Marine N-3 Polyunsaturated Fatty Acids Are Inversely Associated with Risk of Type 2 Diabetes in Asians: A Systematic Review and Meta-Analysis
Open accessAbstract
BACKGROUND: Prospective cohort studies in relation to the associations between n-3 polyunsaturated fatty acids (PUFA) and risk of type 2 diabetes (T2D) were inconsistent. Differences in tissue n-3 PUFA compositions in subjects with and without T2D were also inconsistent in both cohort and case-control studies. We conducted a systematic review and meta-analysis of prospective cohort studies to examine the associations of fish and n-3 PUFA intake with T2D risk. The differences in tissue n-3 PUFA compositions in subjects with and without T2D were investigated based on cohort and case-control studies. METHODS AND FINDINGS: PubMed, Embase, Cochrane library, China National Knowledge Infrastructure (CNKI) and Chinese VIP database up to January 2012 was used to identify relevant studies, and reference lists from retrieved studies were reviewed. Two authors independently extracted the data. Random-effects models were used to pool the summary relative risk (RR). Twenty-four studies including 24,509 T2D patients and 545,275 participants were identified. For cohort studies, the summary RR of T2D for the highest vs lowest categories of total fish, marine n-3 PUFA and alpha-linolenic acid intake was 1.07 (95% CI: 0.91, 1.25), 1.07 (95% CI: 0.95, 1.20) and 0.93 (95% CI: 0.81, 1.07), respectively. Subgroup analyses indicated that summary RR (highest vs lowest category) of T2D for fish and marine n-3 PUFA intake was 0.89 (95% CI: 0.81, 0.98) and 0.87 (95% CI: 0.79, 0.96) for Asian populations, and 1.20 (95% CI: 1.01, 1.44) and 1.16 (95% CI: 1.04, 1.28) for Western populations. Asian subjects with T2D had significantly lower tissue compositions of C22:6n-3 (SMD: -1.43; 95% CI: -1.75, -1.12) and total n-3 PUFA (SMD: -1.41; 95% CI: -2.23, -0.59) compared with those without T2D. CONCLUSION: This systematic review and meta-analysis provides evidence that marine n-3 PUFA have beneficial effects on the prevention of T2D in Asian populations.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Fish and omega-3 intake have little association with diabetes risk, although protective associations are seen in Asian populations and fish oil supplementation modestly raises adiponectin.
“Fish and omega-3 intake also have little association with diabetes risk, although protective associations are seen in Asian populations209-211 and fish oil supplementation modestly raises adiponectin.212”
From Dietary and Policy Priorities for Cardiovascular Disease, Diabetes, and Obesity: A Comprehensive Review (2016) · cites this paper as [209]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Measuring inconsistency in meta-analyses
Higgins, J. P. T., Thompson, S. G., Deeks, J. J., & Altman, D. G. (2003) · BMJ · doi:10.1136/bmj.327.7414.557 · Cited by 63,139 · see citing works
Stroup, D. F. (2000) · JAMA · doi:10.1001/jama.283.15.2008 · Cited by 20,623 · see citing works
Global estimates of the prevalence of diabetes for 2010 and 2030
Shaw, J. E., Sicree, R. A., & Zimmet, P. Z. (2010) · Diabetes Research and Clinical Practice · doi:10.1016/j.diabres.2009.10.007 · Cited by 7,216 · see citing works
Hindorff, L. A., Sethupathy, P., Junkins, H. A., Ramos, E. M., Mehta, J. P., Collins, F. S., & Manolio, T. A. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0903103106 · Cited by 4,013 · see citing works
Methods for Trend Estimation from Summarized Dose-Response Data, with Applications to Meta-Analysis
Greenland, S., & Longnecker, M. P. (1992) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a116237 · Cited by 2,353 · see citing works
Generalized Least Squares for Trend Estimation of Summarized Dose–response Data
Orsini, N., Bellocco, R., & Greenland, S. (2006) · The Stata Journal Promoting communications on statistics and Stata · doi:10.1177/1536867x0600600103 · Cited by 1,245 · see citing works
Storlien, L. H., Jenkins, A. B., Chisholm, D. J., Pascoe, W. S., Khouri, S., & Kraegen, E. W. (1991) · Diabetes · doi:10.2337/diab.40.2.280 · Cited by 967 · see citing works
Borkman, M., Storlien, L. H., Pan, D. A., Jenkins, A. B., Chisholm, D. J., & Campbell, L. V. (1993) · New England Journal of Medicine · doi:10.1056/nejm199301283280404 · Cited by 835 · see citing works
Dietary Patterns and Risk for Type 2 Diabetes Mellitus in U.S. Men
van Dam, R. M., Rimm, E. B., Willett, W. C., Stampfer, M. J., & Hu, F. B. (2002) · Annals of Internal Medicine · doi:10.7326/0003-4819-136-3-200202050-00008 · Cited by 801 · see citing works
Fish Oil Prevents Insulin Resistance Induced by High-Fat Feeding in Rats
Storlien, L. H., Kraegen, E. W., Chisholm, D. J., Ford, G. L., Bruce, D. G., & Pascoe, W. S. (1987) · Science · doi:10.1126/science.3303333 · Cited by 650 · see citing works
Dietary Fat and Meat Intake in Relation to Risk of Type 2 Diabetes in Men
van Dam, R. M., Willett, W. C., Rimm, E. B., Stampfer, M. J., & Hu, F. B. (2002) · Diabetes Care · doi:10.2337/diacare.25.3.417 · Cited by 593 · see citing works
Feskens, E. J. M., Virtanen, S. M., Räsänen, L., Tuomilehto, J. O., Stengård, J., Pekkanen, J., Nissinen, A. M., & Kromhout, D. (1995) · Diabetes Care · doi:10.2337/diacare.18.8.1104 · Cited by 504 · see citing works
Dietary fat and incidence of type 2 diabetes in older Iowa women
Meyer, K. A., Kushi, L. H., Jacobs, D. R., & Folsom, A. R. (2001) · Diabetes Care · doi:10.2337/diacare.24.9.1528 · Cited by 382 · see citing works
Wang, L., Folsom, A. R., Zheng, Z.-J., Pankow, J. S., & Eckfeldt, J. H. (2003) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/78.1.91 · Cited by 364 · see citing works
n−3 Fatty acids and gene expression
Deckelbaum, R. J., Worgall, T. S., & Seo, T. (2006) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/83.6.1520s · Cited by 360 · see citing works
Woodman, R. J., Mori, T. A., Burke, V., Puddey, I. B., Watts, G. F., & Beilin, L. J. (2002) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/76.5.1007 · Cited by 338 · see citing works
Fish consumption and CHD mortality: an updated meta-analysis of seventeen cohort studies.
Zheng, J., Huang, T., Yu, Y., Hu, X., Yang, B., & Li, D. (2012) · Public Health Nutrition · doi:10.1017/s1368980011002254 · Cited by 311 · see citing works
Self-citationFish oil and glycemic control in diabetes. A meta-analysis.
Friedberg, C. E., Janssen, M. J. F. M., Heine, R. J., & Grobbee, D. E. (1998) · Diabetes Care · doi:10.2337/diacare.21.4.494 · Cited by 303 · see citing works
Hodge, A. M., English, D. R., O’Dea, K., Sinclair, A. J., Makrides, M., Gibson, R. A., & Giles, G. G. (2007) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/86.1.189 · Cited by 287 · see citing works
Kröger, J., Zietemann, V., Enzenbach, C., Weikert, C., Jansen, E. H., Döring, F., Joost, H.-G., Boeing, H., & Schulze, M. B. (2011) · The American Journal of Clinical Nutrition · doi:10.3945/ajcn.110.005447 · Cited by 270 · see citing works
The Risk to Develop NIDDM Is Related to the Fatty Acid Composition of the Serum Cholesterol Esters
Vessby, B. O., Aro, A., Skarfors, E., Berglund, L., Salminen, I., & Lithell, H. (1994) · Diabetes · doi:10.2337/diab.43.11.1353 · Cited by 258 · see citing works
Dietary Patterns and the Incidence of Type 2 Diabetes
Montonen, J. (2005) · American Journal of Epidemiology · doi:10.1093/aje/kwi039 · Cited by 258 · see citing works
Cross‐Talk between PPARγand Insulin Signaling and Modulation of Insulin Sensitivity
Leonardini, A., Laviola, L., Perrini, S., Natalicchio, A., & Giorgino, F. (2009) · PPAR Research · doi:10.1155/2009/818945 · Cited by 241 · see citing works
Storlien, L. H., Jenkins, A. B., Chisholm, D. J., Pascoe, W. S., Khouri, S., & Kraegen, E. W. (1991) · Diabetes · doi:10.2337/diabetes.40.2.280 · Cited by 229 · see citing works
Feskens, E. J. M., Bowles, C. H., & Kromhout, D. (1991) · Diabetes Care · doi:10.2337/diacare.14.11.935 · Cited by 219 · see citing works
Long-chain omega-3 fatty acids, fish intake, and the risk of type 2 diabetes mellitus
Kaushik, M., Mozaffarian, D., Spiegelman, D. L., Manson, J. E., Willett, W. C., & Hu, F. B. (2009) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.2008.27424 · Cited by 208 · see citing works
Dietary omega-3 fatty acids and fish consumption and risk of type 2 diabetes
Djoussé, L., Gaziano, J. M., Buring, J. E., & Lee, I.-M. M. (2010) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.110.005603 · Cited by 182 · see citing works
Akinkuolie, A. O., Ngwa, J. S., Meigs, J. B., & Djoussé, L. (2011) · Clinical Nutrition · doi:10.1016/j.clnu.2011.08.013 · Cited by 167 · see citing works
Toft, I., Bonaa, K. H., Ingebretsen, O. C., Nordoy, A., & Jenssen, T. (1995) · Annals of Internal Medicine · doi:10.7326/0003-4819-123-12-199512150-00003 · Cited by 159 · see citing works
Fatty acid profile of the erythrocyte membrane preceding development of Type 2 diabetes mellitus
Krachler, B., Norberg, M., Eriksson, J. W., Hallmans, G., Johansson, I., Vessby, B. O., Weinehall, L., & Lindahl, B. (2007) · Nutrition Metabolism and Cardiovascular Diseases · doi:10.1016/j.numecd.2007.04.005 · Cited by 158 · see citing works
Mostad, I. L., Bjerve, K. S., Bjorgaas, M. R., Lydersen, S., & Grill, V. (2006) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/84.3.540 · Cited by 152 · cited 1× · see citing works
“Most controlled trials [50,51] did not find significant associations between fish oil treatment and parameters of glucose metabolism; some controlled trials [52,53] even reported mild adverse effects of fish oil on glucose metabolism.”
BackgroundDietary factors determining diabetes and impaired glucose tolerance
Feskens, E. J. M., Virtanen, S., Räsänen, L., Tuomilehto, J., Stengård, J., Pekkanen, J., Nissinen, A. E. T., & Kromhout, D. (1995) · Diabetes Care · Cited by 148 · see citing works
Association Between Type of Dietary Fish and Seafood Intake and the Risk of Incident Type 2 Diabetes
Patel, P. S., Sharp, S. J., Luben, R. N., Khaw, K.-T., Bingham, S. A., Wareham, N. J., & Forouhi, N. G. (2009) · Diabetes Care · doi:10.2337/dc09-0116 · Cited by 140 · see citing works
Chen, R., Corona, E., Sikora, M., Dudley, J. T., Morgan, A. A., Moreno‐Estrada, A., Nilsen, G. B., Ruau, D., Lincoln, S. E., Bustamante, C. D., et al. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1002621 · Cited by 127 · see citing works
Plasma omega-3 fatty acids and incident diabetes in older adults
Djoussé, L., Biggs, M. L., Lemaître, R. N., King, I. B., Song, X., Ix, J. H., Mukamal, K. J., Siscovick, D. S., & Mozaffarian, D. (2011) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.111.013334 · Cited by 117 · see citing works
Fish-seafood consumption, obesity, and risk of type 2 diabetes: an ecological study
Nkondjock, A., & Receveur, O. (2003) · Diabetes & Metabolism · doi:10.1016/s1262-3636(07)70080-0 · Cited by 111 · see citing works
Eating Fish and Risk of Type 2 Diabetes
Woudenbergh, G. J. G.-V., van Ballegooijen, A. J., Kuijsten, A., Sijbrands, E. J. G., van Rooij, F. J. A., Geleijnse, J. M., Albert Hofman, D., Witteman, J. C. M., & Feskens, E. J. M. (2009) · Diabetes Care · doi:10.2337/dc09-1042 · Cited by 110 · see citing works
Villegas, R., Xiang, Y.-B., Elasy, T. A., Li, H. L., Yang, G., Cai, H., Ye, F., Gao, Y.-T., Shyr, Y., Zheng, W., et al. (2011) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.111.013193 · Cited by 110 · see citing works
Nanri, A., Mizoue, T., Noda, M., Takahashi, Y., Matsushita, Y., Poudel‐Tandukar, K., Kato, M., Oba, S., Inoue, M., & Tsugane, S. (2011) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.111.012252 · Cited by 110 · see citing works
Omega-3 fatty acids and incident type 2 diabetes: the Singapore Chinese Health Study
Brostow, D. P., Odegaard, A., Koh, W., Duval, S., Gross, M. D., Yuan, J., & Pereira, M. A. (2011) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.110.009357 · Cited by 103 · see citing works
Genes, Diet and Type 2 Diabetes Mellitus: A Review
Dedoussis, G. V., Kaliora, A. C., & Panagiotakos, D. B. (2007) · The Review of Diabetic Studies · doi:10.1900/rds.2007.4.13 · Cited by 87 · see citing works
Serum phospholipid fatty acid composition and insulin action in type 2 diabetic patients
Pelik�nov�, T., Kazdov�, L., Chvojkov[aacute], [., & Ba[scaron]e, J. (2001) · Metabolism · doi:10.1053/meta.2001.27195 · Cited by 80 · see citing works
Klimentidis, Y. C., Abrams, M., Wang, J., Fernández, J. R., & Allison, D. B. (2010) · Human Genetics · doi:10.1007/s00439-010-0935-z · Cited by 74 · see citing works
Lee, Y., Lai, C., Ordovás, J. M., & Parnell, L. D. (2011) · Journal of Data Mining in Genomics & Proteomics · doi:10.4172/2153-0602.1000106 · Cited by 67 · see citing works
The risk to develop NIDDM is related to the fatty acid composition of the serum cholesterol esters
Vessby, B., Aro, A., Skarfors, E., et al. (1994) · Diabetes · doi:10.2337/diabetes.43.11.1353 · Cited by 67 · see citing works
Bakan, E., Yıldırım, A., Kurtul, N., Polat, M., Dursun, H., & Cayir, K. (2006) · Acta Diabetologica · doi:10.1007/s00592-007-0224-4 · Cited by 63 · see citing works
Huang, T., Wahlqvist, M. L., Xu, T., Xu, A., Zhang, A., & Li, D. (2009) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.200900189 · Cited by 53 · see citing works
Self-citationPlasma phospholipids n‐3 polyunsaturated fatty acid is associated with metabolic syndrome
Huang, T., Bhulaidok, S., Cai, Z., Xu, T., Xu, F., Wahlqvist, M. L., & Li, D. (2010) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201000025 · Cited by 38 · see citing works
Self-citationEgert, S., Fobker, M., Andersen, G., Somoza, V., Erbersdobler, H. F., & Wahrburg, U. (2008) · Annals of Nutrition and Metabolism · doi:10.1159/000172980 · Cited by 38 · see citing works
Red blood cell and plasma fatty acid composition in diabetes mellitus
Faas, F. H., Dang, A. Q., Kemp, K., Norman, J., & Carter, W. J. (1988) · Metabolism · doi:10.1016/0026-0495(88)90002-9 · Cited by 34 · see citing works
Rodríguez, Y., & Christophe, A. B. (2004) · Annals of Nutrition and Metabolism · doi:10.1159/000081201 · Cited by 12 · see citing works
Adaptive Genetic Variation and Population Differences
Lai, C. (2012) · Progress in molecular biology and translational science · doi:10.1016/b978-0-12-398397-8.00018-6 · Cited by 10 · see citing works
The prevention of type 2 diabetes: should we recommend vegetable oils instead of fatty fish?
Feskens, E. J. M. (2011) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.111.020172 · Cited by 9 · see citing works
Eating Fish and Risk of Type 2 Diabetes: A Population-Based, Prospective Follow-Up Study
Boucher, B. J., & Mannan, N. (2010) · Diabetes Care · doi:10.2337/dc10-0852 · Cited by 8 · see citing works
Abnormal Serum Fatty Acid Composition in Non‐Insulin‐Dependent Diabetes Mellitus
Bohov, P., GELIENOVÁ, K., ŠEBÖKOVÁ, E., & Klimeś, I. (1993) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1993.tb35736.x · Cited by 5 · see citing works
Du, L. (2007) · Zhongguo quanke yixue · Cited by 1 · see citing works
Flagged first, then by citations
1 of the 57 references couldn’t be matched to a known paper.
Research works printed but not linked: 1
- [32]Zhang B, Wang ZZ, Song HP (2011) The change of plasma long-chain polyunsaturated fatty acids in type 2 diabetes (in Chinese). Journal of China Traditional Chinese Medicine Information 3: 353– 354.
Cited by
Sorted by citations
Mozaffarian, D. (2016) · Circulation · doi:10.1161/circulationaha.115.018585 · Cited by 2,216 · see citing works
Del Gobbo, L. C., Imamura, F., Aslibekyan, S., Marklund, M., Virtanen, J. K., Wennberg, M., Yakoob, M. Y., Chiuve, S. E., dela Cruz, L., Frazier-Wood, A. C., et al. (2016) · JAMA Internal Medicine · doi:10.1001/jamainternmed.2016.2925 · Cited by 404 · see citing works
Fatty Acid Desaturases, Polyunsaturated Fatty Acid Regulation, and Biotechnological Advances
Lee, J. M., Lee, H., Kang, S., & Park, W. (2016) · Nutrients · doi:10.3390/nu8010023 · Cited by 401 · see citing works
Brown, T. J., Brainard, J., Song, F., Wang, X., Abdelhamid, A., & Hooper, L. (2019) · BMJ · doi:10.1136/bmj.l4697 · Cited by 313 · see citing works
EFSA Dietetic Products, N. (2014) · EFSA Journal · doi:10.2903/j.efsa.2014.3761 · Cited by 217 · see citing works
Health benefits of plant-derived α-linolenic acid
Rajaram, S. (2014) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.113.071514 · Cited by 211 · see citing works
Forouhi, N. G., Imamura, F., Sharp, S. J., Koulman, A., Schulze, M. B., Zheng, J., Ye, Z., Sluijs, I., Guevara, M., Huerta, J. M., et al. (2016) · PLoS Medicine · doi:10.1371/journal.pmed.1002094 · Cited by 208 · see citing works
Self-citationThe Effect of n-3 Fatty Acids on Glucose Homeostasis and Insulin Sensitivity
Flachs, P., Rossmeisl, M., & Kopecký, J. (2014) · Physiological Research · doi:10.33549/physiolres.932715 · Cited by 183 · see citing works
Phung, T. L., Anothaisintawee, T., Chaikledkaew, U., Briones, J. R., Reutrakul, S., & Thakkinstian, A. (2020) · Nutrients · doi:10.3390/nu12092722 · Cited by 194 · see citing works
Mahendran, Y., Cederberg, H., Vangipurapu, J., Kangas, A. J., Soininen, P., Kuusisto, J., Uusitupa, M. I. J., Ala‐Korpela, M., & Laakso, M. (2013) · Diabetes Care · doi:10.2337/dc13-0800 · Cited by 162 · see citing works
Insulin-sensitizing effects of omega-3 fatty acids: lost in translation?
Lalia, A., & Lanza, I. (2016) · Nutrients · doi:10.3390/nu8060329 · Cited by 141 · see citing works
Chen, C., Yu, X., & Shao, S. (2015) · PLOS ONE · doi:10.1371/journal.pone.0139565 · Cited by 133 · see citing works
Virtanen, J. K., Mursu, J., Voutilainen, S., Uusitupa, M. I. J., & Tuomainen, T. (2013) · Diabetes Care · doi:10.2337/dc13-1504 · Cited by 114 · see citing works
Update on cardiometabolic health effects of ω-3 fatty acids
Kromhout, D., & de Goede, J. (2013) · Current Opinion in Lipidology · doi:10.1097/mol.0000000000000041 · Cited by 101 · see citing works
Dietary Fat and Risk for Type 2 Diabetes: a Review of Recent Research
Bradley, B. H. R. (2018) · Current Nutrition Reports · doi:10.1007/s13668-018-0244-z · Cited by 99 · see citing works
Furan fatty acids – Beneficial or harmful to health?
Xu, L., Sinclair, A. J., Faiza, M., Li, D., Han, X., Yin, H., & Wang, Y. (2017) · Progress in Lipid Research · doi:10.1016/j.plipres.2017.10.002 · Cited by 98 · see citing works
Self-citationNatural Molecules in the Management of Polycystic Ovary Syndrome (PCOS): An Analytical Review
Iervolino, M., Lepore, E., Forte, G., Laganà, A. S., Buzzaccarini, G., & Unfer, V. (2021) · Nutrients · doi:10.3390/nu13051677 · Cited by 98 · see citing works
An Improvement of Cardiovascular Risk Factors by Omega-3 Polyunsaturated Fatty Acids
Yanai, H., Masui, Y., Katsuyama, H., Adachi, H., Kawaguchi, A., Hakoshima, M., Waragai, Y., Harigae, T., & Sako, A. (2018) · Journal of Clinical Medicine Research · doi:10.14740/jocmr3362w · Cited by 93 · see citing works
Venkatakrishnan, K., Chiu, H., & Wang, C. (2019) · Journal of Functional Foods · doi:10.1016/j.jff.2019.04.039 · Cited by 91 · see citing works
Batis, C., Méndez, M. A., Gordon‐Larsen, P., Sotres‐Alvarez, D., Adair, L. S., & Popkin, B. M. (2015) · Public Health Nutrition · doi:10.1017/s1368980014003103 · Cited by 85 · see citing works
Zhu, Y., Li, M., Rahman, M. L., Hinkle, S. N., Wu, J., Weir, N. L., Lin, Y., Yang, H., Tsai, M. Y., Ferrara, A., et al. (2019) · PLOS Medicine · doi:10.1371/journal.pmed.1002910 · Cited by 79 · see citing works
Zheng, J., Lin, M., Fang, L., Yu, Y., Yuan, L., Jin, Y., Feng, J., Wang, L., Yang, H., Chen, W., et al. (2016) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201600230 · Cited by 70 · see citing works
Self-citationZhang, M., Picard‐Deland, É., & Marette, A. (2013) · International Journal of Endocrinology · doi:10.1155/2013/501015 · Cited by 66 · see citing works
DHA-enriched fish oil reduces insulin resistance in overweight and obese adults
Abbott, K. A., Burrows, T. L., Acharya, S., Thota, R. N., & Garg, M. L. (2020) · Prostaglandins Leukotrienes and Essential Fatty Acids · doi:10.1016/j.plefa.2020.102154 · Cited by 63 · see citing works
Marushka, L., Batal, M., David, W., Schwartz, H. M., Ing, A., Fediuk, K., Sharp, D., Black, A., Tikhonov, C., & Chan, H. M. (2017) · Environmental Research · doi:10.1016/j.envres.2017.04.034 · Cited by 60 · see citing works
Chang, J. P., Tseng, P., Zeng, B., Chang, C., Su, H., Chou, P., & Su, K. (2023) · Advances in Nutrition · doi:10.1016/j.advnut.2023.08.003 · Cited by 59 · see citing works
Li, D. (2015) · PubMed · doi:10.6133/apjcn.2015.24.1.21 · Cited by 58 · see citing works
Self-citationWang, F., Wang, Y., Zhu, Y., Liu, X., Xia, H., Yang, X., & Sun, G. (2016) · European Journal of Nutrition · doi:10.1007/s00394-016-1352-4 · Cited by 57 · see citing works
Gao, C., Liu, Y., Gan, Y., Bao, W., Peng, X., Xing, Q., Gao, H., Lai, J., Liu, L., Wang, Z., et al. (2020) · Lipids in Health and Disease · doi:10.1186/s12944-020-01214-w · Cited by 56 · see citing works
Chen, C., Yang, Y., Yu, X., Hu, S., & Shao, S. (2016) · Journal of Diabetes Investigation · doi:10.1111/jdi.12614 · Cited by 54 · see citing works
Zheng, J., Lin, M., Imamura, F., Cai, W., Wang, L., Feng, J., Ruan, Y., Tang, J., Wang, F., Yang, H., et al. (2016) · Scientific Reports · doi:10.1038/srep29522 · Cited by 53 · see citing works
Self-citationSadeghi, A., Djafarian, K., Mohammadi, H., & Shab‐Bidar, S. (2016) · Diabetes & Metabolic Syndrome Clinical Research & Reviews · doi:10.1016/j.dsx.2016.06.025 · Cited by 49 · see citing works
Peluso, I., Romanelli, L., & Palmery, M. (2014) · International Journal of Food Sciences and Nutrition · doi:10.3109/09637486.2014.880670 · Cited by 48 · see citing works
Zheng, J., Arnett, D. K., Lee, Y., Shen, J., Parnell, L. D., Smith, C. E., Richardson, K., Li, D., Borecki, I. B., Ordovás, J. M., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0077442 · Cited by 45 · see citing works
Self-citationFatty acids from diet and microbiota regulate energy metabolism
Alcock, J., & Lin, H. C. (2015) · F1000Research · doi:10.12688/f1000research.6078.1 · Cited by 45 · see citing works
Zhang, H., Gao, X., Guo, X., Li, K., Li, S., Sinclair, A. J., & Li, D. (2021) · Clinical Nutrition · doi:10.1016/j.clnu.2021.05.025 · Cited by 42 · see citing works
Self-citationEffect of Fatty Acids on Glucose Metabolism and Type 2 Diabetes
Sivri, D., & Akdevelıoğlu, Y. (2024) · Nutrition Reviews · doi:10.1093/nutrit/nuae165 · Cited by 40 · see citing works
Jafari, T., Fallah, A. A., & Azadbakht, L. (2013) · Maturitas · doi:10.1016/j.maturitas.2013.01.008 · Cited by 39 · see citing works
Biomarkers of Fish Oil Omega‐3 Polyunsaturated Fatty Acids Intake in Humans
Silva, V., Barazzoni, R., & Singer, P. (2013) · Nutrition in Clinical Practice · doi:10.1177/0884533613516144 · Cited by 40 · see citing works
Asadi, M., Shahzeidi, M., Nadjarzadeh, A., yusefabad, H. H., & Mansoori, A. (2019) · Nutrition & Dietetics · doi:10.1111/1747-0080.12514 · Cited by 37 · see citing works
Phospholipids from herring roe improve plasma lipids and glucose tolerance in healthy, young adults
Bjørndal, B., Strand, E., Gjerde, J., Bohov, P., Svardal, A. M., Diehl, B. W. K., Innis, S. M., Berger, A., & Berge, R. K. (2014) · Lipids in Health and Disease · doi:10.1186/1476-511x-13-82 · Cited by 37 · see citing works
Serum Lipids in Association With Type 2 Diabetes Risk and Prevalence in a Chinese Population
Lu, Y., Wang, Y., Zou, L., Xu, L., Ong, C. N., Subramaniam, T., Yuan, J., Koh, W., & Pan, A. (2017) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2017-02176 · Cited by 34 · see citing works
Breaking the cycle: the role of omega-3 polyunsaturated fatty acids in inflammation-driven cancers
Patterson, W. L., & Georgel, P. T. (2014) · Biochemistry and Cell Biology · doi:10.1139/bcb-2013-0127 · Cited by 32 · see citing works
Current level of fish and omega-3 fatty acid intakes and risk of Type 2 diabetes in China
Zhang, Y., Zhuang, P., Mao, L., Chen, X., Wang, J., Cheng, L., Ding, G., & Jiao, J. (2019) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2019.108249 · Cited by 30 · see citing works
Dow, C., Mangin, M., Balkau, B., Affret, A., Boutron‐Ruault, M., Clavel‐Chapelon, F., Bonnet, F., & Fagherazzi, G. (2016) · British Journal Of Nutrition · doi:10.1017/s0007114516003883 · Cited by 29 · see citing works
Monmai, C., Go, S. H., Shin, I.-S., You, S. G., Lee, H., Kang, S. B., & Park, W. J. (2018) · Marine Drugs · doi:10.3390/md16090309 · Cited by 29 · see citing works
Wang, J., Song, M., Bae, U., Lim, J. M., Kwon, K. S., & Park, B. (2015) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201500299 · Cited by 26 · see citing works
Mandalazi, E., Drake, I., Wirfält, E., Orho‐Melander, M., & Sonestedt, E. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17060901 · Cited by 27 · see citing works
Dietary habits associated with reduced insulin resistance: The Nagahama study
Ikeda, K., Sato, T. S., Nakayama, T., Tanaka, D., Nagashima, K., Mano-Usui, F., Joo, E., Fujimoto, S., Takahashi, Y., Kosugi, S., et al. (2018) · Diabetes Research and Clinical Practice · doi:10.1016/j.diabres.2018.04.006 · Cited by 26 · see citing works
Lipidomics in gestational diabetes mellitus
Wang, Y., Pan, X., & Pan, A. (2022) · Current Opinion in Lipidology · doi:10.1097/mol.0000000000000858 · Cited by 25 · see citing works
Eekelen, E. W.-V., Geelen, A., Alssema, M., Lamb, H. J., Roos, A., Rosendaal, F. R., & de Mutsert, R. (2018) · Journal of Nutrition · doi:10.1093/jn/nxy260 · Cited by 23 · see citing works
Sex-dependent association between erythrocyten-3 PUFA and type 2 diabetes in older overweight people
Abbott, K. A., Veysey, M. J., Lucock, M. D., Niblett, S. H., King, K., Burrows, T. L., & Garg, M. L. (2016) · British Journal Of Nutrition · doi:10.1017/s0007114516000258 · Cited by 21 · see citing works
Marushka, L., Hu, X., Batal, M., Sadik, T., Schwartz, H. M., Ing, A., Fediuk, K., Tikhonov, C., & Chan, H. M. (2018) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph15030539 · Cited by 21 · see citing works
Lee, S. M., Chung, S. H., Park, Y., Park, M. K., Son, Y. K., Kim, S. E., & An, W. S. (2015) · International Journal of Endocrinology · doi:10.1155/2015/208121 · Cited by 20 · see citing works
Ma, J., Kitaura, H., Ogawa, S., Ohori, F., Noguchi, T., Marahleh, A., Nara, Y., Pramusita, A., Kinjo, R., Kanou, K., et al. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2022.929690 · Cited by 20 · see citing works
Zheng, J., Lin, J.-S., Dong, H.-L., Zeng, F., Li, D., Song, Y., & Chen, Y. (2018) · Clinical Nutrition · doi:10.1016/j.clnu.2018.09.018 · Cited by 20 · see citing works
Self-citationDietary fat and risk of type 2 diabetes
Schlesinger, S., Schwingshackl, L., & Neuenschwander, M. (2018) · Current Opinion in Lipidology · doi:10.1097/mol.0000000000000567 · Cited by 18 · see citing works
Impact of dietary fat composition on prediabetes: a 12-year follow-up study
Krishnan, S., Steffen, L. M., Paton, C. M., & Cooper, J. A. (2017) · Public Health Nutrition · doi:10.1017/s1368980016003669 · Cited by 18 · see citing works
Marushka, L., Hu, X., Batal, M., Tikhonov, C., Sadik, T., Schwartz, H. M., Ing, A., Fediuk, K., & Chan, H. M. (2021) · Canadian Journal of Public Health · doi:10.17269/s41997-021-00484-w · Cited by 18 · see citing works
Jo, S., An, W.-S., & Park, Y. (2013) · Annals of Nutrition and Metabolism · doi:10.1159/000357018 · Cited by 18 · see citing works
Chen, G., Li, Y., Zeng, F., Deng, G., Liang, J., Wang, J., Su, Y., Chen, Y., Mao, L., Liu, Z., et al. (2020) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2020.1784839 · Cited by 17 · see citing works
Design Issues in Personalized Nutrition Advice Systems
de Hoogh, I. M., Reinders, M. J., Doets, E. L., Hoevenaars, F. P. M., & Top, J. L. (2023) · Journal of Medical Internet Research · doi:10.2196/37667 · Cited by 17 · see citing works
Monmai, C., Go, S. H., Shin, I., You, S., Kim, D., Kang, S., & Park, W. J. (2018) · Journal of Microbiology and Biotechnology · doi:10.4014/jmb.1802.03044 · Cited by 17 · see citing works
Wang, W., Zhao, R. Z., Liu, B., & Li, K. (2025) · Frontiers in Nutrition · doi:10.3389/fnut.2025.1549509 · Cited by 16 · see citing works
Effects of Intake of Fish or Fish Oils on the Development of Diabetes
Yanai, H., Hamasaki, H., Katsuyama, H., Adachi, H., Moriyama, S., & Sako, A. (2014) · Journal of Clinical Medicine Research · doi:10.14740/jocmr1964w · Cited by 16 · see citing works
Zhuang, P., Wang, W., Wang, J., Zhang, Y., & Jiao, J. (2018) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201700898 · Cited by 16 · see citing works
Zhang, W., Gan, D., Huo, S., & Chen, P. (2024) · Frontiers in Nutrition · doi:10.3389/fnut.2024.1490953 · Cited by 14 · see citing works
Zheng, J., Huang, T., Li, K., Chen, Y., Xie, H., Xu, D., Sun, J., & Li, D. (2015) · Lifestyle Genomics · doi:10.1159/000381348 · Cited by 14 · see citing works
Self-citationProspects in development of quality rice for human nutrition
Se, C., Khor, B., & Karupaiah, T. (2015) · Cited by 13 · see citing works
Delarue, J., Allain, G., Guillerm, S., Cruciani‐Guglielmacci, C., Magnan, C., Moineau, M., & Guen, V. L. (2016) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201500469 · Cited by 14 · see citing works
Monmai, C., Jang, A.-Y., Kim, J., Lee, S.-M., You, S., Kang, S., & Park, W. J. (2020) · Journal of Microbiology and Biotechnology · doi:10.4014/jmb.2007.07032 · Cited by 12 · see citing works
Gishini, M. F. S., Zebarjadi, A., Abdoli-Nasab, M., Javaran, M. J., Kahrizi, D., & Hildebrand, D. F. (2019) · Functional & Integrative Genomics · doi:10.1007/s10142-019-00718-8 · Cited by 11 · see citing works
Pastorino, S., Bishop, T. R. P., Sharp, S. J., Pearce, M., Akbaraly, T. N., Barbieri, N. B., Bes‐Rastrollo, M., Beulens, J. W. J., Chen, Z., Du, H., et al. (2021) · Nutrients · doi:10.3390/nu13041223 · Cited by 11 · see citing works
A plasma fatty acid profile associated to type 2 diabetes development: from the CORDIOPREV study
Villasanta‐Gonzalez, A., Alcala-Diaz, J. F., Vals‐Delgado, C., Arenas, A. P., Cardelo, M. P., Romero‐Cabrera, J. L., Rodríguez-Cantalejo, F., Delgado‐Lista, J., Malagón, M. M., Pérez‐Martínez, P., et al. (2021) · European Journal of Nutrition · doi:10.1007/s00394-021-02676-z · Cited by 10 · see citing works
Do statins increase and Mediterranean diet decrease the risk of breast cancer?
de Lorgeril, M., & Salen, P. (2014) · BMC Medicine · doi:10.1186/1741-7015-12-94 · Cited by 10 · see citing works
Zheng, J., Lai, C., Parnell, L. D., Lee, Y., Shen, J., Smith, C. E., Casas‐Agustench, P., Richardson, K., Li, D., Noel, S. E., et al. (2014) · BMC Genomics · doi:10.1186/1471-2164-15-781 · Cited by 10 · see citing works
Self-citationKuang, X., Shao, X., Li, H., Jiang, D., Gao, T., Yang, J., Li, K., & Li, D. (2022) · Journal of the Science of Food and Agriculture · doi:10.1002/jsfa.12346 · Cited by 11 · see citing works
Self-citationZheng, J., Arnett, D. K., Parnell, L. D., Lee, Y., Ma, Y., Smith, C. E., Richardson, K., Li, D., Borecki, I. B., Tucker, K. L., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0067394 · Cited by 9 · see citing works
Self-citationThe Biochemistry and Regulation of Fatty Acid Desaturases in Animals
Park, W. J. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-811230-4.00005-3 · Cited by 9 · see citing works
Fish consumption is inversely associated with type 2 diabetes in Manitoba First Nations communities
Marushka, L., Batal, M., Sharp, D., Schwartz, H. M., Ing, A., Fediuk, K., Black, A., Tikhonov, C., & Chan, H. M. (2017) · FACETS · doi:10.1139/facets-2017-0023 · Cited by 8 · see citing works
Lifestyle Genomics: Addressing the Multifactorial Nature of Personalized Health
Mutch, D. M., Zulyniak, M. A., Rudkowska, I., & Tejero, M. E. (2018) · Lifestyle Genomics · doi:10.1159/000492297 · Cited by 8 · see citing works
Patel, N., Dinesh, S., & Sharma, S. (2023) · Current Diabetes Reviews · doi:10.2174/0115733998266653231005072450 · Cited by 7 · see citing works
Urla, R., Kumar, P. P., Prabhakar, S., Khareedu, V. R., & Vudem, D. R. (2017) · Plant Biotechnology Reports · doi:10.1007/s11816-017-0450-y · Cited by 7 · see citing works
Li, K., Wu, K., Zhao, Y., Huang, T., Lou, D.-J., Yu, X., & Li, D. (2015) · Marine Drugs · doi:10.3390/md13095564 · Cited by 6 · see citing works
Self-citationBroadhurst, C. L., Schmidt, W., Nguyen, J. K., Qin, J., Chao, K., & Kim, M. S. (2018) · Journal of Biophysical Chemistry · doi:10.4236/jbpc.2018.91001 · Cited by 6 · see citing works
Bakre, A. T., Chen, A., Tao, X. G., Hou, J., Yao, Y., Nevill, A. M., Tang, J. J., Rohrmann, S., Ni, J., Hu, Z., et al. (2022) · European Journal of Nutrition · doi:10.1007/s00394-022-02887-y · Cited by 6 · see citing works
Health effects of omega-3 polyunsaturated fatty acids in common diseases
Jia, G., Qiong, Z., & Yonghua, W. (2021) · International Food Research Journal · doi:10.47836/ifrj.28.6.01 · Cited by 6 · see citing works
n-3 Polyunsaturated Fatty Acids in Type 2 Diabetes Mellitus
Valdés‐Ramos, R., López, A. L. G., Martínez‐Carrillo, B. E., & Harbige, L. S. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-813822-9.00013-8 · Cited by 6 · see citing works
Musazadeh, V., Mahmoudinezhad, M., Pam, P., Brazandeh, S., Faramarzi, F., Mohammadpour, Y., Faghfouri, A. H., & Gheibi, S. (2025) · Nutrition & Metabolism · doi:10.1186/s12986-025-00952-x · Cited by 5 · see citing works
DHA- and EPA-rich oil from microalgae
Lupette, J. (2023) · Elsevier eBooks · doi:10.1016/b978-0-323-99196-4.00035-8 · Cited by 5 · see citing works
Box–Behnken modeling of biodiesel production from Botryococcus braunii microalgae
Hassaan, M. A., Abdelaziz, N. I. M., Nazir, M. A., Jamshaid, M., Hassouna, M. S. E.-D., & Nemr, A. E. (2024) · Biofuels Bioproducts and Biorefining · doi:10.1002/bbb.2626 · Cited by 5 · see citing works
Liu, X., Gu, Y., Zhou, Y., Zhang, R., & Koyama, T. (2024) · Molecules · doi:10.3390/molecules29246000 · Cited by 5 · see citing works
Fish consumption and omega-3-fatty acids in prevention of diet-related noncommunicable diseases
Jacob, J. J. (2016) · Journal of Social Health and Diabetes · doi:10.4103/2321-0656.187989 · Cited by 5 · see citing works
The Health Impact of Eating Foods of Animal Origin
Marsh, K. A., Saunders, A. V., & Zeuschner, C. L. (2018) · Advances in marketing, customer relationship management, and e-services book series · doi:10.4018/978-1-5225-4757-0.ch002 · Cited by 5 · see citing works
Dietary fish intake and the risk for type 2 diabetes and cardiovascular disease
Kröger, J., & Schulze, M. B. (2014) · Current Opinion in Lipidology · doi:10.1097/mol.0000000000000078 · Cited by 5 · see citing works
Meat Food Group Intakes and the Risk of Type 2 Diabetes Incidence
Hosseini‐Esfahani, F., Beheshti, N., Koochakpoor, G., Mirmiran, P., & Azizi, F. (2022) · Frontiers in Nutrition · doi:10.3389/fnut.2022.891111 · Cited by 4 · see citing works
Li, K., Huang, T., Zheng, J., Sun, J., Chen, Y., Xie, H., Xu, D.-F., Wan, J., & Li, D. (2014) · Lifestyle Genomics · doi:10.1159/000381347 · Cited by 4 · see citing works
Self-citationBjørndal, B., Berge, K., Barger, J. L., Berge, R. K., & Burri, L. (2013) · Journal of Functional Foods · doi:10.1016/j.jff.2013.11.003 · Cited by 4 · see citing works
Li, Y., Sun, T., Wu, Y., Li, C., Ling, C.-Y., Zeng, F., & Chen, Y. (2020) · International Journal of Obesity · doi:10.1038/s41366-020-0569-8 · Cited by 4 · see citing works
Are marine n-3 fatty acids protective towards insulin resistance? From cell to human
Delarue, J. (2020) · Proceedings of The Nutrition Society · doi:10.1017/s0029665120000087 · Cited by 4 · see citing works
- Authors
- Zheng, J.-S., Huang, T., Yang, J., Fu, Y.-Q., & Li, D.
- Affiliations
- Zhejiang University (CN)
- Corresponding author
- Li, Duo
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2012-09-11
- Volume
- 7
- Issue
- 9
- Pages
- e44525
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC3439396
- OpenAlex
- W2074950966
- Cited by
- 126
- References
- 57
- Citations by year
- 2025: 6 · 2024: 8 · 2023: 5 · 2022: 6 · 2021: 8 · 2020: 8 · 2019: 8 · 2018: 17 · 2017: 6 · 2016: 19 · 2015: 11 · 2014: 12 · 2013: 12
- FWCI
- 1.37
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Funders
- National Natural Science Foundation of China (973 Program, 2011CB504002, 30972464)
- National Key Research and Development Program of China (30972464, 2011CB504002)
- Topics
- Health Sciences › Nursing › Nutrition and Dietetics › Fatty Acid Research and Health
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Nutritional Studies and Diet
- Life Sciences › Agricultural and Biological Sciences › Aquatic Science › Aquaculture Nutrition and Growth
- Keywords
- type 2 diabetes, omega-3 fatty acids, marine fatty acids, fish consumption, alpha-linolenic acid, dietary intake, tissue fatty acid composition, Asian populations, Western populations, docosahexaenoic acid, EPA, diabetes risk, prospective cohort, subgroup analysis by ethnicity, omega-3 supplementation, diabetes remission, glycemic control
- MeSH terms
- Adult, Aged, Animals, Diabetes Mellitus, Type 2, Diet, Female, Fish Oils, Humans, Male, Middle Aged, Prospective Studies, Risk, Cohort Studies, Fatty Acids, Omega-3, Case-Control Studies, Asian People
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
