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Published in: European Journal of Nutrition 2/2017

Open Access 01-03-2017 | Original Contribution

Fish consumption and frying of fish in relation to type 2 diabetes incidence: a prospective cohort study of Swedish men

Authors: Alice Wallin, Daniela Di Giuseppe, Nicola Orsini, Agneta Åkesson, Nita G. Forouhi, Alicja Wolk

Published in: European Journal of Nutrition | Issue 2/2017

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Abstract

Purpose

Epidemiological evidence on the association between fish consumption and risk of type 2 diabetes is heterogeneous across geographical regions. Differences related to fish consumption pattern could possibly help explain the discrepancy between the findings. We therefore aimed to investigate the association between fish consumption (total, fried, specific fish items) and type 2 diabetes incidence, taking exposure to contaminants present in fish (polychlorinated biphenyls and methyl mercury) into consideration.

Methods

The population-based Cohort of Swedish Men, including 35,583 men aged 45–79 years, was followed from 1998 to 2012. We estimated hazard ratios (HRs) with 95 % confidence intervals (CIs) using Cox proportional hazards models.

Results

During 15 years of follow-up, 3624 incident cases were identified. Total fish consumption (≥4 servings/week vs. <1 serving/week) was not associated with type 2 diabetes in multivariable-adjusted analysis (HR 1.00; 95 % CI 0.85–1.18); however, a statistically non-significant inverse association was observed after adjustment for dietary contaminant exposures (HR 0.79; 95 % CI 0.60–1.04). Fried fish (≥6 servings/month vs. ≤1 servings/month) and shellfish consumption (≥1 serving/week vs. never/seldom) were associated with HRs of 1.14 (95 % CI 1.03–1.31) and 1.21 (95 % CI 1.07–1.36), respectively.

Conclusions

We observed no overall association between total fish consumption and type 2 diabetes. The results indicated that dietary contaminants in fish may influence the relationship. Fried fish and shellfish consumption were associated with higher type 2 diabetes incidence. These findings suggest that more specific advice on fish species sub-types (varying in contamination) and preparation methods may be warranted.
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Literature
1.
go back to reference Whiting DR, Guariguata L, Weil C, Shaw J (2011) IDF diabetes atlas: global estimates of the prevalence of diabetes for 2011 and 2030. Diabetes Res Clin Pract 94:311–321CrossRef Whiting DR, Guariguata L, Weil C, Shaw J (2011) IDF diabetes atlas: global estimates of the prevalence of diabetes for 2011 and 2030. Diabetes Res Clin Pract 94:311–321CrossRef
2.
go back to reference He K (2009) Fish, long-chain omega-3 polyunsaturated fatty acids and prevention of cardiovascular disease—Eat fish or take fish oil supplement? Prog Cardiovasc Dis 52:95–114CrossRef He K (2009) Fish, long-chain omega-3 polyunsaturated fatty acids and prevention of cardiovascular disease—Eat fish or take fish oil supplement? Prog Cardiovasc Dis 52:95–114CrossRef
3.
go back to reference Montonen J, Jarvinen R, Heliovaara M, Reunanen A, Aromaa A, Knekt P (2005) Food consumption and the incidence of type II diabetes mellitus. Eur J Clin Nutr 59:441–448CrossRef Montonen J, Jarvinen R, Heliovaara M, Reunanen A, Aromaa A, Knekt P (2005) Food consumption and the incidence of type II diabetes mellitus. Eur J Clin Nutr 59:441–448CrossRef
4.
go back to reference Vang A, Singh PN, Lee JW, Haddad EH, Brinegar CH (2008) Meats, processed meats, obesity, weight gain and occurrence of diabetes among adults: findings from Adventist Health Studies. Ann Nutr Metab 52:96–104CrossRef Vang A, Singh PN, Lee JW, Haddad EH, Brinegar CH (2008) Meats, processed meats, obesity, weight gain and occurrence of diabetes among adults: findings from Adventist Health Studies. Ann Nutr Metab 52:96–104CrossRef
5.
go back to reference Kaushik M, Mozaffarian D, Spiegelman D, Manson JE, Willett WC, Hu FB (2009) Long-chain omega-3 fatty acids, fish intake, and the risk of type 2 diabetes mellitus. Am J Clin Nutr 90:613–620CrossRef Kaushik M, Mozaffarian D, Spiegelman D, Manson JE, Willett WC, Hu FB (2009) Long-chain omega-3 fatty acids, fish intake, and the risk of type 2 diabetes mellitus. Am J Clin Nutr 90:613–620CrossRef
6.
go back to reference Patel PS, Sharp SJ, Luben RN, Khaw KT, Bingham SA, Wareham NJ, Forouhi NG (2009) Association between type of dietary fish and seafood intake and the risk of incident type 2 diabetes: the European prospective investigation of cancer (EPIC)-Norfolk cohort study. Diabetes Care 32:1857–1863CrossRef Patel PS, Sharp SJ, Luben RN, Khaw KT, Bingham SA, Wareham NJ, Forouhi NG (2009) Association between type of dietary fish and seafood intake and the risk of incident type 2 diabetes: the European prospective investigation of cancer (EPIC)-Norfolk cohort study. Diabetes Care 32:1857–1863CrossRef
7.
go back to reference van Woudenbergh GJ, van Ballegooijen AJ, Kuijsten A, Sijbrands EJ, van Rooij FJ, Geleijnse JM, Hofman A, Witteman JC, Feskens EJ (2009) Eating fish and risk of type 2 diabetes: a population-based, prospective follow-up study. Diabetes Care 32:2021–2026CrossRef van Woudenbergh GJ, van Ballegooijen AJ, Kuijsten A, Sijbrands EJ, van Rooij FJ, Geleijnse JM, Hofman A, Witteman JC, Feskens EJ (2009) Eating fish and risk of type 2 diabetes: a population-based, prospective follow-up study. Diabetes Care 32:2021–2026CrossRef
8.
go back to reference Patel PS, Sharp SJ, Jansen E, Luben RN, Khaw KT, Wareham NJ, Forouhi NG (2010) Fatty acids measured in plasma and erythrocyte-membrane phospholipids and derived by food-frequency questionnaire and the risk of new-onset type 2 diabetes: a pilot study in the European Prospective Investigation into Cancer and Nutrition (EPIC)-Norfolk cohort. Am J Clin Nutr 92:1214–1222CrossRef Patel PS, Sharp SJ, Jansen E, Luben RN, Khaw KT, Wareham NJ, Forouhi NG (2010) Fatty acids measured in plasma and erythrocyte-membrane phospholipids and derived by food-frequency questionnaire and the risk of new-onset type 2 diabetes: a pilot study in the European Prospective Investigation into Cancer and Nutrition (EPIC)-Norfolk cohort. Am J Clin Nutr 92:1214–1222CrossRef
9.
go back to reference Brostow DP, Odegaard AO, Koh WP, Duval S, Gross MD, Yuan JM, Pereira MA (2011) Omega-3 fatty acids and incident type 2 diabetes: the Singapore Chinese Health Study. Am J Clin Nutr 94:520–526CrossRef Brostow DP, Odegaard AO, Koh WP, Duval S, Gross MD, Yuan JM, Pereira MA (2011) Omega-3 fatty acids and incident type 2 diabetes: the Singapore Chinese Health Study. Am J Clin Nutr 94:520–526CrossRef
10.
go back to reference Djousse L, Biggs ML, Lemaitre RN, King IB, Song X, Ix JH, Mukamal KJ, Siscovick DS, Mozaffarian D (2011) Plasma omega-3 fatty acids and incident diabetes in older adults. Am J Clin Nutr 94:527–533CrossRef Djousse L, Biggs ML, Lemaitre RN, King IB, Song X, Ix JH, Mukamal KJ, Siscovick DS, Mozaffarian D (2011) Plasma omega-3 fatty acids and incident diabetes in older adults. Am J Clin Nutr 94:527–533CrossRef
11.
go back to reference Djousse L, Gaziano JM, Buring JE, Lee IM (2011) Dietary omega-3 fatty acids and fish consumption and risk of type 2 diabetes. Am J Clin Nutr 93:143–150CrossRef Djousse L, Gaziano JM, Buring JE, Lee IM (2011) Dietary omega-3 fatty acids and fish consumption and risk of type 2 diabetes. Am J Clin Nutr 93:143–150CrossRef
12.
go back to reference Nanri A, Mizoue T, Noda M, Takahashi Y, Matsushita Y, Poudel-Tandukar K, Kato M, Oba S, Inoue M, Tsugane S (2011) Fish intake and type 2 diabetes in Japanese men and women: the Japan Public Health Center-based Prospective Study. Am J Clin Nutr 94:884–891CrossRef Nanri A, Mizoue T, Noda M, Takahashi Y, Matsushita Y, Poudel-Tandukar K, Kato M, Oba S, Inoue M, Tsugane S (2011) Fish intake and type 2 diabetes in Japanese men and women: the Japan Public Health Center-based Prospective Study. Am J Clin Nutr 94:884–891CrossRef
13.
go back to reference Villegas R, Xiang YB, Elasy T, Li HL, Yang G, Cai H, Ye F, Gao YT, Shyr Y, Zheng W, Shu XO (2011) Fish, shellfish, and long-chain n-3 fatty acid consumption and risk of incident type 2 diabetes in middle-aged Chinese men and women. Am J Clin Nutr 94:543–551CrossRef Villegas R, Xiang YB, Elasy T, Li HL, Yang G, Cai H, Ye F, Gao YT, Shyr Y, Zheng W, Shu XO (2011) Fish, shellfish, and long-chain n-3 fatty acid consumption and risk of incident type 2 diabetes in middle-aged Chinese men and women. Am J Clin Nutr 94:543–551CrossRef
14.
go back to reference Rylander C, Sandanger TM, Engeset D, Lund E (2014) Consumption of lean fish reduces the risk of type 2 diabetes mellitus: a prospective population based cohort study of Norwegian women. PLoS ONE 9:e89845CrossRef Rylander C, Sandanger TM, Engeset D, Lund E (2014) Consumption of lean fish reduces the risk of type 2 diabetes mellitus: a prospective population based cohort study of Norwegian women. PLoS ONE 9:e89845CrossRef
15.
go back to reference Virtanen JK, Mursu J, Voutilainen S, Uusitupa M, Tuomainen TP (2014) Serum omega-3 polyunsaturated fatty acids and risk of incident type 2 diabetes in men: the Kuopio Ischaemic Heart Disease Risk Factor study. Diabetes Care 37:189–196CrossRef Virtanen JK, Mursu J, Voutilainen S, Uusitupa M, Tuomainen TP (2014) Serum omega-3 polyunsaturated fatty acids and risk of incident type 2 diabetes in men: the Kuopio Ischaemic Heart Disease Risk Factor study. Diabetes Care 37:189–196CrossRef
16.
go back to reference Ericson U, Sonestedt E, Gullberg B, Hellstrand S, Hindy G, Wirfalt E, Orho-Melander M (2013) High intakes of protein and processed meat associate with increased incidence of type 2 diabetes. Br J Nutr 109:1143–1153CrossRef Ericson U, Sonestedt E, Gullberg B, Hellstrand S, Hindy G, Wirfalt E, Orho-Melander M (2013) High intakes of protein and processed meat associate with increased incidence of type 2 diabetes. Br J Nutr 109:1143–1153CrossRef
17.
go back to reference Wallin A, Di Giuseppe D, Orsini N, Patel PS, Forouhi NG, Wolk A (2012) Fish consumption, dietary long-chain n-3 fatty acids, and risk of type 2 diabetes: systematic review and meta-analysis of prospective studies. Diabetes Care 35:918–929CrossRef Wallin A, Di Giuseppe D, Orsini N, Patel PS, Forouhi NG, Wolk A (2012) Fish consumption, dietary long-chain n-3 fatty acids, and risk of type 2 diabetes: systematic review and meta-analysis of prospective studies. Diabetes Care 35:918–929CrossRef
18.
go back to reference Xun P, He K (2012) Fish consumption and incidence of diabetes: meta-analysis of data from 438,000 individuals in 12 independent prospective cohorts with an average 11-year follow-up. Diabetes Care 35:930–938CrossRef Xun P, He K (2012) Fish consumption and incidence of diabetes: meta-analysis of data from 438,000 individuals in 12 independent prospective cohorts with an average 11-year follow-up. Diabetes Care 35:930–938CrossRef
19.
go back to reference Wu JH, Micha R, Imamura F, Pan A, Biggs ML, Ajaz O, Djousse L, Hu FB, Mozaffarian D (2012) Omega-3 fatty acids and incident type 2 diabetes: a systematic review and meta-analysis. Br J Nutr 107(Suppl 2):S214–S227CrossRef Wu JH, Micha R, Imamura F, Pan A, Biggs ML, Ajaz O, Djousse L, Hu FB, Mozaffarian D (2012) Omega-3 fatty acids and incident type 2 diabetes: a systematic review and meta-analysis. Br J Nutr 107(Suppl 2):S214–S227CrossRef
20.
go back to reference Mark AB, Poulsen MW, Andersen S, Andersen JM, Bak MJ, Ritz C, Holst JJ, Nielsen J, de Courten B, Dragsted LO, Bugel SG (2014) Consumption of a diet low in advanced glycation end products for 4 weeks improves insulin sensitivity in overweight women. Diabetes Care 37:88–95CrossRef Mark AB, Poulsen MW, Andersen S, Andersen JM, Bak MJ, Ritz C, Holst JJ, Nielsen J, de Courten B, Dragsted LO, Bugel SG (2014) Consumption of a diet low in advanced glycation end products for 4 weeks improves insulin sensitivity in overweight women. Diabetes Care 37:88–95CrossRef
21.
go back to reference Felton JS, Malfatti MA, Knize MG, Salmon CP, Hopmans EC, Wu RW (1997) Health risks of heterocyclic amines. Mutat Res 376:37–41CrossRef Felton JS, Malfatti MA, Knize MG, Salmon CP, Hopmans EC, Wu RW (1997) Health risks of heterocyclic amines. Mutat Res 376:37–41CrossRef
22.
go back to reference Mozaffarian D (2003) Cardiac benefits of fish consumption may depend on the type of fish meal consumed: the cardiovascular health study. Circulation 107:1372–1377CrossRef Mozaffarian D (2003) Cardiac benefits of fish consumption may depend on the type of fish meal consumed: the cardiovascular health study. Circulation 107:1372–1377CrossRef
23.
go back to reference Mozaffarian D, Bryson CL, Lemaitre RN, Burke GL, Siscovick DS (2005) Fish intake and risk of incident heart failure. J Am Coll Cardiol 45:2015–2021CrossRef Mozaffarian D, Bryson CL, Lemaitre RN, Burke GL, Siscovick DS (2005) Fish intake and risk of incident heart failure. J Am Coll Cardiol 45:2015–2021CrossRef
24.
go back to reference Mozaffarian D, Longstreth WT Jr, Lemaitre RN, Manolio TA, Kuller LH, Burke GL, Siscovick DS (2005) Fish consumption and stroke risk in elderly individuals: the cardiovascular health study. Arch Intern Med 165:200–206CrossRef Mozaffarian D, Longstreth WT Jr, Lemaitre RN, Manolio TA, Kuller LH, Burke GL, Siscovick DS (2005) Fish consumption and stroke risk in elderly individuals: the cardiovascular health study. Arch Intern Med 165:200–206CrossRef
25.
go back to reference Mozaffarian D (2004) Fish intake and risk of incident atrial fibrillation. Circulation 110:368–373CrossRef Mozaffarian D (2004) Fish intake and risk of incident atrial fibrillation. Circulation 110:368–373CrossRef
26.
go back to reference Belin RJ, Greenland P, Martin L, Oberman A, Tinker L, Robinson J, Larson J, Van Horn L, Lloyd-Jones D (2011) Fish intake and the risk of incident heart failure: the women’s health initiative. Circ Heart Fail 4:404–413CrossRef Belin RJ, Greenland P, Martin L, Oberman A, Tinker L, Robinson J, Larson J, Van Horn L, Lloyd-Jones D (2011) Fish intake and the risk of incident heart failure: the women’s health initiative. Circ Heart Fail 4:404–413CrossRef
27.
go back to reference Bergkvist C, Akesson A, Glynn A, Michaelsson K, Rantakokko P, Kiviranta H, Wolk A, Berglund M (2012) Validation of questionnaire-based long-term dietary exposure to polychlorinated biphenyls using biomarkers. Mol Nutr Food Res 56:1748–1754CrossRef Bergkvist C, Akesson A, Glynn A, Michaelsson K, Rantakokko P, Kiviranta H, Wolk A, Berglund M (2012) Validation of questionnaire-based long-term dietary exposure to polychlorinated biphenyls using biomarkers. Mol Nutr Food Res 56:1748–1754CrossRef
28.
go back to reference Strom S, Helmfrid I, Glynn A, Berglund M (2011) Nutritional and toxicological aspects of seafood consumption—an integrated exposure and risk assessment of methylmercury and polyunsaturated fatty acids. Environ Res 111:274–280CrossRef Strom S, Helmfrid I, Glynn A, Berglund M (2011) Nutritional and toxicological aspects of seafood consumption—an integrated exposure and risk assessment of methylmercury and polyunsaturated fatty acids. Environ Res 111:274–280CrossRef
29.
go back to reference Wu H, Bertrand KA, Choi AL, Hu FB, Laden F, Grandjean P, Sun Q (2013) Persistent organic pollutants and type 2 diabetes: a prospective analysis in the nurses’ health study and meta-analysis. Environ Health Perspect 121:153–161 Wu H, Bertrand KA, Choi AL, Hu FB, Laden F, Grandjean P, Sun Q (2013) Persistent organic pollutants and type 2 diabetes: a prospective analysis in the nurses’ health study and meta-analysis. Environ Health Perspect 121:153–161
30.
go back to reference He K, Xun P, Liu K, Morris S, Reis J, Guallar E (2013) Mercury exposure in young adulthood and incidence of diabetes later in life: the CARDIA Trace Element Study. Diabetes Care 36:1584–1589CrossRef He K, Xun P, Liu K, Morris S, Reis J, Guallar E (2013) Mercury exposure in young adulthood and incidence of diabetes later in life: the CARDIA Trace Element Study. Diabetes Care 36:1584–1589CrossRef
31.
go back to reference Norman A, Bellocco R, Vaida F, Wolk A (2002) Total physical activity in relation to age, body mass, health and other factors in a Cohort of Swedish Men. Int J Obes Relat Metab Disord 26:670–675CrossRef Norman A, Bellocco R, Vaida F, Wolk A (2002) Total physical activity in relation to age, body mass, health and other factors in a Cohort of Swedish Men. Int J Obes Relat Metab Disord 26:670–675CrossRef
32.
go back to reference Hansson LM, Galanti MR (2000) Diet-associated risks of disease and self-reported food consumption: How shall we treat partial nonresponse in a food frequency questionnaire? Nutr Cancer 36:1–6CrossRef Hansson LM, Galanti MR (2000) Diet-associated risks of disease and self-reported food consumption: How shall we treat partial nonresponse in a food frequency questionnaire? Nutr Cancer 36:1–6CrossRef
33.
go back to reference Bergström L, Kylberg E, Hagman U, Erikson H, Bruce A (1991) The food composition database KOST: the National Administration’s information system for nutritive values of food. Vår Föda 43:439–447 Bergström L, Kylberg E, Hagman U, Erikson H, Bruce A (1991) The food composition database KOST: the National Administration’s information system for nutritive values of food. Vår Föda 43:439–447
34.
go back to reference Messerer M, Johansson SE, Wolk A (2004) The validity of questionnaire-based micronutrient intake estimates is increased by including dietary supplement use in Swedish Men. J Nutr 134:1800–1805 Messerer M, Johansson SE, Wolk A (2004) The validity of questionnaire-based micronutrient intake estimates is increased by including dietary supplement use in Swedish Men. J Nutr 134:1800–1805
35.
go back to reference Fung TT, Chiuve SE, McCullough ML, Rexrode KM, Logroscino G, Hu FB (2008) Adherence to a DASH-style diet and risk of coronary heart disease and stroke in women. Arch Intern Med 168:713–720CrossRef Fung TT, Chiuve SE, McCullough ML, Rexrode KM, Logroscino G, Hu FB (2008) Adherence to a DASH-style diet and risk of coronary heart disease and stroke in women. Arch Intern Med 168:713–720CrossRef
36.
go back to reference Glynn AW, Granath F, Aune M, Atuma S, Darnerud PO, Bjerselius R, Vainio H, Weiderpass E (2003) Organochlorines in Swedish women: determinants of serum concentrations. Environ Health Perspect 111:349–355CrossRef Glynn AW, Granath F, Aune M, Atuma S, Darnerud PO, Bjerselius R, Vainio H, Weiderpass E (2003) Organochlorines in Swedish women: determinants of serum concentrations. Environ Health Perspect 111:349–355CrossRef
37.
go back to reference Pauwels A, Covaci A, Weyler J, Delbeke L, Dhont M, De Sutter P, D’Hooghe T, Schepens PJ (2000) Comparison of persistent organic pollutant residues in serum and adipose tissue in a female population in Belgium, 1996–1998. Arch Environ Contam Toxicol 39:265–270CrossRef Pauwels A, Covaci A, Weyler J, Delbeke L, Dhont M, De Sutter P, D’Hooghe T, Schepens PJ (2000) Comparison of persistent organic pollutant residues in serum and adipose tissue in a female population in Belgium, 1996–1998. Arch Environ Contam Toxicol 39:265–270CrossRef
38.
go back to reference Willett W, Stampfer MJ (1986) Total energy intake: implications for epidemiologic analyses. Am J Epidemiol 124:17–27CrossRef Willett W, Stampfer MJ (1986) Total energy intake: implications for epidemiologic analyses. Am J Epidemiol 124:17–27CrossRef
39.
go back to reference Norman A, Bellocco R, Bergstrom A, Wolk A (2001) Validity and reproducibility of self-reported total physical activity—differences by relative weight. Int J Obes Relat Metab Disord 25:682–688CrossRef Norman A, Bellocco R, Bergstrom A, Wolk A (2001) Validity and reproducibility of self-reported total physical activity—differences by relative weight. Int J Obes Relat Metab Disord 25:682–688CrossRef
41.
go back to reference Patel PS, Forouhi NG, Kuijsten A, Schulze MB, van Woudenbergh GJ, Ardanaz E, Amiano P, Arriola L, Balkau B, Barricarte A, Beulens JW, Boeing H, Buijsse B, Crowe FL, de Lauzon-Guillan B, Fagherazzi G, Franks PW, Gonzalez C, Grioni S, Halkjaer J, Huerta JM, Key TJ, Kuhn T, Masala G, Nilsson P, Overvad K, Panico S, Quiros JR, Rolandsson O, Sacerdote C, Sanchez MJ, Schmidt EB, Slimani N, Spijkerman AM, Teucher B, Tjonneland A, Tormo MJ, Tumino R, van der AD, van der Schouw YT, Sharp SJ, Langenberg C, Feskens EJ, Riboli E, Wareham NJ (2012) The prospective association between total and type of fish intake and type 2 diabetes in 8 European countries: EPIC-InterAct Study. Am J Clin Nutr 95:1445–1453CrossRef Patel PS, Forouhi NG, Kuijsten A, Schulze MB, van Woudenbergh GJ, Ardanaz E, Amiano P, Arriola L, Balkau B, Barricarte A, Beulens JW, Boeing H, Buijsse B, Crowe FL, de Lauzon-Guillan B, Fagherazzi G, Franks PW, Gonzalez C, Grioni S, Halkjaer J, Huerta JM, Key TJ, Kuhn T, Masala G, Nilsson P, Overvad K, Panico S, Quiros JR, Rolandsson O, Sacerdote C, Sanchez MJ, Schmidt EB, Slimani N, Spijkerman AM, Teucher B, Tjonneland A, Tormo MJ, Tumino R, van der AD, van der Schouw YT, Sharp SJ, Langenberg C, Feskens EJ, Riboli E, Wareham NJ (2012) The prospective association between total and type of fish intake and type 2 diabetes in 8 European countries: EPIC-InterAct Study. Am J Clin Nutr 95:1445–1453CrossRef
42.
go back to reference Cahill LE, Pan A, Chiuve SE, Sun Q, Willett WC, Hu FB, Rimm EB (2014) Fried-food consumption and risk of type 2 diabetes and coronary artery disease: a prospective study in 2 cohorts of US women and men. Am J Clin Nutr 100:667–675CrossRef Cahill LE, Pan A, Chiuve SE, Sun Q, Willett WC, Hu FB, Rimm EB (2014) Fried-food consumption and risk of type 2 diabetes and coronary artery disease: a prospective study in 2 cohorts of US women and men. Am J Clin Nutr 100:667–675CrossRef
43.
go back to reference Guallar-Castillon P, Rodriguez-Artalejo F, Fornes NS, Banegas JR, Etxezarreta PA, Ardanaz E, Barricarte A, Chirlaque MD, Iraeta MD, Larranaga NL, Losada A, Mendez M, Martinez C, Quiros JR, Navarro C, Jakszyn P, Sanchez MJ, Tormo MJ, Gonzalez CA (2007) Intake of fried foods is associated with obesity in the cohort of Spanish adults from the European Prospective Investigation into Cancer and Nutrition. Am J Clin Nutr 86:198–205 Guallar-Castillon P, Rodriguez-Artalejo F, Fornes NS, Banegas JR, Etxezarreta PA, Ardanaz E, Barricarte A, Chirlaque MD, Iraeta MD, Larranaga NL, Losada A, Mendez M, Martinez C, Quiros JR, Navarro C, Jakszyn P, Sanchez MJ, Tormo MJ, Gonzalez CA (2007) Intake of fried foods is associated with obesity in the cohort of Spanish adults from the European Prospective Investigation into Cancer and Nutrition. Am J Clin Nutr 86:198–205
44.
go back to reference Sayon-Orea C, Martinez-Gonzalez MA, Gea A, Flores-Gomez E, Basterra-Gortari FJ, Bes-Rastrollo M (2014) Consumption of fried foods and risk of metabolic syndrome: the SUN cohort study. Clin Nutr 33:545–549CrossRef Sayon-Orea C, Martinez-Gonzalez MA, Gea A, Flores-Gomez E, Basterra-Gortari FJ, Bes-Rastrollo M (2014) Consumption of fried foods and risk of metabolic syndrome: the SUN cohort study. Clin Nutr 33:545–549CrossRef
45.
go back to reference Lutsey PL, Steffen LM, Stevens J (2008) Dietary intake and the development of the metabolic syndrome: the Atherosclerosis Risk in Communities study. Circulation 117:754–761CrossRef Lutsey PL, Steffen LM, Stevens J (2008) Dietary intake and the development of the metabolic syndrome: the Atherosclerosis Risk in Communities study. Circulation 117:754–761CrossRef
46.
go back to reference Wagner KH, Elmadfa I (2012) Chemical and biological modulations of food due to the frying process. Int J Vitam Nutr Res 82:163–167CrossRef Wagner KH, Elmadfa I (2012) Chemical and biological modulations of food due to the frying process. Int J Vitam Nutr Res 82:163–167CrossRef
47.
go back to reference Elmstahl S, Gullberg B (1997) Bias in diet assessment methods–consequences of collinearity and measurement errors on power and observed relative risks. Int J Epidemiol 26:1071–1079CrossRef Elmstahl S, Gullberg B (1997) Bias in diet assessment methods–consequences of collinearity and measurement errors on power and observed relative risks. Int J Epidemiol 26:1071–1079CrossRef
48.
go back to reference Mozaffarian D, Shi P, Morris JS, Grandjean P, Siscovick DS, Spiegelman D, Hu FB (2013) Methylmercury exposure and incident diabetes in U.S. men and women in two prospective cohorts. Diabetes Care 36:3578–3584CrossRef Mozaffarian D, Shi P, Morris JS, Grandjean P, Siscovick DS, Spiegelman D, Hu FB (2013) Methylmercury exposure and incident diabetes in U.S. men and women in two prospective cohorts. Diabetes Care 36:3578–3584CrossRef
49.
go back to reference Sunderland EM (2007) Mercury exposure from domestic and imported estuarine and marine fish in the U.S. seafood market. Environ Health Perspect 115:235–242CrossRef Sunderland EM (2007) Mercury exposure from domestic and imported estuarine and marine fish in the U.S. seafood market. Environ Health Perspect 115:235–242CrossRef
50.
go back to reference Aguilar A, Borrell A, Reijnders PJ (2002) Geographical and temporal variation in levels of organochlorine contaminants in marine mammals. Mar Environ Res 53:425–452CrossRef Aguilar A, Borrell A, Reijnders PJ (2002) Geographical and temporal variation in levels of organochlorine contaminants in marine mammals. Mar Environ Res 53:425–452CrossRef
51.
go back to reference Glynn AW, Wolk A, Aune M, Atuma S, Zettermark S, Maehle-Schmid M, Darnerud PO, Becker W, Vessby B, Adami HO (2000) Serum concentrations of organochlorines in men: a search for markers of exposure. Sci Total Environ 263:197–208CrossRef Glynn AW, Wolk A, Aune M, Atuma S, Zettermark S, Maehle-Schmid M, Darnerud PO, Becker W, Vessby B, Adami HO (2000) Serum concentrations of organochlorines in men: a search for markers of exposure. Sci Total Environ 263:197–208CrossRef
52.
go back to reference Deckelbaum RJ, Worgall TS, Seo T (2006) n-3 fatty acids and gene expression. Am J Clin Nutr 83:1520S–1525S Deckelbaum RJ, Worgall TS, Seo T (2006) n-3 fatty acids and gene expression. Am J Clin Nutr 83:1520S–1525S
53.
go back to reference Akinkuolie AO, Ngwa JS, Meigs JB, Djousse L (2011) Omega-3 polyunsaturated fatty acid and insulin sensitivity: a meta-analysis of randomized controlled trials. Clin Nutr 30:702–707CrossRef Akinkuolie AO, Ngwa JS, Meigs JB, Djousse L (2011) Omega-3 polyunsaturated fatty acid and insulin sensitivity: a meta-analysis of randomized controlled trials. Clin Nutr 30:702–707CrossRef
54.
go back to reference Afzal S, Bojesen SE, Nordestgaard BG (2013) Low 25-hydroxyvitamin D and risk of type 2 diabetes: a prospective cohort study and metaanalysis. Clin Chem 59:381–391CrossRef Afzal S, Bojesen SE, Nordestgaard BG (2013) Low 25-hydroxyvitamin D and risk of type 2 diabetes: a prospective cohort study and metaanalysis. Clin Chem 59:381–391CrossRef
55.
go back to reference Ye Z, Sharp SJ, Burgess S, Scott RA, Imamura F, Langenberg C, Wareham NJ, Forouhi NG (2015) Association between circulating 25-hydroxyvitamin D and incident type 2 diabetes: a mendelian randomisation study. Lancet Diabetes Endocrinol 3:35–42CrossRef Ye Z, Sharp SJ, Burgess S, Scott RA, Imamura F, Langenberg C, Wareham NJ, Forouhi NG (2015) Association between circulating 25-hydroxyvitamin D and incident type 2 diabetes: a mendelian randomisation study. Lancet Diabetes Endocrinol 3:35–42CrossRef
56.
go back to reference Seida JC, Mitri J, Colmers IN, Majumdar SR, Davidson MB, Edwards AL, Hanley DA, Pittas AG, Tjosvold L, Johnson JA (2014) Effect of vitamin D supplementation on improving glucose homeostasis and preventing diabetes: a systematic review and meta-analysis. J Clin Endocrinol Metab 99:3551–3560CrossRef Seida JC, Mitri J, Colmers IN, Majumdar SR, Davidson MB, Edwards AL, Hanley DA, Pittas AG, Tjosvold L, Johnson JA (2014) Effect of vitamin D supplementation on improving glucose homeostasis and preventing diabetes: a systematic review and meta-analysis. J Clin Endocrinol Metab 99:3551–3560CrossRef
57.
go back to reference Park K, Rimm EB, Siscovick DS, Spiegelman D, Manson JE, Morris JS, Hu FB, Mozaffarian D (2012) Toenail selenium and incidence of type 2 diabetes in U.S. men and women. Diabetes Care 35:1544–1551CrossRef Park K, Rimm EB, Siscovick DS, Spiegelman D, Manson JE, Morris JS, Hu FB, Mozaffarian D (2012) Toenail selenium and incidence of type 2 diabetes in U.S. men and women. Diabetes Care 35:1544–1551CrossRef
58.
go back to reference Stranges S, Marshall JR, Natarajan R, Donahue RP, Trevisan M, Combs GF, Cappuccio FP, Ceriello A, Reid ME (2007) Effects of long-term selenium supplementation on the incidence of type 2 diabetes: a randomized trial. Ann Intern Med 147:217–223CrossRef Stranges S, Marshall JR, Natarajan R, Donahue RP, Trevisan M, Combs GF, Cappuccio FP, Ceriello A, Reid ME (2007) Effects of long-term selenium supplementation on the incidence of type 2 diabetes: a randomized trial. Ann Intern Med 147:217–223CrossRef
59.
go back to reference Vikoren LA, Nygard OK, Lied E, Rostrup E, Gudbrandsen OA (2013) A randomised study on the effects of fish protein supplement on glucose tolerance, lipids and body composition in overweight adults. Br J Nutr 109:648–657CrossRef Vikoren LA, Nygard OK, Lied E, Rostrup E, Gudbrandsen OA (2013) A randomised study on the effects of fish protein supplement on glucose tolerance, lipids and body composition in overweight adults. Br J Nutr 109:648–657CrossRef
60.
go back to reference Ouellet V, Marois J, Weisnagel SJ, Jacques H (2007) Dietary cod protein improves insulin sensitivity in insulin-resistant men and women: a randomized controlled trial. Diabetes Care 30:2816–2821CrossRef Ouellet V, Marois J, Weisnagel SJ, Jacques H (2007) Dietary cod protein improves insulin sensitivity in insulin-resistant men and women: a randomized controlled trial. Diabetes Care 30:2816–2821CrossRef
Metadata
Title
Fish consumption and frying of fish in relation to type 2 diabetes incidence: a prospective cohort study of Swedish men
Authors
Alice Wallin
Daniela Di Giuseppe
Nicola Orsini
Agneta Åkesson
Nita G. Forouhi
Alicja Wolk
Publication date
01-03-2017
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Nutrition / Issue 2/2017
Print ISSN: 1436-6207
Electronic ISSN: 1436-6215
DOI
https://doi.org/10.1007/s00394-015-1132-6

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