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Carbohydrates: is the advice to eat less justified for diabetes and cardiovascular health? Jim Manna,b and Kirsten McAuleya Purpose of review Recent randomized controlled trials examining diets of varying carbohydrate composition recommended for people with diabetes and cardiovascular disease and those at risk are summarized. Recent findings Severe carbohydrate restriction results in appreciable initial weight loss and improvement in risk factors. After a year, however, the beneficial effects are equal to or less than those achieved on conventional alternatives. Some people develop elevations of LDL cholesterol. Modest carbohydrate restriction with relatively high intakes of cisunsaturated fatty acids and protein is acceptable to many people and is more likely to produce sustained benefit in terms of weight loss and cardiovascular risk indicators. Summary Diets involving moderate carbohydrate restriction are suitable alternatives to high-carbohydrate, high-fibre diets for weight loss and reduction of cardiovascular disease and diabetes risk, as well as to treat individuals with the conditions. As such diets are generally high in protein and unsaturated fatty acids, they are not recommended for those with established or incipient nephropathy. High-carbohydrate, high-fibre diets remain appropriate for use in all those situations, provided carbohydrate is derived principally from minimally processed wholegrain breads and cereals and intact vegetables and fruit. Lower carbohydrate options may be preferable for markedly insulin-resistant individuals. Keywords cardiovascular disease, diabetes, low-carbohydrate diet, nutrition Curr Opin Lipidol 18:9–12. ß 2007 Lippincott Williams & Wilkins. a Edgar National Centre for Diabetes Research, University of Otago, Dunedin, New Zealand and bDepartment of Human Nutrition, University of Otago, Dunedin, New Zealand Correspondence to Jim Mann, Edgar National Centre for Diabetes Research, University of Otago, PO Box 56, Dunedin, New Zealand Tel: +64 3 479 7719; fax: +64 3 474 7641; e-mail: [email protected] Current Opinion in Lipidology 2007, 18:9–12 ß 2007 Lippincott Williams & Wilkins 0957-9672 Introduction The suggestion that low-carbohydrate diets might be appropriate for people with diabetes is not new. In the eighteenth century, the diabetic dietary prescription in Britain involved severe carbohydrate restriction [1]. As recently as the 1970s, in most Western countries, it was generally recommended that around 40% total energy be derived from carbohydrate, with sugars being eliminated as far as possible [2]. The demonstration of a substantially increased risk of cardiovascular morbidity and mortality and the potential atherogenicity of diets high in saturated fat, led to the questioning of this approach [1]. A series of studies in the 1970s and 1980s demonstrated, in both type 1 and 2 diabetes, that high-carbohydrate, high-fibre diets low in saturated fat could improve glycaemic control and a range of cardiovascular risk factors when compared with the standard low-carbohydrate dietary regime [1]. By the 1990s, nutritional recommendations for people with diabetes suggested a much more liberal approach with regard to carbohydrates, with organizations such as the European Association for the Study of Diabetes, through its Nutrition Advisory Group, suggesting that carbohydrate might provide as much as 60% of total dietary energy [3]. The epidemiological evidence suggesting that populations consuming high-carbohydrate diets have low rates of cardiovascular disease, and the generally favourable effect of low-fat, high-carbohydrate diets on cardiovascular risk factors, especially total and low density lipoprotein cholesterol, have led to a widespread acceptance that such diets are cardioprotective for the population at large, as well as people with diabetes [4]. Unfortunately, the importance of the nature of the carbohydrate-containing foods has not been sufficiently emphasized when recommending relatively high carbohydrate intakes. Epidemiological and experimental evidence suggesting the cardioprotection and improved glycaemic control, associated with high-carbohydrate diets, is based upon studies in which vegetables, fruits and wholegrain cereals rich in nonstarch polysaccharides (dietary fibre) predominate [5]. When rice, potato and highly refined cereals constitute a high proportion of the carbohydrate-containing foods, a high-carbohydrate diet may result in elevation of triglycerides, reduction of HDL cholesterol and deterioration of glycaemic control (in people with diabetes) [6]. These observations and the widespread promotion of a range of commercially driven low-carbohydrate diets have prompted a reappraisal 9 Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited. 10 Nutrition and metabolism of the benefits in terms of cardiovascular and diabetic health and potential adverse effects of low-carbohydrate diets. There is no universally accepted definition of a lowcarbohydrate diet, but it seems that it is used for diets including as little as 20 g carbohydrate daily, as well as for those in which around 40% total energy is derived from carbohydrate. Severe carbohydrate restriction The Atkins diet has been the most popular of the diets involving severe carbohydrate restriction, typically starting with no more than 20 g carbohydrate daily, gradually increasing to 50 g or 60 g per day. This approach has principally been recommended as a weight-loss diet but it has been claimed to have beneficial effects on cardiovascular risk factors. Two recent randomized trials have been particularly helpful in establishing the place of such an approach. Dansinger et al. [7] randomized 160 overweight participants (BMI: 27–42) with at least one cardiovascular risk factor to four groups receiving one of four sets of dietary advice: the Atkins diet, the Zone diet (40% carbohydrate, 30% fat, 30% protein), Weightwatchers diet (strictly calorie controlled), and the Ornish diet (10% fat, vegetarian). The study was continued for 12 months, but dropout rates were very high: only about half of those recommended the Ornish or Atkins diet completed the 12-month study, with modestly higher (65%) retention rates on the other two diets. Among those who completed the study, weight loss at 1 year was around 2 kg for Atkins participants and 3 kg for those on the other diet groups. The ratio of LDL to HDL was reduced by about 10% in each of the diet groups. Changes in lipoprotein-mediated risk (as measured by total/HDL cholesterol), C-reactive protein and insulin levels were all significantly associated with weight loss, with no significant differences between diets. Amount of weight loss was associated with self-reported dietary adherence level, regardless of diet type. The study by McAuley and colleagues [8,9] included 96 overweight insulin-resistant women who were randomized to receive dietary advice based on the Atkins approach, the Zone approach or a high-carbohydrate, high-fibre diet. They too were followed for a year, but the aims and method of dietary instruction differed, in that during the first 8-week period, the intensive intervention carried out under strict supervision aimed to achieve weight loss, and the second phase (also 8 weeks) aimed for weight maintenance. During the final 8 months, participants were encouraged to maintain weight loss, but were offered no further dietary advice. Retention rates after 1 year were relatively low in the Atkins group (77%), among whom an interesting trend was apparent with regard to a number of outcome measures. During the first 2 months, the reductions in total body weight and fat mass were greater in this group than in the other two groups. Thereafter, however, these measures of adiposity tended to trend upwards towards initial levels. Several cardiovascular risk factors, including triglycerides and insulin levels, followed a similar trend. These observations are broadly compatible with a metaanalysis [10] published in February 2006 that included the Dansinger study and four earlier studies. Although weight loss after 6 months was greater ( 3.3 kg; 95% confidence interval: 5.3 to 1.4) on the low-carbohydrate than on the high-carbohydrate diets, after 12 months there was no difference. In the meta-analysis, triglycerides and HDL cholesterol tended to be more favourable on the low-carbohydrate diets whereas total and LDL cholesterol were significantly lower on the lowfat, relatively high-carbohydrate diets. Retention rates were generally poor. Thus in terms of longer-term weight loss, there appears to be little merit in the severely carbohydrate-restricted Atkins approach. The adverse effects noted on total and LDL cholesterol argue rather strongly against the use of this method, despite the potentially beneficial changes in some other cardiovascular risk factors. It has been argued that for those who find it a palatable method for weight loss, it is acceptable in the short term. This matter remains to be finally resolved but, in our opinion, the generally poor retention rates and the effects on raising total and LDL cholesterol in some people, even during the weight-loss phase, argue strongly in favour of excluding this approach from the nutritional armamentarium. If it is to be used, monitoring of total and LDL cholesterol is necessary. There would appear to be no justification for its long-term use. Modest carbohydrate restriction More modest degrees of carbohydrate restriction have been studied in the context of the Zone, Southbeach and Commonwealth (of Australia) Scientific and Industrial Research Organisation (CSIRO) diets, which tend to be relatively high in protein and fat. As indicated earlier, the Dansinger et al. study [7] reported broadly similar findings on all diets. On the other hand, McAuley et al. [8,9] found the most favourable overall set of results among those allocated to the high-protein, lower-carbohydrate (Zone) diet. Initial losses of weight and fat mass ( 6 kg and 4 kg) were generally maintained over the entire 1-year period as were the improvements in metabolic measures. Retention rates were highest in this group (93%). Although those randomized to the highcarbohydrate, high-fibre diet were also able to retain the benefits achieved in body mass and risk factors, all improvements were less marked. This is perhaps because compliance was relatively poor compared with the degree of compliance with the lower-carbohydrate, highprotein approach. High-protein diets (28% total energy) relatively low in carbohydrate (42% total energy) have also been compared Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited. Carbohydrates advice Mann and McAuley 11 with relatively high-carbohydrate diets (55% total energy) in people with type 2 diabetes [11]. Glycaemic control did not differ on the two diets, but LDL cholesterol was lower on the high-protein diet and, in women, reduction in fat mass was greater. In this study, however, total dietary fibre intake did not differ appreciably on the two diets. Thus it is conceivable that, as with the McAuley study, there was insufficient consumption of the appropriate high-fibre, carbohydrate-containing foods (by those randomized to the higher carbohydrate diet) to produce the benefits repeated elsewhere of such diets [5]. The group from Adelaide, South Australia, have carried out the longest study to date in which two relatively lowfat diets were compared in obese hyperinsulinaemic subjects: one provided 15% total energy from protein, 55% from carbohydrate, and the other 30% protein, 40% carbohydrate. Intensive dietary advice relating to weight loss was given during the first 12 weeks. This was followed by a 4-week period of instruction regarding weight maintenance. Participants were then followed for a further 52 weeks but no professional support was offered. Long-term compliance without active ongoing advice was poor but participants in both groups achieved modest weight loss, a reduction in fasting insulin and insulin resistance, as well as some improvement in inflammatory markers [12]. Using a similar experimental design, this group has also investigated subjects with type 2 diabetes, and reported a more favourable carbohydrate risk profile on the higher protein diet [13]. There appears to be little difference when protein or monounsaturated fatty acids predominate in a carbohydrate-restricted diet. Luscombe-Marsh and colleagues [14] compared 35% carbohydrate diets that were relatively high in protein (34% total energy) or monounsaturated fatty acids (24% total energy) in obese hyperinsulinaemic women. Weight loss and improvements in insulin resistance and cardiovascular risk factors were similar in the two diets. Thus with regard to diabetic and cardiovascular health, a relatively low-carbohydrate diet (35–40% total energy) appears to be a reasonable option for weight loss and improvement in cardiovascular risk factors and glycaemic control. The apparently better results than those observed on high-carbohydrate, high-fibre diets seem to relate to improved compliance. Thus for those who find it difficult to consume the appropriate carbohydrate-containing foods, a higher intake of protein or unsaturated fatty acids in conjunction with a reduced intake of carbohydrate may facilitate compliance and, as a consequence, more favourable outcomes. Safety of low-carbohydrate diets Issues of both efficacy and safety have been the subject of a recent systematic review [15]. Few randomized studies have continued for as long as a year and only one for longer. Thus it is difficult to offer definitive comments on safety. Severe carbohydrate restriction as occurs at least initially in the Atkins approach is associated with ketosis. The extent to which this has deleterious effects in those with abnormalities of carbohydrate metabolism or indeed in those who do not is unclear. There is no doubt, however, that at least some individuals will respond to the high saturated-fat intake, which almost invariably accompanies the substantial reduction of carbohydrate, by increasing LDL levels, sometimes markedly. While we do not recommend such diets, if they are used it would seem prudent to measure lipids and lipoproteins. With modest carbohydrate restriction, usually associated with an increase in protein and unsaturated fatty acids, there would seem to be a small likelihood of untoward effects, at least in those who do not have diabetes or renal disease. Indeed, even in those who have diabetes but normal renal function, a moderate increase in protein appears to be well tolerated [16]. In the presence of renal disease, however, perhaps especially in those with diabetes, an appreciable increase in protein may not be appropriate [17]. Further research in this regard is necessary since no definitive studies have been conducted. Conclusion The question posed does not lead to a single unequivocal affirmative or negative response. Carbohydrate restriction to the extent that induces ketosis may result in short-term weight loss. Such advice is probably not justified, however, given that long-term benefits in terms of reduced adiposity and cardiovascular risk factors are no greater on those diets than on those more closely aligned to eating patterns to which humans have long been adapted. Furthermore, some people consuming such diets will develop raised LDL levels and there are potential adverse effects of high intakes of saturated fatty acids (e.g. reduced insulin sensitivity-enhanced thrombogenesis), which have not been well studied and may be especially relevant after the weight-loss phase. On the other hand, modest carbohydrate restriction in association with somewhat higher than usual intakes of protein and cis-unsaturated fatty acids can facilitate long-term reduction of excess adiposity, enhance insulin sensitivity and favourably influence several cardiovascular risk factors. It also seems to be acceptable to those accustomed to a typical Western dietary pattern. Thus it would appear to be a reasonable alternative to the high-carbohydrate, high-fibre diet, especially as many people appear to prefer the food choices associated with a lower carbohydrate intake to the fibre-rich wholegrain cereal and breads, vegetables and fruit that are an essential component of high-carbohydrate, high-fibre diets. Rather Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited. 12 Nutrition and metabolism than recommend carbohydrate restriction, however, health professionals should inform patients and those at risk of diabetes and cardiovascular disease, that alternatives are available. References and recommended reading Papers of particular interest, published within the annual period of review, have been highlighted as: of special interest of outstanding interest Additional references related to this topic can also be found in the Current World Literature section in this issue (p. 73). 1 Mann JI. Lawrence lecture: Lines to legumes: changing concepts of diabetic diets. Diabet Med 1984; 1:191–198. 2 Truswell AS, Thomas BJ, Brown AM. Survey on dietary policy and management in British diabetic clinics. Br Med J 1975; ii:7–11. 3 Mann JI, De Leeuw I, Hermansen K, et al. Evidence-based nutritional approaches to the treatment and prevention of diabetes mellitus. Nutr Metab Cardiovasc Dis 2004; 14:373–394. 4 World Health Organisation. Diet, nutrition and the prevention of chronic diseases. Report of a Joint WHO/FAO Expert Consultation (Geneva). WHO Technical Report Series 2003; 916. 5 Mann J. Dietary fibre and diabetes revisited. Eur J Clin Nutr 2001; 55:919– 921. 6 Venn BJ, Mann JI. Cereal grains, legumes and diabetes. Eur J Clin Nutr 2004; 58:1443–1461. Dansinger ML, Gleason JA, Griffith JL, et al. Comparison of the Atkins, Ornish, Weight Watchers, and Zone diets for weight loss and heart disease risk reduction: a randomized trial. J Am Med Assoc 2005; 293: 43–53. This study evaluated the effects of four different dietary approaches to weight loss and demonstrated similar effects of each, improvements being related principally to extent of reported compliance. 7 8 McAuley KA, Hopkins CM, Smith KJ, et al. Comparison of high-fat and highprotein diets with a high-carbohydrate diet in insulin-resistant obese women. Diabetologia 2005; 48:8–16. McAuley KA, Smith KJ, Taylor RW, et al. Long-term effects of popular dietary approaches on weight loss and features of insulin resistance. Int J Obes 2006; 30:342–349. This study compared high fat and high protein diets with a high carbohydrate diet, while the high fat diet produced impressive short term results, the most favourable outcomes were reported on the high protein approach. 9 10 Nordmann AJ, Nordmann A, Briel M, et al. Effects of low-carbohydrate vs low fat diets on weight loss and cardiovascular risk factors: a meta-analysis of randomized controlled trials. Arch Int Med 2006; 166:285–293. This meta-analysis involved a comparison of low carbohydrate and low fat dietary approaches. The low carbohydrate high fat approach was associated with elevated LDL cholesterol. 11 Parker B, Noakes M, Luscombe N, Clifton P. Effect of a high-protein, highmonounsaturated fat weight loss diet on glycemic control and lipid levels in type 2 diabetes. Diabetes Care 2002; 25:425–430. 12 Brinkworth GD, Noakes M, Keogh JB, et al. Long-term effects of a highprotein, low-carbohydrate diet on weight control and cardiovascular risk markers in obese hyperinsulinemic subjects. Int J Obes Relat Metabol Disord 2004; 28:661–670. 13 Brinkworth GD, Noakes M, Parker B, et al. Long-term effects of advice to consume a high-protein, low-fat diet, rather than a conventional weight-loss diet, in obese adults with type 2 diabetes: one-year follow-up of a randomised trial. Diabetologia 2004; 47:1677–1686. 14 Luscombe-Marsh ND, Noakes M, Wittert GA, et al. Carbohydrate-restricted diets high in either monounsaturated fat or protein are equally effective at promoting fat loss and improving blood lipids. Am J Clin Nutr 2005; 81:762–772. 15 Bravata DM, Sanders L, Huang J, et al. Efficacy and safety of low-carbohydrate diets: a systematic review. J Am Med Assoc 2003; 289:1837–1850. 16 Nuttall FQ, Gannon MC. Metabolic response of people with type 2 diabetes to a high protein diet. Nutr Metab 2004; 1:6. 17 Pedrini MT, Levey AS, Lau J, et al. The effect of dietary protein restriction on the progression of diabetic and nondiabetic renal diseases: a meta-analysis. Ann Intern Med 1996; 124:627–632. Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.