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Published in: Cardiovascular Diabetology 1/2018

Open Access 01-12-2018 | Review

Omega-3 polyunsaturated fatty acids favourably modulate cardiometabolic biomarkers in type 2 diabetes: a meta-analysis and meta-regression of randomized controlled trials

Authors: Lauren L. O’Mahoney, Jamie Matu, Oliver J. Price, Karen M. Birch, Ramzi A. Ajjan, Diane Farrar, Robyn Tapp, Daniel J. West, Kevin Deighton, Matthew D. Campbell

Published in: Cardiovascular Diabetology | Issue 1/2018

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Abstract

Background

Randomized controlled trials (RCTs) suggest that supplementation with omega-3 polyunsaturated fatty acids (n-3PUFAs) may favourably modify cardiometabolic biomarkers in type 2 diabetes (T2DM). Previous meta-analyses are limited by insufficient sample sizes and omission of meta-regression techniques, and a large number of RCTs have subsequently been published since the last comprehensive meta-analysis. Updated information regarding the impact of dosage, duration or an interaction between these two factors is therefore warranted. The objective was to comprehensively assess the effect of n-3PUFAs supplementation on cardiometabolic biomarkers including lipid profiles, inflammatory parameters, blood pressure, and indices of glycaemic control, in people with T2DM, and identify whether treatment dosage, duration or an interaction thereof modify these effects.

Methods

Databases including PubMed and MEDLINE were searched until 13th July 2017 for RCTs investigating the effect of n-3PUFAs supplementation on lipid profiles, inflammatory parameters, blood pressure, and indices of glycaemic control. Data were pooled using random-effects meta-analysis and presented as standardised mean difference (Hedges g) with 95% confidence intervals (95% CI). Meta-regression analysis was performed to investigate the effects of duration of supplementation and total dosage of n-3PUFAs as moderator variables where appropriate.

Results

A total of 45 RCTs were identified, involving 2674 people with T2DM. n-3PUFAs supplementation was associated with significant reductions in LDL [ES: − 0.10, (95% CI − 0.17, − 0.03); p = 0.007], VLDL (ES: − 0.26 (− 0.51, − 0.01); p = 0.044], triglycerides (ES: − 0.39 (− 0.55, − 0.24; p ≤ 0.001] and HbA1c (ES: − 0.27 (− 0.48, − 0.06); p = 0.010]. Moreover, n-3PUFAs supplementation was associated with reduction in plasma levels of TNF-α [ES: − 0.59 (− 1.17, − 0.01); p = 0.045] and IL-6 (ES: − 1.67 (− 3.14, − 0.20); p = 0.026]. All other lipid markers, indices of glycaemic control, inflammatory parameters, and blood pressure remained unchanged (p > 0.05).

Conclusions

n-3PUFAs supplementation produces favourable hypolipidemic effects, a reduction in pro-inflammatory cytokine levels and improvement in glycaemia. Neither duration nor dosage appear to explain the observed heterogeneity in response to n-3PUFAs.
Trial registration This trial was registered at http://​www.​crd.​york.​ac.​uk as CRD42016050802
Appendix
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Literature
1.
go back to reference Morrish NJ, Wang SL, Stevens LK, Fuller JH, Keen H. Mortality and causes of death in the WHO multinational study of vascular disease in diabetes. Diabetologia. 2001;44(Suppl 2):14–21.CrossRef Morrish NJ, Wang SL, Stevens LK, Fuller JH, Keen H. Mortality and causes of death in the WHO multinational study of vascular disease in diabetes. Diabetologia. 2001;44(Suppl 2):14–21.CrossRef
2.
go back to reference Holman RR, Paul SK, Bethel MA, Matthews DR, Neil HA. 10-year follow-up of intensive glucose control in type 2 diabetes. N Engl J Med. 2008;359:1577–89.CrossRefPubMed Holman RR, Paul SK, Bethel MA, Matthews DR, Neil HA. 10-year follow-up of intensive glucose control in type 2 diabetes. N Engl J Med. 2008;359:1577–89.CrossRefPubMed
3.
go back to reference Action to Control Cardiovascular Risk in Diabetes Study Group, Gerstein HC, Miller ME, Byington RP, Goff DC Jr, Bigger JT, Buse JB, Cushman WC, Genuth S, Ismail-Beigi F, et al. Effects of intensive glucose lowering in type 2 diabetes. N Engl J Med. 2008;358:2545–59.CrossRef Action to Control Cardiovascular Risk in Diabetes Study Group, Gerstein HC, Miller ME, Byington RP, Goff DC Jr, Bigger JT, Buse JB, Cushman WC, Genuth S, Ismail-Beigi F, et al. Effects of intensive glucose lowering in type 2 diabetes. N Engl J Med. 2008;358:2545–59.CrossRef
4.
go back to reference Advance Collaborative Group, Patel A, MacMahon S, Chalmers J, Neal B, Billot L, Woodward M, Marre M, Cooper M, Glasziou P, et al. Intensive blood glucose control and vascular outcomes in patients with type 2 diabetes. N Engl J Med. 2008;358:2560–72.CrossRef Advance Collaborative Group, Patel A, MacMahon S, Chalmers J, Neal B, Billot L, Woodward M, Marre M, Cooper M, Glasziou P, et al. Intensive blood glucose control and vascular outcomes in patients with type 2 diabetes. N Engl J Med. 2008;358:2560–72.CrossRef
5.
go back to reference Kirkman MS, Mahmud H, Korytkowski MT. Intensive blood glucose control and vascular outcomes in patients with type 2 diabetes mellitus. Endocrinol Metab Clin North Am. 2018;47:81–96.CrossRefPubMed Kirkman MS, Mahmud H, Korytkowski MT. Intensive blood glucose control and vascular outcomes in patients with type 2 diabetes mellitus. Endocrinol Metab Clin North Am. 2018;47:81–96.CrossRefPubMed
6.
go back to reference UK Prospective Diabetes Study. UKPDS) Group. Intensive blood-glucose control with sulphonylureas or insulin compared with conventional treatment and risk of complications in patients with type 2 diabetes (UKPDS 33. Lancet. 1998;352:837–53.CrossRef UK Prospective Diabetes Study. UKPDS) Group. Intensive blood-glucose control with sulphonylureas or insulin compared with conventional treatment and risk of complications in patients with type 2 diabetes (UKPDS 33. Lancet. 1998;352:837–53.CrossRef
7.
go back to reference Abdul-Ghani M, DeFronzo RA, Del Prato S, Chilton R, Singh R, Ryder REJ. Cardiovascular disease and type 2 diabetes: has the Dawn of a New Era arrived? Diabetes Care. 2017;40:813–20.CrossRefPubMedPubMedCentral Abdul-Ghani M, DeFronzo RA, Del Prato S, Chilton R, Singh R, Ryder REJ. Cardiovascular disease and type 2 diabetes: has the Dawn of a New Era arrived? Diabetes Care. 2017;40:813–20.CrossRefPubMedPubMedCentral
8.
go back to reference Lamichhane AP, Crandell JL, Jaacks LM, Couch SC, Lawrence JM, Mayer-Davis EJ. Longitudinal associations of nutritional factors with glycated hemoglobin in youth with type 1 diabetes: the SEARCH Nutrition Ancillary Study. Am J Clin Nutr. 2015;101:1278–85.CrossRefPubMedPubMedCentral Lamichhane AP, Crandell JL, Jaacks LM, Couch SC, Lawrence JM, Mayer-Davis EJ. Longitudinal associations of nutritional factors with glycated hemoglobin in youth with type 1 diabetes: the SEARCH Nutrition Ancillary Study. Am J Clin Nutr. 2015;101:1278–85.CrossRefPubMedPubMedCentral
9.
go back to reference Micha R, Penalvo JL, Cudhea F, Imamura F, Rehm CD, Mozaffarian D. Association between dietary factors and mortality from heart disease, stroke, and type 2 diabetes in the United States. JAMA. 2017;317:912–24.CrossRefPubMedPubMedCentral Micha R, Penalvo JL, Cudhea F, Imamura F, Rehm CD, Mozaffarian D. Association between dietary factors and mortality from heart disease, stroke, and type 2 diabetes in the United States. JAMA. 2017;317:912–24.CrossRefPubMedPubMedCentral
10.
go back to reference Bang HO, Dyerberg J, Nielsen AB. Plasma lipid and lipoprotein pattern in Greenlandic West-coast Eskimos. Lancet. 1971;1:1143–5.CrossRefPubMed Bang HO, Dyerberg J, Nielsen AB. Plasma lipid and lipoprotein pattern in Greenlandic West-coast Eskimos. Lancet. 1971;1:1143–5.CrossRefPubMed
11.
12.
go back to reference Harris WS. n-3 fatty acids and serum lipoproteins: human studies. Am J Clin Nutr. 1997;65(Suppl 5):1645–54.CrossRef Harris WS. n-3 fatty acids and serum lipoproteins: human studies. Am J Clin Nutr. 1997;65(Suppl 5):1645–54.CrossRef
13.
go back to reference Sawada T, Tsubata H, Hashimoto N, Takabe M, Miyata T, Aoki K, Yamashita S, Oishi S, Osue T, Yokoi K, et al. Effects of 6-month eicosapentaenoic acid treatment on postprandial hyperglycemia, hyperlipidemia, insulin secretion ability, and concomitant endothelial dysfunction among newly-diagnosed impaired glucose metabolism patients with coronary artery disease. An open label, single blinded, prospective randomized controlled trial. Cardiovasc Diabetol. 2016;15:121.CrossRefPubMedPubMedCentral Sawada T, Tsubata H, Hashimoto N, Takabe M, Miyata T, Aoki K, Yamashita S, Oishi S, Osue T, Yokoi K, et al. Effects of 6-month eicosapentaenoic acid treatment on postprandial hyperglycemia, hyperlipidemia, insulin secretion ability, and concomitant endothelial dysfunction among newly-diagnosed impaired glucose metabolism patients with coronary artery disease. An open label, single blinded, prospective randomized controlled trial. Cardiovasc Diabetol. 2016;15:121.CrossRefPubMedPubMedCentral
14.
go back to reference Jacobo-Cejudo MG, Valdes-Ramos R, Guadarrama-Lopez AL, Pardo-Morales RV, Martinez-Carrillo BE, Harbige LS. Effect of n-3 polyunsaturated fatty acid supplementation on metabolic and inflammatory biomarkers in type 2 diabetes mellitus patients. Nutrients. 2017;9:573.CrossRefPubMedCentral Jacobo-Cejudo MG, Valdes-Ramos R, Guadarrama-Lopez AL, Pardo-Morales RV, Martinez-Carrillo BE, Harbige LS. Effect of n-3 polyunsaturated fatty acid supplementation on metabolic and inflammatory biomarkers in type 2 diabetes mellitus patients. Nutrients. 2017;9:573.CrossRefPubMedCentral
15.
go back to reference Fayh APT, Borges K, Cunha GS, Krause M, Rocha R, de Bittencourt PIH, Moreira JCF, Friedman R, da Silva Rossato J, Fernandes JR, et al. Effects of n-3 fatty acids and exercise on oxidative stress parameters in type 2 diabetic: a randomized clinical trial. J Int Soc Sports Nutr. 2018;15:18.CrossRefPubMedPubMedCentral Fayh APT, Borges K, Cunha GS, Krause M, Rocha R, de Bittencourt PIH, Moreira JCF, Friedman R, da Silva Rossato J, Fernandes JR, et al. Effects of n-3 fatty acids and exercise on oxidative stress parameters in type 2 diabetic: a randomized clinical trial. J Int Soc Sports Nutr. 2018;15:18.CrossRefPubMedPubMedCentral
16.
go back to reference Poreba M, Mostowik M, Siniarski A, Golebiowska-Wiatrak R, Malinowski KP, Haberka M, Konduracka E, Nessler J, Undas A, Gajos G. Treatment with high-dose n-3PUFAs has no effect on platelet function, coagulation, metabolic status or inflammation in patients with atherosclerosis and type 2 diabetes. Cardiovasc Diabetol. 2017;16:50.CrossRefPubMedPubMedCentral Poreba M, Mostowik M, Siniarski A, Golebiowska-Wiatrak R, Malinowski KP, Haberka M, Konduracka E, Nessler J, Undas A, Gajos G. Treatment with high-dose n-3PUFAs has no effect on platelet function, coagulation, metabolic status or inflammation in patients with atherosclerosis and type 2 diabetes. Cardiovasc Diabetol. 2017;16:50.CrossRefPubMedPubMedCentral
18.
go back to reference Hartweg J, Farmer AJ, Perera R, Holman RR, Neil HA. Meta-analysis of the effects of n-3 polyunsaturated fatty acids on lipoproteins and other emerging lipid cardiovascular risk markers in patients with type 2 diabetes. Diabetologia. 2007;50:1593–602.CrossRefPubMed Hartweg J, Farmer AJ, Perera R, Holman RR, Neil HA. Meta-analysis of the effects of n-3 polyunsaturated fatty acids on lipoproteins and other emerging lipid cardiovascular risk markers in patients with type 2 diabetes. Diabetologia. 2007;50:1593–602.CrossRefPubMed
20.
go back to reference Hartweg J, Farmer AJ, Holman RR, Neil A. Potential impact of omega-3 treatment on cardiovascular disease in type 2 diabetes. Curr Opin Lipidol. 2009;20:30–8.CrossRefPubMed Hartweg J, Farmer AJ, Holman RR, Neil A. Potential impact of omega-3 treatment on cardiovascular disease in type 2 diabetes. Curr Opin Lipidol. 2009;20:30–8.CrossRefPubMed
21.
go back to reference Chen C, Yu X, Shao S. Effects of omega-3 fatty acid supplementation on glucose control and lipid levels in type 2 diabetes: a meta-analysis. PLoS ONE. 2015;10:1–14. Chen C, Yu X, Shao S. Effects of omega-3 fatty acid supplementation on glucose control and lipid levels in type 2 diabetes: a meta-analysis. PLoS ONE. 2015;10:1–14.
22.
go back to reference Jump DB, Depner CM, Tripathy S. Omega-3 fatty acid supplementation and cardiovascular disease: thematic review series: new lipid and lipoprotein targets for the treatment of cardiometabolic diseases. J Lipid Res. 2012;53:2525–45.CrossRefPubMedPubMedCentral Jump DB, Depner CM, Tripathy S. Omega-3 fatty acid supplementation and cardiovascular disease: thematic review series: new lipid and lipoprotein targets for the treatment of cardiometabolic diseases. J Lipid Res. 2012;53:2525–45.CrossRefPubMedPubMedCentral
23.
go back to reference Fox CS, Golden SH, Anderson C, Bray GA, Burke LE, de Boer IH, Deedwania P, Eckel RH, Ershow AG, Fradkin J, et al. Update on prevention of cardiovascular disease in adults with type 2 diabetes mellitus in light of recent evidence: a scientific statement from the american heart association and the american diabetes association. Diabetes Care. 2015;38:1777–803.CrossRefPubMedPubMedCentral Fox CS, Golden SH, Anderson C, Bray GA, Burke LE, de Boer IH, Deedwania P, Eckel RH, Ershow AG, Fradkin J, et al. Update on prevention of cardiovascular disease in adults with type 2 diabetes mellitus in light of recent evidence: a scientific statement from the american heart association and the american diabetes association. Diabetes Care. 2015;38:1777–803.CrossRefPubMedPubMedCentral
24.
go back to reference Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gøtzsche PC, Ioannidis JPA, Clarke M, Devereaux PJ, Kleijnen J, Moher D. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: explanation and elaboration. BMJ. 2009;339:b2700.CrossRefPubMedPubMedCentral Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gøtzsche PC, Ioannidis JPA, Clarke M, Devereaux PJ, Kleijnen J, Moher D. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: explanation and elaboration. BMJ. 2009;339:b2700.CrossRefPubMedPubMedCentral
25.
go back to reference Higgins JPT, Altman DG, Gøtzsche PC, Jüni P, Moher D, Oxman AD, Savović J, Schulz KF, Weeks L, Sterne JAC. The Cochrane Collaboration’s tool for assessing risk of bias in randomised trials. BMJ. 2011;343:d5928.CrossRefPubMedPubMedCentral Higgins JPT, Altman DG, Gøtzsche PC, Jüni P, Moher D, Oxman AD, Savović J, Schulz KF, Weeks L, Sterne JAC. The Cochrane Collaboration’s tool for assessing risk of bias in randomised trials. BMJ. 2011;343:d5928.CrossRefPubMedPubMedCentral
26.
go back to reference Wan X, Wang W, Liu J, Tong T. Estimating the sample mean and standard deviation from the sample size, median, range and/or interquartile range. BMC Med Res Methodol. 2014;14:135.CrossRefPubMedPubMedCentral Wan X, Wang W, Liu J, Tong T. Estimating the sample mean and standard deviation from the sample size, median, range and/or interquartile range. BMC Med Res Methodol. 2014;14:135.CrossRefPubMedPubMedCentral
27.
go back to reference Borenstein M, Hedges LV, Higgins JP, Rothstein HR. Introduction to meta-analysis. 1st ed. West Sussex: Wiley; 2009.CrossRef Borenstein M, Hedges LV, Higgins JP, Rothstein HR. Introduction to meta-analysis. 1st ed. West Sussex: Wiley; 2009.CrossRef
28.
go back to reference Faraone SV. Interpreting estimates of treatment effects: implications for managed care. P T PeerRev J Formul Manag. 2008;33:700–11. Faraone SV. Interpreting estimates of treatment effects: implications for managed care. P T PeerRev J Formul Manag. 2008;33:700–11.
29.
go back to reference Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med. 2002;21:1539–58.CrossRefPubMed Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med. 2002;21:1539–58.CrossRefPubMed
30.
go back to reference Mozaffarian D, Rimm EB. Fish intake, contaminants, and human health: evaluating the risks and the benefits. JAMA. 2006;296:1885–99.CrossRefPubMed Mozaffarian D, Rimm EB. Fish intake, contaminants, and human health: evaluating the risks and the benefits. JAMA. 2006;296:1885–99.CrossRefPubMed
31.
go back to reference Kris-Etherton PM, Harris WS, Appel LJ, American Heart Association. Nutrition C. Fish consumption, fish oil, omega-3 fatty acids, and cardiovascular disease. Circulation. 2002;106:2747–57.CrossRefPubMed Kris-Etherton PM, Harris WS, Appel LJ, American Heart Association. Nutrition C. Fish consumption, fish oil, omega-3 fatty acids, and cardiovascular disease. Circulation. 2002;106:2747–57.CrossRefPubMed
32.
go back to reference Shearer GC, Savinova OV, Harris WS. Fish oil—how does it reduce plasma triglycerides? Biochim Biophys Acta. 2012;1821:843–51.CrossRefPubMed Shearer GC, Savinova OV, Harris WS. Fish oil—how does it reduce plasma triglycerides? Biochim Biophys Acta. 2012;1821:843–51.CrossRefPubMed
33.
go back to reference Harris WS, Miller M, Tighe AP, Davidson MH, Schaefer EJ. Omega-3 fatty acids and coronary heart disease risk: clinical and mechanistic perspectives. Atherosclerosis. 2008;197:12–24.CrossRefPubMed Harris WS, Miller M, Tighe AP, Davidson MH, Schaefer EJ. Omega-3 fatty acids and coronary heart disease risk: clinical and mechanistic perspectives. Atherosclerosis. 2008;197:12–24.CrossRefPubMed
34.
go back to reference Adkins Y, Kelley DS. Mechanisms underlying the cardioprotective effects of omega-3 polyunsaturated fatty acids. J Nutr Biochem. 2010;21:781–92.CrossRefPubMed Adkins Y, Kelley DS. Mechanisms underlying the cardioprotective effects of omega-3 polyunsaturated fatty acids. J Nutr Biochem. 2010;21:781–92.CrossRefPubMed
35.
go back to reference Sandhu PK, Musaad SM, Remaley AT, Buehler SS, Strider S, Derzon JH, Vesper HW, Ranne A, Shaw CS, Christenson RH. Lipoprotein biomarkers and risk of cardiovascular disease: a laboratory medicine best practices (LMBP) systematic review. J Appl Lab Med. 2016;1:214–29.PubMedPubMedCentralCrossRef Sandhu PK, Musaad SM, Remaley AT, Buehler SS, Strider S, Derzon JH, Vesper HW, Ranne A, Shaw CS, Christenson RH. Lipoprotein biomarkers and risk of cardiovascular disease: a laboratory medicine best practices (LMBP) systematic review. J Appl Lab Med. 2016;1:214–29.PubMedPubMedCentralCrossRef
36.
go back to reference Wadhera RK, Steen DL, Khan I, Giugliano RP, Foody JM. A review of low-density lipoprotein cholesterol, treatment strategies, and its impact on cardiovascular disease morbidity and mortality. J Clin Lipidol. 2016;10:472–89.CrossRefPubMed Wadhera RK, Steen DL, Khan I, Giugliano RP, Foody JM. A review of low-density lipoprotein cholesterol, treatment strategies, and its impact on cardiovascular disease morbidity and mortality. J Clin Lipidol. 2016;10:472–89.CrossRefPubMed
37.
go back to reference Stone NJ, Robinson JG, Lichtenstein AH, Bairey Merz CN, Blum CB, Eckel RH, Goldberg AC, Gordon D, Levy D, Lloyd-Jones DM, et al. 2013 ACC/AHA guideline on the treatment of blood cholesterol to reduce atherosclerotic cardiovascular risk in adults: a report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines. J Am Coll Cardiol. 2014;63:2889–934.CrossRefPubMed Stone NJ, Robinson JG, Lichtenstein AH, Bairey Merz CN, Blum CB, Eckel RH, Goldberg AC, Gordon D, Levy D, Lloyd-Jones DM, et al. 2013 ACC/AHA guideline on the treatment of blood cholesterol to reduce atherosclerotic cardiovascular risk in adults: a report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines. J Am Coll Cardiol. 2014;63:2889–934.CrossRefPubMed
38.
go back to reference Bradberry JC, Hilleman DE. Overview of omega-3 fatty acid therapies. Pharm Ther. 2013;38:681–91. Bradberry JC, Hilleman DE. Overview of omega-3 fatty acid therapies. Pharm Ther. 2013;38:681–91.
39.
go back to reference Emerging Risk Factors Collaboration, Kaptoge S, Di Angelantonio E, Lowe G, Pepys MB, Thompson SG, Collins R, Danesh J. C-reactive protein concentration and risk of coronary heart disease, stroke, and mortality: an individual participant meta-analysis. Lancet. 2010;375:132–40.CrossRef Emerging Risk Factors Collaboration, Kaptoge S, Di Angelantonio E, Lowe G, Pepys MB, Thompson SG, Collins R, Danesh J. C-reactive protein concentration and risk of coronary heart disease, stroke, and mortality: an individual participant meta-analysis. Lancet. 2010;375:132–40.CrossRef
40.
go back to reference Mirza S, Hossain M, Mathews C, Martinez P, Pino P, Gay JL, Rentfro A, McCormick JB, Fisher-Hoch SP. Type 2-diabetes is associated with elevated levels of TNF-alpha, IL-6 and adiponectin and low levels of leptin in a population of Mexican Americans: a cross-sectional study. Cytokine. 2012;57:136–42.CrossRefPubMed Mirza S, Hossain M, Mathews C, Martinez P, Pino P, Gay JL, Rentfro A, McCormick JB, Fisher-Hoch SP. Type 2-diabetes is associated with elevated levels of TNF-alpha, IL-6 and adiponectin and low levels of leptin in a population of Mexican Americans: a cross-sectional study. Cytokine. 2012;57:136–42.CrossRefPubMed
41.
go back to reference Tuttle HA, Davis-Gorman G, Goldman S, Copeland JG, McDonagh PF. Proinflammatory cytokines are increased in type 2 diabetic women with cardiovascular disease. J Diabetes Complications. 2004;18:343–51.CrossRefPubMed Tuttle HA, Davis-Gorman G, Goldman S, Copeland JG, McDonagh PF. Proinflammatory cytokines are increased in type 2 diabetic women with cardiovascular disease. J Diabetes Complications. 2004;18:343–51.CrossRefPubMed
42.
go back to reference Collaboration Emerging Risk Factors, Kaptoge S, Di Angelantonio E, Pennells L, Wood AM, White IR, Gao P, Walker M, Thompson A, Sarwar N, et al. C-reactive protein, fibrinogen, and cardiovascular disease prediction. N Engl J Med. 2012;367:1310–20.CrossRef Collaboration Emerging Risk Factors, Kaptoge S, Di Angelantonio E, Pennells L, Wood AM, White IR, Gao P, Walker M, Thompson A, Sarwar N, et al. C-reactive protein, fibrinogen, and cardiovascular disease prediction. N Engl J Med. 2012;367:1310–20.CrossRef
43.
go back to reference Donath MY. Targeting inflammation in the treatment of type 2 diabetes: time to start. Nat Rev Drug Discov. 2014;13:465–76.CrossRefPubMed Donath MY. Targeting inflammation in the treatment of type 2 diabetes: time to start. Nat Rev Drug Discov. 2014;13:465–76.CrossRefPubMed
45.
46.
go back to reference Hotamisligil GS, Shargill NS, Spiegelman BM. Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance. Science. 1993;259:87–91.CrossRefPubMed Hotamisligil GS, Shargill NS, Spiegelman BM. Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance. Science. 1993;259:87–91.CrossRefPubMed
47.
go back to reference Montane J, Cadavez L, Novials A. Stress and the inflammatory process: a major cause of pancreatic cell death in type 2 diabetes. Diabetes Metab Syndr Obes. 2014;7:25–34.PubMedPubMedCentral Montane J, Cadavez L, Novials A. Stress and the inflammatory process: a major cause of pancreatic cell death in type 2 diabetes. Diabetes Metab Syndr Obes. 2014;7:25–34.PubMedPubMedCentral
48.
go back to reference Glauber H, Wallace P, Griver K, Brechtel G. Adverse metabolic effect of omega-3 fatty acids in non-insulin-dependent diabetes mellitus. Ann Intern Med. 1988;108:663–8.CrossRefPubMed Glauber H, Wallace P, Griver K, Brechtel G. Adverse metabolic effect of omega-3 fatty acids in non-insulin-dependent diabetes mellitus. Ann Intern Med. 1988;108:663–8.CrossRefPubMed
51.
go back to reference Rice HB, Bernasconi A, Maki KC, Harris WS, von Schacky C, Calder PC. Conducting omega-3 clinical trials with cardiovascular outcomes: Proceedings of a workshop held at ISSFAL 2014. Prostaglandins Leukot Essent Fatty Acids. 2016;107:30–42. Rice HB, Bernasconi A, Maki KC, Harris WS, von Schacky C, Calder PC. Conducting omega-3 clinical trials with cardiovascular outcomes: Proceedings of a workshop held at ISSFAL 2014. Prostaglandins Leukot Essent Fatty Acids. 2016;107:30–42.
52.
go back to reference Harris WS. Assessing fatty acid biostatus: red blood cells or plasma? Lipid Technol. 2013;25:179–81.CrossRef Harris WS. Assessing fatty acid biostatus: red blood cells or plasma? Lipid Technol. 2013;25:179–81.CrossRef
Metadata
Title
Omega-3 polyunsaturated fatty acids favourably modulate cardiometabolic biomarkers in type 2 diabetes: a meta-analysis and meta-regression of randomized controlled trials
Authors
Lauren L. O’Mahoney
Jamie Matu
Oliver J. Price
Karen M. Birch
Ramzi A. Ajjan
Diane Farrar
Robyn Tapp
Daniel J. West
Kevin Deighton
Matthew D. Campbell
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Cardiovascular Diabetology / Issue 1/2018
Electronic ISSN: 1475-2840
DOI
https://doi.org/10.1186/s12933-018-0740-x

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