originally published online on June 25, 2008
International Journal of Epidemiology 2008 37(5):1008-1017; doi:10.1093/ije/dyn117
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Mortality in a cohort with high fish consumption
1 National Public Health Institute, Department of Environmental Health, Kuopio, Finland.
2 Finnish Cancer Registry, Institute for Statistical and Epidemiological Cancer Research, Helsinki, Finland.
3 National Public Health Institute, Department of Health and Functional Capacity, Turku, Finland.
4 National Public Health Institute, Department of Health Promotion and Chronic Disease Prevention, Helsinki, Finland.
5 Department of Environmental Sciences, University of Kuopio, Kuopio, Finland.
* Corresponding author. National Public Health Institute, Department of Environmental Health, PO Box 95, FI-70701 Kuopio, Finland. E-mail: anu.turunen{at}ktl.fi
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Abstract |
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Background Our aim was to assess the mortality of fishermen and fishermen's wives in Finland, presuming that the mortality reflects their high consumption of contaminated fish.
Methods All Finnish fishermen, registered since 1980, were identified from the Professional Fishermen Register (N = 6410), and the fishermen's wives from the national population register (N = 4260). The cohorts were individually linked with cause-of-death data until 2005 at Statistics Finland. The follow-up started in the year after the first registration as a fisherman and at marriage (if later) for the wives. The standardized mortality ratios (SMRs) were calculated based on the national mortality rates. In addition, blood samples and food frequency questionnaire data were collected from a volunteer sample.
Results The average fish consumption and serum concentrations of fish-derived fatty acids and environmental contaminants were higher among the fishermen and their wives than among the general population from the same region. The fishermen and their wives had lower mortality from all causes (SMR 0.78, 95% confidence interval (CI) 0.73–0.82, and 0.84, 0.76–0.93, respectively), and ischaemic heart diseases (0.73, 0.65–0.81, and 0.65, 0.50–0.83) than the general population. Mortality from cerebrovascular diseases and malignant neoplasms was decreased among the fishermen (0.67, 0.52–0.85, and 0.90, 0.80–1.01), but not among the wives. In addition, the fishermen's mortality from water transport accidents was extremely high (8.31, 5.65–11.79).
Conclusions The fishermen and their wives had lower mortality from many natural causes. The high intakes of environmental contaminants in fish were not seen as excess mortality.
Keywords Mortality, causes of death, diseases, accidents, dietary fish, omega-3 fatty acids, dioxins, polychlorinated biphenyls
Accepted 19 May 2008
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Introduction |
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Dietary fish contains beneficial nutritional compounds, such as long-chain polyunsaturated fatty acids (omega-3 PUFAs), and vitamin D. High fish consumption and high omega-3 PUFA intake may protect against fatal coronary heart disease,1,2 ischaemic stroke3,4 and certain cancers.5–11 Conversely, fish may also contain various persistent environmental contaminants, for instance polychlorinated dibenzo-p-dioxins and dibenzofurans (PCDD/Fs, called dioxins in this work), and polychlorinated biphenyls (PCBs). The most toxic dioxin congener, 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) is carcinogenic12 and may also have harmful effects on the cardiovascular system.13
In northern Europe, the Baltic Sea area is heavily contaminated with persistent organic pollutants.14 For example, big Baltic herring and wild salmon often exceed the maximum level of World Health Organisation (WHO) toxic equivalent quantity (8 pg WHOPCDD/F-PCBTEQ per gram fresh weight).15 In our previous study, Finnish Baltic Sea fishermen had at least 2-fold serum concentrations of dioxins and PCBs than the general male population.16,17 These concentrations were comparable to those found in Seveso, Italy, after the industrial accident,18 and considerably higher than for example, concentrations among the Canadian Inuit19 or the frequent fish consumers in the Great Lakes area in the United States.20
Previous epidemiological data on the health behaviour of Finnish professional fishermen are scarce. Based on high serum concentrations of persistent organic pollutants, we presumed that high fish consumption is an important characteristic of Finnish fishermen's diet.16,17 Regarding fishermen's health, mortality from occupational accidents is presumed to be high, but less is known about mortality from natural causes (disease mortality), which reflects both life habits and work-related exposures. This study aims to assess cause-specific mortality in a cohort of Finnish professional fishermen and their wives.
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Materials
Mortality study
In this longitudinal study, the cohort consisted of Finnish professional fishermen (N = 6410) and their wives (N = 4260). The fishermen were identified from the Professional Fishermen Register,21 which was maintained by the Finnish Game and Fisheries Research Institute under the Ministry of Agriculture and Forestry from the early 1980s to 1995. The regional Employment and Economic Development Centres (TE-Centres) have kept the register since 1995, when Finland joined the European Union (EU). The Professional Fishermen Register automatically includes all fishermen, who own a fishing vessel. In addition, all fishermen are obligated to notify the agricultural industry district (regional TE-Centre) before taking up fishing activities. All maritime and freshwater area fishermen who had entered the register at least once between 1980 and 2002 were included in the study cohort.
A fisherman's wife was defined as a woman married to a fisherman at the time of the registration of the fisherman, or later. The wives were identified from the Population Information System of the Population Register Centre (for more information, see http://www.vaestorekisterikeskus.fi/vrk/home.nsf/www/populationinformationsystem). Spouses cohabiting without marriage could not be identified from the population register.
The cohort was linked with Statistics Finland's national cause-of-death data22 from 1980 to 2005 by unique personal identity codes (for more information, see http://www.stat.fi/til/ksyyt/index_en). To enable easy production of time series over the years, Statistics Finland transfers the original cause-of-death codes to a standard 54-category list of causes of death. This list was used in the present study.
Fish consumption and life habit study
In the mortality study, we did not have data on life habits. Therefore, we conducted a cross-sectional sub-sample study. We first drew a national sample of 4487 fishermen, their wives and other family members from the registers to conduct a health questionnaire study. From 1429 respondents, 309 volunteers living at the southern and south-western sea coast of Finland (Helsinki and Turku regions) attended a health examination between August 2004 and May 2005. Of those, 88 were fishermen and 94 were fishermen's wives, aged 45–74 years (the Fishermen study). For comparison, we used data from the population-based Health 2000 health examination survey23 (n = 6986). The study subjects from the supplemental study on cardiovascular disease and diabetes (n = 1526), conducted between October 2001 and December 2002, represented the regional general Finnish population. Data were available from 313 males and 361 females, aged 45–74 years, from Helsinki and Turku regions (the Health 2000 survey).
The health examination protocols were similar in the Fishermen study and in the Health 2000 survey. Diet was assessed by a validated self-administered semi-quantitative 128-item food frequency questionnaire (FFQ) designed to cover the diet over the preceding 12 months.24 Dietary data were processed in the Fineli® Finnish Food Composition Database.25 During the health examinations, fasting blood samples were collected to analyse serum concentrations of nutrients and environmental contaminants, and anthropometric measures were taken to assess body composition. Serum total fatty acid composition was analysed using gas chromatography (capillary column, flame ionization detector),26 and the concentration of 25-hydroxy-derivative of vitamin D (25-hydroxy-cholecalciferol) was analysed by radioimmunoassay. A high resolution mass spectrometer equipped with a gas chromatograph was used to analyse 17 dioxin and 37 PCB congeners from serum.16 The analyses were performed at the National Public Health Institute's accredited testing laboratory in Turku and Kuopio (Code T077, EN ISO/IEC 17025).
To analyse environmental contaminants, serum samples were not available from the Health 2000 survey. Therefore, results from the National Public Health Institute's case-control study on soft tissue sarcoma,27 conducted from 1997 to 1999, were used instead. In this work, we re-calculated the concentrations of dioxins and PCBs analysed from adipose tissue for 47 male and 41 female controls (appendicitis patients), aged 45–74 years, living at the southern and south-western sea coast of Finland (the Sarcoma study).28 Adipose tissue concentrations are comparable with those measured from serum fat.29
Statistical analyses
In the mortality study, calculation of person-years started at the beginning of the year after the first registration (any year between 1981 and 2002) to the Professional Fishermen Register for the fishermen, and at marriage (if later) for the wives. The follow-up ended at death, at emigration, or on December 31, 2005, whichever came first. The observed numbers of deaths and person-years at risk were calculated separately by gender and 5-year age group for four calendar periods (1980–86, 1987–93, 1994–99 and 2000–05). The expected numbers of deaths were calculated by multiplying the number of person-years in each stratum by the corresponding national mortality rate during the period of observation. The standardized mortality ratios (SMRs) were calculated as the ratio of the observed to the expected deaths with 95% confidence interval (CI) based on the Poisson distribution for observed deaths. After considering the annual SMRs, the first 3 years of the follow-up were excluded from the analysis to eliminate the healthy population selection effect.30 On the grounds of biological and epidemiological evidence, the most relevant causes of death were chosen for closer review from the 54-category list.
In the fish consumption and life habit study, means for fish consumption, intakes of fish-derived omega-3 PUFAs (g/day, age- and energy-adjusted), alcohol intake (percentage of total daily energy intake, age-adjusted), and serum concentrations of two omega-3 PUFAs (i.e. eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA), percentage of serum fatty acids, age-adjusted), vitamin D (nmol/l, age-adjusted), and toxic equivalent quantities31 for dioxins (WHOPCDD/FTEQ, pg/g fat, age-adjusted) and PCBs (WHOPCB TEQ, pg/g fat, age-adjusted) were calculated separately for men and women. The variables for body mass index (BMI, kg/m2), smoking, frequency of hangovers, and physical activity both on free-time and at work were each divided into three categories. Age-adjusted estimates for prevalence were calculated for BMI (<25, 25–29, 
30 kg/m2), smoking (never smoker, occasional or former smoker, daily smoker), the frequency of hangovers during the last year (no hangovers, 1–6 hangovers, >6 hangovers), physical activity at free-time (exercise 4 times/week, 1–3 times/week, 
3 times/month) and physical activity at work (heavy exertion, moderate exertion, mainly sedentary).
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Mortality study
The study cohort provided
128 000 person-years at follow-up (Table 1). The average follow-up time was 12 years.
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The fishermen had 22% lower all-cause mortality than the general male population (Table 2). There were 27% and 33% deficits in the fishermen's mortality from ischaemic heart diseases and cerebrovascular diseases, respectively. Mortality from all malignant neoplasms was slightly decreased by 10%. The statistically non-significant SMR estimates were <1 for cancers of the colon, rectum and anus, stomach, and larynx, trachea and lung, slightly >1 for cancers of the lymphoid, haematopoietic and related tissue, and close to unity for prostate cancer. Deficits were also observed in other causes of death, such as diabetes (by 57%), dementia and Alzheimer's disease (by 46%), all diseases of the respiratory system (by 42%), alcohol-related diseases and accidental poisonings by alcohol (by 41%) and suicide (by 39%). Mortality from accidents and violence was close to unity. In contrast, the fishermen had 3-fold mortality from drowning and over 8-fold mortality from water transport accidents compared with the general male population.
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The fishermen's wives had 16% lower all-cause mortality and 35% lower ischaemic heart disease mortality than the general female population (Table 2). The SMR estimates for cerebrovascular diseases and all cancers were close to unity. The statistically non-significant SMR estimates were <1 for cancers of the stomach, breast, larynx, trachea and lung, and lymphoid, haematopoietic and related tissue, and >1 for cancers of the colon, and rectum and anus. A 68% deficit was seen in mortality from all diseases of the respiratory system.
Further, the SMR estimates for all causes, ischaemic heart diseases, cerebrovascular diseases and cancers were <1 in almost all age groups (Table 3).
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Fish consumption and life habit study
The fishermen consumed 85% more fish and had 59% higher intake of fish-derived omega-3 PUFAs than males of the Health 2000 survey (Table 4). The serum concentrations of EPA and DHA were 2-fold, and vitamin D concentration was 40% higher among the fishermen. The concentrations of dioxins and PCBs in serum fat were 2-fold among the fishermen compared with those of the Sarcoma study males.
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The fishermen's wives consumed 45% more fish and had 29% higher intake of fish-derived omega-3 PUFAs than females of the Health 2000 survey (Table 4). The serum EPA concentration was 67% higher, DHA concentration was 2-fold, and vitamin D concentration was 30% higher among the fishermen's wives. The concentrations of dioxins and PCBs in serum fat were
20% higher among the fishermen's wives than among the Sarcoma study females.
As compared with the males and females of the Health 2000 survey, the fishermen and their wives had higher prevalence of obesity (BMI 30), lower prevalence of current daily smoking, and lower frequency of hangovers. Alcohol intake as a proportion of total energy intake was slightly higher among the fishermen than among the males of the Health 2000 survey. The prevalence of free-time regular and sufficient physical activity (exercise 4 times/week) was lower, whereas the prevalence of heavy exertion at work was considerably higher among the fishermen than among the Health 2000 males. Among the females of the Fishermen study and the Health 2000 survey, alcohol intake and physical activity both during free-time and work did not differ considerably.
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Discussion |
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In the present study, the fishermen had decreased mortality from all-causes, ischaemic heart diseases, cerebrovascular diseases, cancers, diabetes, dementia and Alzheimer's disease, diseases of the respiratory system, alcohol-related diseases and accidental poisonings by alcohol and suicide compared with the general male population. Further, they had almost 2-fold fish consumption, 1.6-fold fish-derived omega-3 PUFA intake, 1.4-fold serum vitamin D concentration and 2-fold serum EPA, DHA, dioxin and PCB concentrations compared with the males of the general population sub-sample. Similarly, the fishermen's wives had lower mortality from all-causes, ischaemic heart diseases, and respiratory diseases than the general female population. Their fish consumption, omega-3 PUFA intake and serum concentrations of vitamin D, EPA, DHA, dioxins and PCBs were higher than those of the females of the general population sub-sample.
In Finland, administrative registers, such as Population Information System and cause-of-death register, have good coverage and validity,32 and the automated record linkage procedure is based on unique personal identity codes. Although the determination principles of the underlying cause of death may slightly vary by time, region, social class and occupation,33 the variation among the fishermen and their wives is likely to be similar to the variation in the general population. The automatic registration based on fishing vessel register and the notification obligation by law since 1995 have improved the file coverage of the Professional Fishermen Register close to 100%.
The majority of the Finnish fishermen live at the south-western sea coast of Finland, but we do not have regional reference mortality rates for that region and for a comparable time period. We evaluated the magnitude of the potential effect of geographical variation in the mortality by using the Small Area Statistics on Health System.34 In short, we calculated the SMRs (adjusted for socio-economic status) for the population living within 20 km from the Finnish coastline in the year 1980, excluding fishermen and their wives. The size of the population was 0.9 million persons, and it provided 20 million person-years during the follow-up from 1981 to 2005. Mortality was 3% lower from all causes and 7% lower from ischaemic heart diseases among those living at the coastal areas than among the general population of Finland. Cancer mortality did not differ between the coastal areas and the rest of Finland. Hence, the use of regional reference mortality rates would not have changed the SMR estimates notably.
We evaluated the potential for healthy population selection effect30 in our cohort by calculating the SMRs separately for each year from the beginning of the follow-up. The healthy population selection effect was distinctive during the first 3 years of the follow-up, and the annual SMR estimates stabilized to their long-term level after the third year. For example, the SMR estimate for all diseases among the fishermen was 0.39 (0.24–0.60), 0.41 (0.26–0.62) and 0.57 (0.40–0.79) during the first 3 years, and stabilized after the third year at the level around 0.75. Therefore, the first 3 years of the follow-up were excluded from the mortality analyses. In the previous studies on fishermen, the healthy population selection effect has not been actively controlled. It can be speculated that decreased mortality especially among the Canadian35 fishermen is partially explained by the healthy population selection effect.
In the longitudinal mortality study, we did not have data on confounding factors, such as diet, smoking, alcohol consumption and physical activity. Instead, we assessed life habits in small volunteer samples of the study populations. In general, volunteers tend to be more health conscious than the average population, and therefore, the results from the Fishermen study sub-sample may not be fully generalizable to all Finnish fishermen and their wives (and similarly, the results from the Health 2000 survey sub-sample may not be fully generalizable to the general population). However, comparisons between the two similarly selected volunteer samples will at least diminish the bias.
Our results on mortality among the Finnish fishermen and their wives are in line with the reported associations between high fish consumption or high omega-3 PUFA intake and reduced all-cause mortality,2,36 fatal coronary heart disease (summarized in several reviews1,2,37,38), and ischaemic stroke.3,4 In previous studies in cohorts with high fish consumption, a decreased ischaemic heart disease risk has been reported for the Greenland39 and the Alaskan40 Inuit and the residents of a Japanese fishing village.41 Overall, results from five previous fishermen studies are quite inconsistent. Compared with the Finnish fishermen, only the Swedish42 (0.88, 0.78–0.99) and Canadian35 (0.80, 0.76–0.85) fishermen seem to have a similarly decreased mortality from all causes. Regarding diseases of the circulatory system, only the Canadian35 fishermen have decreased mortality from ischaemic heart diseases (0.72, 0.65–0.80) and cerebrovascular diseases (0.67, 0.51–0.86). Among the Swedish42 and Italian43 fishermen, the SMR estimates for diseases of the circulatory system show statistically non-significant decreases. On the contrary, all-cause and ischaemic heart disease mortality is increased among the Danish44 and Icelandic45 fishermen.
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The lack of decrease or increase in cancer mortality can be seen as a reflection of the unclear net effect of fish consumption on cancer risk. For example, fish or omega-3 PUFAs5–11,46 and vitamin D47 are suspected to have a protective effect against cancer, but TCDD is a human carcinogen.12 With regard to the previous studies, only the Swedish42 (0.77, 0.58–1.02) and Canadian35 (0.92, 0.83–1.02) fishermen and Swedish fishermen's wives from the West coast48 (0.96, 0.87–1.06) seem to have similar cancer mortality when compared with the Finnish fishermen and their wives. The Italian,43 Danish44 and Icelandic45 fishermen have increased cancer mortality.
Decreased mortality from diabetes, diseases of the respiratory system and dementia and Alzheimer's disease is in line with the findings that omega-3 PUFAs49 and vitamin D47 may protect against diabetes and/or its fatal complications, and omega-3 PUFAs may protect from inflammatory diseases37 and dementia.50 In the previous studies, diabetes mortality is reported only among the Canadian35 fishermen (0.33, 0.13–0.68), and it is similar when compared to the Finnish fishermen. In the Seveso study, the SMR estimate for diabetes is >1.51 Regarding respiratory diseases, the Canadian35 fishermen seem to have a similarly decreased mortality (0.39, 0.28–0.54) than the Finnish fishermen. The decreased SMR estimate for respiratory diseases among the Italian45 fishermen and the slightly increased SMR estimates among the Danish44 and Icelandic45 fishermen are statistically non-significant.
Extremely high mortality from water transport accidents and drowning among the fishermen was expected due to fishermen's working conditions on fishing vessels. The observed decreased mortality from suicides could be linked with a recent finding suggesting that high intake of omega-3 PUFAs may affect mental health by protecting from depression and other mental disorders.37,38 However, suicides among professional fishermen are likely to be partly misclassified as water transport accidents and drowning. Regarding the previous studies, mortality from occupational accidents is reported only for the Swedish,42 (11.1, 5.33–20.4) Canadian35 (8.50, 6.87–10.4) and Danish44 (4.75, 3.91–5.71) fishermen, and the results are in line with the results of the present study. Suicide mortality is reported only for Canadian,35 and Danish44 fishermen but those 10% decreases are statistically non-significant.
With regard to the Finnish fishermen's life habits, their high fish consumption, relatively low prevalence of daily smoking, low frequency of hangovers and high frequency of physical activity at work are in line with the observed decreases in mortality from many chronic diseases and the absence of increased SMR estimates for cancers. High physical activity at work may partly compensate for the risk caused by high BMI and low prevalence of regular and sufficient free-time physical activity. In addition, BMI may not be a good measure of body composition in a population with heavy physical exertion.
Regarding the comparability of the fishermen studies, the SMR estimates are expected to vary by country due to differences in national characteristics of professional fishing (e.g. type of the vessel, working methods, distance to the shore and work shift hours) and professional fishermen's life habits (e.g. smoking, fish consumption and other dietary habits, alcohol drinking patterns and physical activity). For example, the reported high smoking prevalence among the Italian43 fishermen could explain their increased mortality from many cancers and a slightly increased SMR estimate for all causes. Increased lung cancer mortality among the Danish44 and Icelandic45 fishermen indicates high smoking prevalence which agrees with their increased mortality from the majority of the reported causes. Further, fish consumption may not be as important characteristic of fishermen's diet in other countries as it is in Finland.
The SMR estimates in different countries may also vary depending on how study population and reference population are defined. With regard to the Icelandic study,45 fishermen and sailors are grouped together which makes that study less suitable for comparisons. In the Danish44 study, the general population in labour force is used as a reference population which could be an additional explanation for the increased estimates. Moreover, due to differences in national reference mortality levels, comparisons of mortality patterns should ideally be based on both relative mortality ratios and absolute mortality rates.
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To conclude, the Finnish fishermen and their wives are a population with high fish consumption and high serum concentrations of dioxins and PCBs. In this study, they had lower mortality from all-causes, ischaemic heart diseases, and respiratory diseases than the respective general male and female populations. The fishermen (but not their wives) also had decreased mortality from cerebrovascular diseases, diabetes, dementia and Alzheimer's disease and suicide. The high intakes of environmental contaminants in fish were not seen as excess mortality. It is possible that exposure to environmental contaminants was not high enough to cause excess mortality, or the beneficial health effects of fish consumption (or some other factor) outweighed the potential hazardous health effects.
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Acknowledgements |
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The authors would like to thank the volunteers and the research staff of the Fishermen study, the Health 2000 health examination survey and the Sarcoma study. The authors would also like to thank Kari Pasanen for the calculations using the Small Area Statistics on Health System. This study was funded by the Academy of Finland (project numbers 52876 and 206950), the Finnish Cancer Organisations, the Yrjö Jahnsson Foundation and the Juho Vainio Foundation.
Conflict of interest: None declared.
KEY MESSAGES
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1 Brouwer IA, Geelen A, Katan MB. n-3 Fatty acids, cardiac arrhythmia and fatal coronary heart disease. Prog Lipid Res (2006) 45:357–67.[CrossRef][Web of Science][Medline]
2 Mozaffarian D, Rimm EB. Fish intake, contaminants, and human health: evaluating the risks and the benefits. JAMA (2006) 296:1885–99.
3 He K, Song Y, Daviglus ML, et al. Fish consumption and incidence of stroke: a meta-analysis of cohort studies. Stroke (2004) 35:1538–42.
4 Skerrett PJ, Hennekens CH. Consumption of fish and fish oils and decreased risk of stroke. Prev Cardiol (2003) 6:38–41.[Medline]
5 Caygill CP, Hill MJ. Fish, n-3 fatty acids and human colorectal and breast cancer mortality. Eur J Cancer Prev (1995) 4:329–32.[Web of Science][Medline]
6 Norat T, Bingham S, Ferrari P, et al. Meat, fish, and colorectal cancer risk: the European Prospective Investigation into cancer and nutrition. J Natl Cancer Inst (2005) 97:906–16.
7 Fernandez E, Chatenoud L, La Vecchia C, Negri E, Franceschi S. Fish consumption and cancer risk. Am J Clin Nutr (1999) 70:85–90.
8 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.
9 Augustsson K, Michaud DS, Rimm EB, et al. A prospective study of intake of fish and marine fatty acids and prostate cancer. Cancer Epidemiol Biomarkers Prev (2003) 12:64–67.
10 Leitzmann MF, Stampfer MJ, Michaud DS, et al. Dietary intake of n-3 and n-6 fatty acids and the risk of prostate cancer. Am J Clin Nutr (2004) 80:204–16.
11 Saadatian-Elahi M, Norat T, Goudable J, Riboli E. Biomarkers of dietary fatty acid intake and the risk of breast cancer: a meta-analysis. Int J Cancer (2004) 111:584–91.[CrossRef][Web of Science][Medline]
12 IARC. France: International Agency for Research on Cancer. In: Polychlorinated dibenzo-p-dioxins and polychlorinated dibenzofurans. Monographs on the evaluation of carcinogenic risks to human Lyon (Report No 69). (1997).
13 Pesatori AC, Zocchetti C, Guercilena S, Consonni D, Turrini D, Bertazzi PA. Dioxin exposure and non-malignant health effects: a mortality study. Occup Environ Med (1998) 55:126–31.
14 Hallikainen A, Kiviranta H, Isosaari P, Vartiainen T, Parmanne R, Vuorinen PJ. Concentrations of dioxins, furans, dioxin-like PCB compounds and polybrominated diphenyl ethers in domestic fresh water and salt water fish (Report No 1/2004). (2004) National Food Agency of Finland.
15 Commission Regulation (EC) No 1881/2006 setting maximum levels for certain contaminants in foodstuffs. Official Journal of the European Union.49(L 364).
16 Kiviranta H, Vartiainen T, Tuomisto J. Polychlorinated dibenzo-p-dioxins, dibenzofurans, and biphenyls in fishermen in Finland. Environ Health Perspect (2002) 110:355–61.[Web of Science][Medline]
17 Kiviranta H, Vartiainen T, Verta M, Tuomisto JT, Tuomisto J. High fish-specific dioxin concentrations in Finland. Lancet (2000) 355:1883–85.[Medline]
18 Needham LL, Gerthoux PM, Patterson DG Jr, et al. Serum dioxin levels in Seveso, Italy, population in 1976. Teratog Carcinog Mutagen (1997) 17:225–40.[CrossRef][Web of Science][Medline]
19 Ayotte P, Dewailly E, Ryan JJ, Bruneau S, Lebel G. PCBs and dioxin-like compounds in plasma of adult Inuit living in Nunavik (Arctic Quebec). Chemosphere (1997) 34:1459–68.[Medline]
20 Falk C, Hanrahan L, Anderson HA, et al. Body burden levels of dioxin, furans, and PCBs among frequent consumers of Great Lakes sport fish. The Great Lakes Consortium. Environ Res (1999) 80:S19–25.[Medline]
21 Decision of the Ministry of Agriculture and Forestry on the Registers of the Fishing Industry 1575/1994. Finland: Ministry of Agriculture and Forestry.
22 Causes of death 2004. Statistics Finland. In: Health. (2005) 1.
23 Aromaa A, Koskinen S. Health and functional capacity in Finland. Baseline Results of the Health 2000 Health Examination Survey (Report No B12/2004). (2004) Helsinki: National Public Health Institute.
24 Paalanen L, Mannisto S, Virtanen MJ, et al. Validity of a food frequency questionnaire varied by age and body mass index. J Clin Epidemiol (2006) 59:994–1001.[CrossRef][Web of Science][Medline]
25 Fineli Finnish food composition database. (2007) Helsinki: National Public Health Institute, Nutrition Unit. Available at: http://www.ktl.fi/fineli/.
26 Jula A, Marniemi J, Ronnemaa T, Virtanen A, Huupponen R. Effects of diet and simvastatin on fatty acid composition in hypercholesterolemic men: a randomized controlled trial. Arterioscler Thromb Vasc Biol (2005) 25:1952–59.
27 Tuomisto JT, Pekkanen J, Kiviranta H, Tukiainen E, Vartiainen T, Tuomisto J. Soft-tissue sarcoma and dioxin: a case-control study. Int J Cancer (2004) 108:893–900.[CrossRef][Web of Science][Medline]
28 Kiviranta H, Tuomisto JT, Tuomisto J, Tukiainen E, Vartiainen T. Polychlorinated dibenzo-p-dioxins, dibenzofurans, and biphenyls in the general population in Finland. Chemosphere (2005) 60:854–69.[Medline]
29 Schecter A, Papke O, Ball M, Ryan JJ. Partitioning of dioxins and dibenzofurans – whole-blood, blood-plasma and adipose-tissue. Chemosphere (1991) 23:1913–19.
30 Vinni K, Hakama M. Healthy worker effect in the total Finnish population. Br J Ind Med (1980) 37:180–84.[Web of Science][Medline]
31 Van den Berg M, Birnbaum L, Bosveld AT, et al. Toxic equivalency factors (TEFs) for PCBs, PCDDs, PCDFs for humans and wildlife. Environ Health Perspect (1998) 106:775–92.[Web of Science][Medline]
32 Gissler G, Haukka J. Finnish health and social welfare registers in epidemiological research. Norsk Epidemiologi (2004) 14:113–20.
33 Pukkala E. Cancer risk by social class and occupation. A Survey of 109 000 Cancer Cases among Finns of Working Age (Report No 7). (1995) Contributions to Epidemiology and Biostatistics.
34 Kokki E, Pukkala E, Verkasalo P, Pekkanen J. Small Area Statistics on Health (SMASH): a system for rapid investigations of cancer in Finland. In: GIS for Emergency Preparedness and Health Risk Reduction.—Briggs D, Forer P, Järup L, Stern R, eds. (2002) Dordrecht: Kluwer Academic Publishers. 255–66.
35 Neutel CI. Mortality in commercial fishermen of Atlantic Canada. Can J Public Health (1989) 80:375–79.[Web of Science][Medline]
36 Bucher HC, Hengstler P, Schindler C, Meier G. N-3 polyunsaturated fatty acids in coronary heart disease: a meta-analysis of randomized controlled trials. Am J Med (2002) 112:298–304.[CrossRef][Web of Science][Medline]
37 Ruxton CH, Reed SC, Simpson MJ, Millington KJ. The health benefits of omega-3 polyunsaturated fatty acids: a review of the evidence. J Hum Nutr Diet (2004) 17:449–59.[CrossRef][Web of Science][Medline]
38 Sidhu KS. Health benefits and potential risks related to consumption of fish or fish oil. Regul Toxicol Pharmacol (2003) 38:336–44.[CrossRef][Web of Science][Medline]
39 Kromann N, Green A. Epidemiological studies in the Upernavik district, Greenland. Incidence of some chronic diseases 1950–1974. Acta Med Scand (1980) 208:401–6.[Web of Science][Medline]
40 Davidson M, Bulkow LR, Gellin BG. Cardiac mortality in Alaska's indigenous and non-Native residents. Int J Epidemiol (1993) 22:62–71.
41 Hirai A, Terano T, Tamura Y, Yoshida S. Eicosapentaenoic acid and adult diseases in Japan: epidemiological and clinical aspects. J Intern Med Suppl (1989) 225:69–75.
42 Hagmar L, Linden K, Nilsson A, et al. Cancer incidence and mortality among Swedish Baltic Sea fishermen. Scand J Work Environ Health (1992) 18:217–24.[Web of Science][Medline]
43 Mastrangelo G, Malusa E, Veronese C, Zucchero A, Marzia V, Boscolo Bariga A. Mortality from lung cancer and other diseases related to smoking among fishermen in north east Italy. Occup Environ Med (1995) 52:150–53.
44 Jensen OC. Mortality in Danish fishermen. Bull Inst Marit Trop Med Gdynia (1996) 47:5–10.[Medline]
45 Rafnsson V, Gunnarsdottir H. Mortality among Icelandic seamen. Int J Epidemiol (1994) 23:730–36.
46 Key TJ, Schatzkin A, Willett WC, Allen NE, Spencer EA, Travis RC. Diet, nutrition and the prevention of cancer. Public Health Nutr (2004) 7:187–200.[CrossRef][Web of Science][Medline]
47 Garland CF, Garland FC, Gorham ED, et al. The role of vitamin D in cancer prevention. Am J Public Health (2006) 96:252–61.
48 Rylander L, Hagmar L. Mortality and cancer incidence among women with a high consumption of fatty fish contaminated with persistent organochlorine compounds. Scand J Work Environ Health (1995) 21:419–26.[Web of Science][Medline]
49 Nettleton JA, Katz R. n-3 long-chain polyunsaturated fatty acids in type 2 diabetes: a review. J Am Diet Assoc (2005) 105:428–40.[CrossRef][Web of Science][Medline]
50 Issa AM, Mojica WA, Morton SC, et al. The efficacy of omega-3 fatty acids on cognitive function in aging and dementia: a systematic review. Dement Geriatr Cogn Disord (2006) 21:88–96.[CrossRef][Web of Science][Medline]
51 Bertazzi PA, Consonni D, Bachetti S, et al. Health effects of dioxin exposure: a 20-year mortality study. Am J Epidemiol (2001) 153:1031–44.
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