Effect of Species and Genotype on the Efficiency of Enrichment of Poultry Meat with n-3 Polyunsaturated Fatty Acids

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1 Effect of Species and Genotype on the Efficiency of Enrichment of Poultry Meat with n-3 Polyunsaturated Fatty Acids C. Rymer* and D.I. Givens Animal Science Research Group, University of Reading, Reading, RG6 6AR, United Kingdom ABSTRACT: The effect of poultry species (broiler or turkey) and genotype (Wrolstad or BUT T8 turkeys and Ross 308 or Cobb 500 broilers) on the efficiency with which dietary longchain n-3 PUFA were incorporated into poultry meat was determined. Broilers and turkeys of both genotypes were fed one of six diets varying in FA composition (two replicates per genotype diet interaction). Diets contained 50 g/kg added oil, which was either blended vegetable oil (control), or partially replaced with linseed oil (20 or 40 g/kg diet), fish oil (20 or 40 g/kg diet), or a mixture of the two (20 g linseed oil and 20 g fish oil/kg diet). Feeds and samples of skinless breast and thigh meat were analyzed for FA. Wrolstad dark meat was slightly more responsive than BUT T8 (P = 0.046) to increased dietary 18:3 concentrations (slopes of and 0.465, respectively). The Ross 308 was also slightly more responsive than the Cobb 500 (P = 0.002) in this parameter (slopes of and 0.449). There were no other significant differences between the genotypes. There was some evidence (based on the estimates of the slopes and their associated standard errors) that white turkey meat was more responsive than white chicken meat to 20:5 (slopes of and for turkeys and broilers, respectively). There was no relationship between dietary 18:3 n-3 content and meat 20:5 and 22:6 contents. If birds do convert 18:3 to higher FA, these acids are not then deposited in the edible tissues. Paper no. L9949 in Lipids 41, (May 2006). The health benefits associated with increased consumption of EPA (C20:5) and DHA (C22:6) as found in fish oil are well established. A meta-analysis of 26 studies by Friedberg et al. in 1998 (1) demonstrated that supplementing the diet with fish oil reduced serum concentration of triacylglycerols, and this effect was even more marked in individuals with Type 2 diabetes. Increasing consumption of EPA and DHA would therefore contribute to a reduction in the incidence of metabolic syndrome, which is characterized by obesity, insulin resistance, or Type 2 diabetes and dyslipidemia (2). However, although recommended minimum intakes of EPA plus DHA are, for example, in the UK, 450 mg/d (3), actual mean consumption in the UK is apparently only about 244 mg/d. Closer analysis of dietary survey data (4) reveals that consumption is in fact lower still, at approximately 113 mg/d (5), as only *To whom correspondence should be addressed at Animal Science Research Group, School of Agriculture, Policy and Development, University of Reading, PO Box 237, Reading, RG6 6AR, United Kingdom. c.rymer@reading.ac.uk Abbreviations: ALA, alpha-linolenic acid; LA, linoleic acid; LC n-3 PUFA, long-chain n-3 PUFA. 27% of the UK population consume any oily fish at all. In this scenario, poultry meat contributes approximately 23% of the EPA and DHA that is consumed (5). This pattern is also observed throughout northern Europe (6). Clearly, from a public health perspective, the consumption of EPA and DHA needs to increase, but efforts to encourage the consumption of oily fish or even fish oil capsules have largely failed. An alternative approach is to increase the EPA and DHA content of those foods (such as poultry meat) that are consumed and already contribute to EPA and DHA intake. The n-3 PUFA content of poultry meat can be readily increased by increasing the n-3 PUFA content of poultry diets (7 10). However, a review of several papers that reported such increases (11) noted that the response, particularly to EPA and DHA, was highly variable. Some of this variability may be due to differences in the species and genotype of bird used, but few data examining these relationships are available. The objective of this study was therefore to determine the effect of different species and genotypes of poultry on their response (as measured by increases in the n-3 PUFA content of their edible tissues) to increased concentrations of n-3 PUFA in their diet. Skinless meats were studied in this experiment, as these are more homogenous than meats with skin on, and also represent more closely what is actually consumed (at least in Europe and North America). Poultry meat is regarded as a lowfat food, and much of the fat that is present is trimmed off either before or after cooking. Thus by studying skinless meat, the impact on human nutrition of altering the FA composition of poultry tissues that are actually consumed could be determined. EXPERIMENTAL PROCEDURES Birds. The species and genotypes of poultry investigated were turkeys (using the bronze Wrolstad and white BUT T8 genotypes) and broilers (using the Ross 308 and Cobb 500 genotypes). These genotypes were selected to be indicative of those commonly consumed in Europe, except for the Wrolstad, which is reared for a more specialized niche Christmas market. Male turkey poults, 100, were purchased as day-old birds; half of them were Wrolstad (Kelly Turkeys, Danbury, Essex, United Kingdom) and the other half were BUT T8 (SCF Turkeys, Liverpool, United Kingdom). On arrival, they were brooded together for 8 wk in separate pens (divided by genotype) and fed a proprietary feed for turkey poults with clean, fresh water always available. Male broiler chicks, 120, Copyright 2006 by AOCS Press 445

2 446 C. RYMER AND D.I. GIVENS were also purchased as day-old birds (Anglia Chicks, Fakenham, Norfolk, United Kingdom); half of these were of the genotype Ross 308 and the other half were Cobb 500. On arrival they were brooded together for 3 wk in separate pens (again divided by genotype) and fed a proprietary chick crumb with clean, fresh water always available. When the turkeys were 8 wk old and the broilers 3 wk old, they were randomly allocated to one of 24 pens (turkeys) or one of 24 cages (broilers). There were four turkeys per pen and six broilers per cage, and all the birds in one pen or cage were of the same genotype. The birds were then fed one of six experimental diets ad libitum with clean, fresh water always available. There were two replicates for each genotype diet interaction. In the first week following allocation to the pens, the experimental diet was mixed on a 50:50 (fresh weight) basis with the proprietary starter pellet that the birds had been fed prior to allocation to the pens. When the broilers were 42 d old and the turkeys 16 wk old, they were humanely slaughtered, bled, plucked, and eviscerated. The head and feet were removed and carcasses were then stored at <5 C in labeled plastic bags. After 7 d, one carcass from each pen was carefully dissected to separate the breast and thigh meat. Samples of skinless breast and thigh meat were placed in clean labeled plastic bags and stored at 20 C pending analysis. Diets. Six different diets were fed to the birds, varying in their proportion of α-linolenic acid (ALA), EPA, and DHA. All diets contained 70 g/kg (fresh weight) ether extract, with 50 g of this ether extract coming from added oil. In the control diets, all the oil was in the form of blended vegetable oil. In diets Lolin and Hilin, the vegetable oil was partially substituted with linseed oil, such that the diets contained 20 and 40 g/kg (fresh weight) linseed oil respectively. In diets Lofish and Hifish, the vegetable oil was partially substituted with fish oil, such that the diets contained 20 and 40 g/kg (fresh weight) fish oil respectively. In diet Linfish, the diet contained 20 g/kg linseed oil and 20 g/kg fish oil (fresh weight basis). Details of the composition of the diets used, and their calculated nutrient compositions, are provided in Tables 1 and 2. The antioxidant used was predominantly vitamin E, which was included in all diets at a rate of 100 mg DL-α-tocopherol acetate/kg diet as fed. In the turkey diets, BHT was also included in the vitamin/mineral mix that was used, and was present in the diets at a concentration of 20 mg/kg (as fed). Analysis. The feeds and the samples of white and dark meat taken from the birds were analyzed for long-chain FA. Lipids were extracted from samples of feed (3 g) or grated frozen meat tissue (20 g) using the method of Folch et al. (12). Samples were then methylated by drying the lipid extract under a stream of nitrogen and then dissolving the residue in dried toluene (1 ml) and sodium methoxide (2.7 g dry sodium methoxide in 100 ml methanol, 2 ml). Glacial acetic acid (0.1 ml) and hexane (2 ml) were added and mixed, followed by water (5 ml). The hexane layer containing the FAME was then separated off and analyzed using a gas chromatograph-mass spectrometer (Hewlett Packard GCD Series 2). Samples were injected (split injection) onto a capillary column (60 m, 0.32 mm diameter) with helium (flow rate 1 ml/min) used as the carrier gas. The column was held at 70 C for 2 min before being raised to 165 C (5 C/min) for 5 min. It was then raised to 180 C (6 C/min) for 10 min and then 230 C (3 C/min) for 3 min. The inlet temperature was 260 C and the detector temperature 250 C. FAME were identified by comparing retention times with those of standards and quantification was done by normalizing the areas under the curve. FA concentrations were calculated in terms of % wt/wt total FA detected. Mean concentrations (mg/100 g fresh meat tissue) of total FA were calculated for each of the four meats (white chicken, dark chicken, white turkey, and dark turkey). From these estimates, the concentrations of individual FA in each poultry meat were calculated and expressed as mg/100 g edible portion. Statistical analysis. ANOVA was used to determine the ef- TABLE 1 Composition of the Diets (g/kg Fresh Weight) Fed to Broilers and Turkeys Turkeys, Turkeys, Broiler 8 12 wk wk Wheat Soybean meal Wheatfeed a Sunflower meal Beans (Phaseolus vulgaris) Fishmeal Oil (vegetable, fish, or linseed) Dicalcium phosphate Calcium carbonate Salt dl-methionine l-lysine Vitamin/mineral premix Premix provided (per kg diet as fed): Vitamin A (IU) 12,000 15,000 12,000 Vitamin D3 (IU) 5,000 5,000 4,000 Vitamin E (mg) Copper (mg) Zinc (mg) Choline chloride (mg) a Wheatfeed is a coproduct of milled wheat comprising a mixture of the bran and endosperm that is separated when cleaned and dehusked grain is milled for flour. TABLE 2 Calculated Nutrient Contents of the Diets Fed to Broilers and Turkeys (kg 1 as Fed) Turkeys, Turkeys, Broiler 8 12 wk wk Metabolizable energy, kcal 3,250 3,203 3,274 Crude protein, g Lysine, g Methionine, g Methionine + cystine, g Tryptophan, g Threonine, g Arginine, g

3 ENRICHING POULTRY MEAT WITH N-3 PUFA 447 fect of genotype, diet, and the interaction between genotype and diet on the FA content of the different poultry tissues. The FA contents of white and dark meat were compared using a paired student s t-test. To consider the efficiency with which FA were enriched in poultry meat, a linear model was used to test the hypothesis of a straight-line relationship between the concentration of an individual FA in the diet (% wt/wt total FA) and its concentration (% wt/wt total FA) in edible tissue (either white or dark meat). The interaction between this estimate of slope and the genotype of the bird was also examined. A linear mixed model was then used to determine whether there was a significant difference between tissues (and a significant interaction with genotype of bird) in the response to increased dietary concentrations of an individual FA. Statistical comparisons were made using SAS (SAS Institute Inc., Cary, NC). In the case of turkeys, the concentrations of dietary FA used were those estimated in the diets fed to the turkeys from 13 to 16 wk of age. No direct statistical comparisons between species of birds could be made, as they were reared for different times, in different houses, and on slightly different diets. However, the slopes and standard errors of the responses to increased dietary concentrations of FA were compared to determine whether there was any evidence of a difference between species in their response to dietary FA concentrations. To ascertain whether there was any difference between genotypes in increased meat concentrations of EPA and DHA resulting from an increased supply of dietary ALA, the linear relationship between diet ALA content and meat EPA or DHA content was estimated using a linear model for each tissue. Data from birds fed Lofish, Hifish, or Linfish were excluded from this analysis as the EPA and DHA present in these diets would have confounded the estimation. RESULTS TABLE 3 FA Composition (% wt/wt Total FA) of Diets Used 18:1 18:2 18:3 20:4 20:5 22:6 Diet 16:0 18: 0 n-9 n-6 n-3 n-6 n-3 n-3 Broilers, 3 6 wk Control Lolin Hilin Lofish Hifish Linfish Turkeys, 8 12 wk Control Lolin Hilin Lofish Hifish Linfish Turkeys, wk Control Lolin Hilin Lofish Hifish Linfish The concentrations of FA in the different diets are presented in Table 3. Increasing the linseed oil content of the diet increased the ALA content of the diet. Adding fish oil to the diet increased the EPA and DHA content of the diet but had a negligible effect on the ALA content. Compared with the controls, all diets had lower concentrations of 18:2 (LA), and lower ratios of n-6:n-3 FA. FA content of edible tissues. Regarding the concentrations of FA in both white and dark meat, there were no significant interactions (with either broilers or turkeys), between diet and the genotype of bird for the concentrations of FA in either white or dark meat (Tables 4 7). The Lofish and Hifish diets increased the 16:0 content of both white and dark meat. The 18:1 n-9 content of Wrolstad dark meat was approximately 12% greater (P = 0.044) than that of BUT T8 dark meat (Table 7). The LA content of meat was not affected by the genotype of bird (be it turkey or broiler), but there was a significant reduction in LA content as vegetable oil was replaced by either linseed oil or fish oil, except in the case of turkey white meat. Conversely, there was a highly significant (P < 0.001) increase in ALA content of all meats when linseed oil was included in the poultry diets, with the genotype of bird having TABLE 4 Effect of Breed and Diet on the Mean FA Content (mg/100 g Tissue) in Chicken White Meat a Control Lolin Hilin Lofish Hifish Linfish P b FA Ross Cobb Ross Cobb Ross Cobb Ross Cobb Ross Cobb Ross Cobb SE B D B D 16: : :1 n :2 n :3 n :4 n :5 n :6 n a Diets comprise (g/kg diet); Control, 50 vegetable oil (VO); Lolin, 20 linseed oil (LO), 30 VO; Hilin, 40 LO, 10 VO; Lofish, 20 fish oil (FO), 30 VO; Hifish, 40 FO, 10 VO; Linfish, 20 LO, 20 FO, 10 VO. Ross, Ross 308; Cobb, Cobb 500. b B, breed of bird; D, diet; B D, interaction between breed and diet.

4 448 C. RYMER AND D.I. GIVENS TABLE 5 Effect of Breed and Diet on the Mean FA Content (mg/100 g Tissue) in Chicken Dark Meat a Control Lolin Hilin Lofish Hifish Linfish P FA Ross Cobb Ross Cobb Ross Cobb Ross Cobb Ross Cobb Ross Cobb SE B D B D 16: : :1 n :2 n :3 n :4 n :5 n :6 n a For diet oil content and abbreviations, see Table 4. TABLE 6 Effect of Breed and Diet on the Mean FA Content (mg/100 g Tissue) in Turkey White Meat a Control Lolin Hilin Lofish Hifish Linfish P FA Wrol BUT Wrol BUT Wrol BUT Wrol BUT Wrol BUT Wrol BUT SE B D B D 16: : :1 n :2 n :3 n :4 n :5 n :6 n a Wrol, Wrolstad; BUT, BUT T8. For diet oil content and other abbreviations, see Table 4. TABLE 7 Effect of Breed and Diet on the Mean FA Content (mg/100 g Tissue) in Turkey Dark Meat a Control Lolin Hilin Lofish Hifish Linfish P FA Wrol BUT Wrol BUT Wrol BUT Wrol BUT Wrol BUT Wrol BUT SE B D B D 16: : :1 n :2 n :3 n :4 n :5 n :6 n a For diet oil content and abbreviations, see Tables 4 and 6. no significant effect. Replacing vegetable oil with n-3 rich oils reduced the 20:4 content of white chicken meat (P = 0.004), and Ross 308 white meat had a lower concentration of 20:4 than Cobb 500 white meat (P = 0.013). With regard to the long chain (LC) n-3 PUFA, increasing the concentration of fish oil in the diet resulted in significant increases in the concentration of both EPA and DHA in all meats. White Cobb 500 meat tended (P = 0.053) to have a higher concentration of DHA than Ross 308 meat, but otherwise there was no effect of poultry genotype. The EPA content of turkey meat was increased by a factor of approximately 2.8 when Hifish was fed instead of control, and the DHA content was also nearly doubled. The DHA content of white chicken meat was trebled, and that of dark chicken meat nearly quadrupled by feeding Hifish instead of control. The most dramatic increases were observed with the EPA content of chicken meat, however, which was increased by a factor of six in the dark meat when Hifish was fed instead of control. The amount of EPA + DHA that might be consumed by eating 100 g portions of poultry fed with Hifish compared with control was doubled in turkeys (from 57 to 114 mg in white meat, and from 89 to 192 mg in dark meat). In broilers, the increase was 226% in white meat (from 46 to 151 mg) and 340% in dark meat (from 27 to 117 mg). The FA content of dark meat was in all cases greater than that of white meat (P < 0.001), except for EPA in chicken meat, in which there was no significant difference, and for 20:4 and DHA in chicken meat, in which the white meat was a richer source than dark meat. Response to dietary concentrations of LNA, EPA, and DHA. Increasing the dietary concentration of LNA, EPA, or DHA resulted in significant (P < 0.001) linear increases in the concentration (% wt/wt total FA) of these acids in poultry meat (Table 8). Generally, there was no significant difference

5 ENRICHING POULTRY MEAT WITH N-3 PUFA 449 TABLE 8 Effect of Poultry Genotype on the Linear Relationship Between the Concentrations of Meat and Diet ALA, EPA, and DHA Turkey genotype P a Broiler genotype P a FA Wrol BUT SE L L B Ross Cobb SE L L B White meat ALA EPA DHA Dark meat ALA EPA DHA a L, significance of the linear relationship between diet and meat n-3 PUFA content; L B, significance of the interaction between L and the genotype of bird. For other abbreviations, see Tables 4 and 6. between the two turkey genotypes in their response to these acids, but Wrolstads did show a greater response to ALA in their dark meat compared with BUT T8. Similarly, the only significant difference between broiler genotypes in their response to these FA was the response in dark meat to ALA, with Ross 308 being more responsive than Cobb 500. There was no significant difference between white and dark meat in terms of its responsiveness to increased concentrations of dietary ALA or EPA in turkeys, but there was a tendency (P = 0.079) for white meat to be more responsive than dark meat to DHA. In broilers, there was a tendency (P = 0.078) for dark meat to be more responsive than white meat to ALA, and although there was no significant difference in their responsiveness to EPA, the response to DHA was much greater (P = 0.001) in white meat compared with dark meat. There was no difference between the broiler genotypes in this differential response by different tissues. Based on the evidence of the coefficients and their standard errors, there was some evidence that turkey white meat may be more responsive than broiler white meat to increased dietary concentrations of EPA, but otherwise there was no evidence of any difference in efficiency between the two species. There was no evidence of a linear relationship between dietary ALA content and the concentration of EPA or DHA in the meat (Table 9). There was also no difference between either broiler or turkey genotypes in this parameter, and no evidence of a difference between the species of poultry. In all cases, the coefficient describing the relationship was 0.1, and in some cases was negative. DISCUSSION Enrichment of poultry meat with n-3 PUFA. The levels of enrichment observed in this experiment with white chicken meat were similar to those reported when broilers were fed a stabilized fishmeal formulation comprising 200 g/kg of the diet (13) or a diet comprising 120 g/kg redfish meal (8). For dark meat, our results were very similar to those observed from feeding 120 g/kg redfish meal (8) or 40 g/kg fish oil (14) to broilers. However, the experiment reported by Howe et al. in 2002 (13) achieved much greater enrichment of dark meat by feeding a stabilized fishmeal formulation, and our results were equivalent to their feeding just 50 g/kg of this formulation. Much greater degrees of enrichment in white and dark meat were reported by Gonzalez-Esquerra and Leeson (15) when they fed broilers a diet comprising just 15 g/kg menhaden oil, but in this case the FA content was measured in cooked meat and Howe et al. (13) demonstrated that cooking can more than double the FA content in the tissue, presumably because of moisture loss. The LC n-3 PUFA content observed by Gonzalez-Esquerra and Leeson (15) is therefore likely, in the fresh tissue, to be similar to that observed in this experiment, although it is remarkable that such a high degree of enrichment could be obtained by them with such a low level of inclusion of the fish oil in the diet. This serves to illustrate the variability in the LC n-3 PUFA content of different fish oils, and does explain, in part, the variability in enrichment observed when similar quantities of fish oil are fed. For example, Zanini et al., in 2004, fed broilers diets com- TABLE 9 Effect of Poultry Genotype on the Linear Relationship Between Diet ALA Content and Meat EPA or DHA Content Turkey genotype P a Broiler genotype P a Acid Wrol BUT SEM L L B Ross Cobb SEM L L B White meat EPA DHA Dark meat EPA DHA a For abbreviations, see Tables 4, 6, and 7.

6 450 C. RYMER AND D.I. GIVENS prising 60 g/kg fish oil yet only achieved LC n-3 PUFA contents of 54 mg/100 g in white meat and 42 mg/100 g in dark meat (16). Similarly, feeding broilers diets comprising 55 g/kg marine algae resulted in the LC n-3 PUFA content of the white meat being just 20 mg/100 g (17). Although conventional poultry meat contributes relatively little LC n-3 PUFA (a 100-g serving of the meat produced in this study would contribute just 12% of the recommended minimum daily intake), poultry meat enriched by dietary means with LC n-3 PUFA does result in meat with a nutritionally meaningful LC n-3 PUFA content. In this experiment, 100 g servings of either chicken or turkey meat (be it white or dark) would contribute approximately 32% of the recommended minimum daily intake of 450 mg LC n-3 PUFA. Effect of poultry species and genotype on enrichment efficiency. The results of this experiment demonstrated that, in modern broiler genotypes, there was no significant difference in the efficiency with which LC n-3 PUFA were incorporated into edible tissue. Even the more genetically diverse white and bronze genotypes of turkey showed a difference only in the incorporation of ALA into dark meat (as did the broilers). This limited difference may still suggest that there is some scope for selecting birds on the basis of their efficiency of transferring dietary n-3 PUFA to their meat tissues, but such selection cannot be at the cost of meat growth potential if this approach is to be viable. There is little evidence from this experiment (and from comparing data from the literature) to suggest that there is any inherent difference between broilers and turkeys in their ability to incorporate n-3 PUFA in their edible tissues, except perhaps for EPA in white meat. The evidence that white chicken meat is a richer source of DHA than dark meat and also has a greater enrichment efficiency than dark meat for DHA is promising, particularly from the European Union viewpoint, since the consumption of white poultry meat far outweighs the consumption of dark meat in the EU. It is not a surprising finding, as the LC n-3 PUFA preferentially accumulate in the phospholipids, which are much more prevalent in the white meat compared with the dark meat (7). The enrichment of EPA and DHA that was achieved in the white and dark meat with the Hifish diet amounted to (mean wt/wt total FA) 3.1% EPA and 8.8% DHA. It is not known what the maximum possible degree of EPA and DHA enrichment in poultry meat is, but it is perhaps worth noting that the skeletal muscle of the king penguin chick, which is hatched from eggs containing the highest known DHA content and which then feeds exclusively on fish, was quite refractory to changes in dietary EPA and DHA content (18). Indeed, although the EPA and DHA content of adipose tissue in the first month of growth increased rapidly and by the time of thermal emancipation was essentially identical to that of the diet, the DHA content of muscle phospholipid in particular remained remarkably constant at about 11.5% (18). There may of course be species differences, but these data may suggest that the maximum degree of enrichment of DHA that may be possible in poultry meat is around 12% wt/wt total FA. This was the degree of enrichment achieved in white chicken meat with the Hifish diet, and would be equivalent to approximately 113 mg DHA/100 g white poultry meat and 189 mg DHA/100 g dark poultry meat. Enrichment of poultry meat with EPA and DHA in response to dietary LNA. If sources other than marine oils are to be used to enrich poultry meats with LC n-3 PUFA, then a disappointing result was the lack of relationship between the dietary ALA content and the EPA and DHA content of the meat. This relationship was calculated after data that involved feeding EPA and DHA to poultry were excluded. It therefore examined the birds ability to convert dietary ALA to EPA and DHA and then deposit these LC n-3 PUFA in the edible tissues. The evidence from this experiment is that such a process is extremely limited, and this was also the conclusion of López-Ferrer et al. in 2001 (19). Their work suggested that although the birds may be capable of converting ALA to EPA and DHA to some extent, these acids were not then deposited in skeletal muscle but rather sequestered in the liver or transported to other tissues. It is not clear what mechanisms control the transport and distribution of EPA and DHA within the bird, but developing a means of controlling and manipulating such pathways would be an extremely valuable means of increasing the impact of measures to enrich poultry meat with the nutritionally valuable LC n-3 PUFA, without reliance on fish oils. ACKNOWLEDGMENTS This is an output of LipGene, an integrated project funded by the European Union Sixth Framework Programme entitled Diet, genomics and the metabolic syndrome: an integrated nutrition, agrofood, social and economic analysis ( Technical support from Mr. C. Green for the rearing of the poultry, Mr. R. Brown for the chemical analysis, and Mr. A.A. Leidi for statistical analysis is gratefully acknowledged. REFERENCES 1 Friedberg, C.E., Janssen, M.J.F.M., Heine, R.J., and Grobbee, D.E. (1998) Fish Oil and Glycemic Control in Diabetes: A Meta-Analysis, Diabetes Care 21, Nugent, A.P. (2004) The Metabolic Syndrome, Nutr. Bull. 29, Scientific Advisory Committee on Nutrition and Committee on Toxicity. (2004) Advice on Fish Consumption: Benefits and Risks. TSO, Norwich. 4. National Diet and Nutrition Survey. (2002) The National Diet and Nutrition Survey: Adults Aged 19 to 64 years. Volume 1: Types and Quantities of Foods Consumed, TSO, London. 5. Givens, D.I., and Gibbs R.A. 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