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Fish Oil Supplementation in Type 2 Diabetes a Quantitative Systematic Review

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Fish Oil Supplementation in Type 2 Diabetes a Quantitative Systematic Review Reviews/Commentaries/Position Statements REVIEW ARTICLE Fish Oil Supplementation in Type 2 Diabetes A quantitative systematic review VICTOR M. MONTORI, MD PETER C. WOLLAN, PHD Greenland (8). Despite ingesting up to 40% ANDREW FARMER, MA BMBCH SEAN F. D INNEEN, MD, MSC of calories as fat (predominantly of marine origin), this population had a lower inci- dence of coronary heart disease than indi- viduals with similar fat intake on a more conventional diet (9). Further evaluation OBJECTIVE — To determine the effects of fish oil supplementation on lipid levels and revealed that dietary fish oil supplementa- glycemic control in patients with type 2 diabetes. tion led to improvement in hypertriglyc- eridemia in nondiabetic individuals RESEARCH DESIGN AND METHODS — A comprehensive search of Medline, through lowering VLDL cholesterol syn- Embase, Lilacs, the Cochrane Clinical Trials Registry, bibliographies of relevant papers, and expert input updated through September 1998 was undertaken. All randomized placebo-con- thesis (10,11). However, concern was trolled trials were included in which fish oil supplementation was the only intervention in sub- raised in the initial nonrandomized studies jects with type 2 diabetes. Three investigators performed data extraction and quality scoring in patients with type 2 diabetes that fish oil independently with discrepancies resolved by consensus. Eighteen trials including 823 subjects supplementation was associated with a followed for a mean of 12 weeks were included. Doses of fish oil used ranged from 3 to 18 g/day. deterioration in glycemic control (6,7). The outcomes studied were glycemic control and lipid levels. This concern continues to be mentioned in narrative reviews on the subject (12,13). RESULTS — Meta-analysis of pooled data demonstrated a statistically significant effect of fish The aim of the present study was to per- Ϫ Ϫ Ϫ oil on lowering triglycerides ( 0.56 mmol/l [95% CI 0.71 to 0.41]) and raising LDL cho- form a systematic review of randomized lesterol (0.21 mmol/l [0.02 to 0.41]). No statistically significant effect was observed for fast- controlled trials addressing the effects of ing glucose, HbA1c, total cholesterol, or HDL cholesterol. The triglyceride-lowering effect and the elevation in LDL cholesterol were most marked in those trials that recruited hypertriglyc- fish oil supplementation in patients with eridemic subjects and used higher doses of fish oil. Heterogeneity was observed and explained type 2 diabetes. We were specifically inter- by the recruitment of subjects with baseline hypertriglyceridemia in some studies. ested in the effects of fish oil on lipid levels and glycemic control. CONCLUSIONS — Fish oil supplementation in type 2 diabetes lowers triglycerides, raises LDL cholesterol, and has no statistically significant effect on glycemic control. Trials with hard clinical end points are needed. RESEARCH DESIGN AND METHODS Diabetes Care 23:1407–1415, 2000 Identification and retrieval of primary studies he typical dyslipidemia associated dietary approaches focus on restriction of We conducted an electronic literature search with type 2 diabetes is a combination saturated fat and limitation of simple car- from 1966 to September 1998 in Medline, Tof hypertriglyceridemia, low levels of bohydrate and alcohol intake (2). During Embase, Lilacs, Science Citation Index, HDL cholesterol, and abnormal LDL com- the late 1980s, several investigators reported and the Cochrane Controlled Trials Regis- position (1). Several pharmacological on the use of dietary supplementation with ter using a protocol that included the approaches have been used to treat diabetic fish oil as a means of treating diabetic dys- Cochrane Collaboration’s search strategy dyslipidemia (2). These include use of 3- lipidemia (6,7). for randomized controlled trials (14) and hydroxy 3-methylglutaryl CoA (HMG- The potential role of fish oil in cardio- the following terms: diabetes mellitus, type CoA) reductase inhibitors (3), fibric acid vascular disease risk reduction first came 2 diabetes, non-insulin dependent diabetes derivatives (4), and niacin (5). Standard from observations involving Inuits in (NIDDM), fish oil, n-3 fatty acids, omega- 3 fatty acids, eicosapentaenoic acid (EPA), and docosahexaenoic acid (DHA). Hand From the Mayo Clinic and Foundation (V.M.M., S.F.D.); the Department of Research and Education (P.C.W.), searching of the bibliographic sections of Olmsted Medical Center, Rochester, Minnesota; and the Health Services Research Unit (A.F.), University of all relevant articles was undertaken. Oxford, Oxford, United Kingdom. Address correspondence and reprint requests to Sean F. Dinneen, MD, MSc, Department of Diabetes and Experts were consulted regarding unpub- Endocrinology, Addenbrookes Hospital, Clinic 12, Box 49, Hills Road, Cambridge CB2 2QQ, U.K. E-mail: lished or ongoing studies. Studies were [email protected]. included if they were randomized placebo- Received for publication 17 December 1999 and accepted in revised form 3 May 2000. controlled trials that used fish oil supple- Abbreviations: DHA, docosahexaenoic acid; EPA, eicosapentaenoic acid; HMG-CoA, 3-hydroxy 3-methyl- glutaryl CoA. mentation as the only intervention in A table elsewhere in this issue shows conventional and Système International (SI) units and conversion subjects with type 2 diabetes. Language factors for many other substances. was not an exclusion criterion. DIABETES CARE, VOLUME 23, NUMBER 9, SEPTEMBER 2000 1407 Fish oil in type 2 diabetes Outcome measures and data Study (64) was excluded because it is a The dose of fish oil ranged from 3 to extraction nonrandomized non–placebo-controlled 18 g (1.08–5.2 g EPA and 0.3–4.8 g DHA). Study selection, data extraction, and assign- addition to the original study (65). Eighteen The fish oil was usually given in capsules ing of a quality score were undertaken trials met inclusion criteria and were with the exception of 1 study, in which a independently by 3 investigators with dis- included in the review (65–82). The effect liquid form was used (70). The dose of crepancies resolved by consensus. When of fish oil on glycemic control and lipid lev- placebo was matched to the dose of fish data were not available in a published els was the focus of 17 of the included tri- oil. The placebo used was a vegetable oil report, efforts were made to contact the pri- als. One study was designed to assess the with the exception of 1 study that used a mary investigators. Data related to the effect of fish oil supplementation on vascu- saline solution (70). effects of fish oil and placebo on glycemic lar physiology; however, these investigators and lipid outcomes were extracted from also reported glycemic and lipid end points Data synthesis each trial. One study reported total glyco- (73). Characteristics of the included studies Glycemic control. Of the 18 trials sylated hemoglobin; a formula was used to are shown in Table 1. included in the review, only 12 reported convert data to HbA1c (15). Study quality their fasting glucose results in a way that was assessed using the score developed by Study characteristics permitted pooling of data (Fig. 1). The Jadad et al. (16), which has a possible range The 18 trials included 7 parallel group pooled weighted mean difference for fast- of 0–5, with a cutoff of 2 used to designate design and 11 crossover design studies. The ing glucose was 0.26 mmol/l (95% CI studies of high versus low quality. parallel group trials ranged in duration from Ϫ0.08 to 0.60). Fifteen trials reported gly- 3 to 24 weeks. The crossover studies had cosylated hemoglobin data, and 11 of these Data analysis and statistical phases that ranged in duration from 2 to 24 were amenable to meta-analysis. The methods weeks. None of the 11 crossover studies pooled weighted mean difference was Extracted data were analyzed using the reported phase-specific data. Four studies 0.15% (Ϫ0.08 to 0.37). Of the 11 Review Manager 3.1 statistical software had a washout period (3–8 weeks in dura- crossover studies, 8 reported glycosylated developed by the Cochrane Collaboration. tion) and 1 of these looked for but did not hemoglobin, and 5 had phase duration of A random-effects model was used to pool find a carryover effect (77). Of the 7 studies Ͻ8 weeks. data. Effect sizes are presented as weighted that did not have a washout period, 5 looked Lipid profile. Fourteen trials reported data mean differences with 95% CIs. Hetero- for and 2 found a carryover effect (66,72). on triglycerides (Fig. 2). The pooled geneity was assessed using the ␹2 method. The interrater reliability for the assign- weighted mean difference was Ϫ0.56 Publication bias was evaluated using a fun- ment of a quality score was substantial (␬ = mmol/l (Ϫ0.71 to Ϫ0.41). This effect was nel plot method (17). The method of 0.77). The studies could be classified by most marked in studies that recruited only Rosenthal (18) was used to estimate the their quality scores into 8 studies of low hypertriglyceridemic subjects; the pooled number of unpublished studies with zero- quality (Յ2 points) (69–71,76,77,79, weighted mean difference was Ϫ0.73 effect that would be required to change a 80,82) and 10 studies of high quality (Ͼ2 mmol/l (Ϫ0.95 to Ϫ0.51). When studies significant result from the meta-analysis points) (65–68,72–75,78,81). Because ran- that used the higher doses of fish oil were into a nonsignificant result. Sensitivity domization was an inclusion criterion, all analyzed, the pooled weighted mean dif- analyses were planned a priori and under- studies started with a score of 1. An addi- ference was Ϫ0.85 mmol/l (Ϫ1.44 to taken for the following variables: study tional point was usually assigned for the Ϫ0.26). Thirteen trials reported data on design, number of subjects, length of inter- presence of blinding.
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