Does diet really matter? Part I: Glycemic control and weight management
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1 Does diet really matter? Part I: Glycemic control and weight management Amy P. Campbell and Melinda D. Maryniuk Clinical Education Programs, Joslin Diabetes Center, Boston, MA, USA Abstract The evidence is clear that diet, or the preferred term medical nutrition therapy (MNT), does make a difference. Long touted as the cornerstone of diabetes care, research clearly supports the role of nutrition (when delivered by a trained professional such as a registered dietitian) to improve outcomes in diabetes care. In this series of two articles we explore the evidence behind the nutrition recommendations made by major health organizations. The focus of the first article is on the science behind the effectiveness of MNT for glycemic control and weight reduction. The second article examines MNT guidelines for the comorbidities of diabetes including hyperlipidemia, hypertension and renal disease. For glycemic control, the focus is placed on carbohydrate control including consistency in type, timing and amounts. Encouraging increased consumption of higher fiber foods that also have a low glycemic index appears to be advantageous. While protein and fat have minimal impact on glycemic control, their intake should be moderated due to the risks of increased saturated fat intake and cardiovascular disease. To promote weight control, there is no clear consensus on the best approach to achieve long-term results. MNT for weight loss needs to be individualized and outcomes do improve with collaborative goal-setting and longer term follow-up. Key words: Diabetes, diet, medical nutrition therapy (MNT), glycemic control, weight management What one eats really does matter and may be at least as effective in diabetes management as many medications Introduction Despite the fact that diet is generally referred to as the cornerstone of diabetes care, the clinical efficacy of nutritional interventions may be questioned. In addition, as the number of options for medication therapy has increased, some health care providers in the United States have placed less emphasis on behavioral therapies such as nutrition and physical activity. In this article we review the evidence demonstrating that what one eats really does matter and may be at least as effective in diabetes management as many medications. Terminology To begin, a clarification of terms is necessary. The terms diet or diet therapy have long been used to describe the component of diabetes care involving guidelines for eating. However, the word diet, at least in the English language, is associated with many negative connotations including deprivation of food, rigidity, and something that people do for a short while ( go on a diet ) and then stop. For successful diabetes management, health care professionals are not asking the individual with diabetes to go on a diet for a period of time, but rather to adopt a lifelong pattern of healthy eating. There are also no well-recognized definitions of the terms diet or healthy eating. Thus nutrition professionals in the United States have advocated using the term meal planning instead of diet. In the mid-1990s, the term medical nutrition therapy (MNT) was adopted by both the American Dietetic Association and the American Diabetes Association. MNT has been defined as nutritional diagnostic, therapy and counseling services for the purpose of disease management, which are provided by a registered dietitian or nutrition professional. Medical nutrition therapy (MNT) In answer to the question, Does diet matter? or Does eating a healthy diet matter? the answer may be, Possibly it depends. However, the answer to the question, Can MNT make a difference in the management of type 1 and type 2 diabetes? is, Absolutely! That is because, by 48 International Diabetes Monitor Volume 21, Number 2, 2009
2 definition, MNT includes specific components including assessment, individualization and follow-up. Clinical trials and outcome studies of MNT have reported decreases in HbA 1c of approximately 1% in type 1 diabetes and 1 2% in type 2 diabetes, depending on the duration of diabetes (with better results achieved in shorter duration disease) [1]. As implied by the definition of MNT, in order for it to be effective, it must be based on an individualized assessment, with recommendations for meal planning and interventions developed to meet treatment goals and desired outcomes. Regular follow-up with a registered dietitian is also critical to adjust and refine the therapy, as needed, and provide ongoing support to enhance behavioral change. In the nutrition practice guideline research conducted to document the efficacy of diabetes MNT, there were generally three to four return visits in the first year of therapy. A wide variety of approaches, demonstrating the importance of individualized therapy have been documented, such as reducing calorie and/or fat intake, carbohydrate counting, simplified meal plans, exchange lists, insulin-to-carbohydrate ratios and behavioral strategies [2]. The American Diabetes Association s Standards of medical care recommend that all individuals with prediabetes and diabetes should receive individualized MNT, preferably by a registered dietitian [3, 4]. Although not part of the scope of this paper, the role of MNT in the prevention of diabetes is also becoming well established following the results of important clinical trials such as the Diabetes Prevention Program (DPP) and the Look AHEAD trial [5]. Table I summarizes the current nutritional recommendations from the American Diabetes Association as well as from the Joslin Diabetes Center, Diabetes UK and the Canadian Diabetes Association. Because MNT can have an impact on various aspects of metabolic control, including glycemia, weight, lipid levels and blood pressure, it is important for the clinician s assessment to take into consideration the target goals of therapy as well as the patient s eating preferences and willingness or readiness to change. For most patients, behaviorally focused interventions need to be made gradually and realistic goals should be set. While the overall goal for an overweight patient with type 2 diabetes and hyperglycemia, hypertension and hyperlipidemia may be to have a meal plan that is moderate (and consistent) in carbohydrate, low in calories, high in fiber, low in saturated fat and trans-fat, and low in sodium, the meal plan might initially focus on one or two changes that will have the most likelihood of improving the hyperglycemia. Once hyperglycemia is successfully managed, the next goal will likely focus on improving the hyperlipidemia and hypertension, for example. In this article we explore the evidence demonstrating the effectiveness of MNT for both glycemic control and weight reduction. In part II (see page 56) we review the evidence behind nutritional recommendations for the comorbidities of diabetes including hyperlipidemia, hypertension and renal disease. Glycemic control The concept of controlling diabetes by nutritional interventions is not new. In the time before insulin was discovered, the only way to treat diabetes was by manipulating the patient s diet. And, since having diabetes meant producing great quantities of sweet urine, dietary treatment usually involved severely restricting or even eliminating carbohydrate. Of course, restricting carbohydrate required the body to use fat and protein as alternative fuel sources, usually resulting in cachexia and a relatively short lifespan. While the discovery of insulin in the early part of the twentieth century was a revolutionary cornerstone of diabetes management, carbohydrate restriction was still recommended by physicians and fat intake remained fairly high. The creation and implementation of the exchange system in the 1950s helped to better balance the recommendations for carbohydrate, protein and fat. Over the years, recommendations for these three macronutrients have varied. Today, guidelines for determining the percentage of calories from carbohydrate, protein and fat are primarily based on the individual and such factors as type of diabetes, extent of glycemic and lipid control, willingness and ability to follow recommendations, and even social and cultural factors. Self-monitoring of blood glucose, plus the myriad diabetes medications now available, has allowed food intake to be more flexible. MNT has been proven to be beneficial in the management of diabetes. In fact, one of the key goals of MNT is to achieve and maintain blood glucose levels in the normal range or as close to normal as is safely possible [4]. Carbohydrate intake and glycemic control Carbohydrate is the body s primary energy source and is the nutrient that has the most impact on postprandial glucose levels. For this reason, some health care professionals subscribe Volume 21, Number 2, 2009 International Diabetes Monitor 49
3 Table I: Comparison of nutrition guidelines for adults with diabetes. American Diabetes Association [6] Joslin Diabetes Center guidelines for overweight and obese patients [7] Diabetes UK [8] Canadian Diabetes Association [9] Carbohydrate A dietary pattern that encourages carbohydrate from fruit, vegetables, whole grains, legumes and low fat milk Approximately 40% of total calories from carbohydrate but no less than 130 g carbohydrate per day Approximately 45 60% Sucrose up to 10% 45 60% of total calories Sucrose up to 10% For weight loss, either low carbohydrate (<130 g/day) or low fat diets may be effective in the short term (<1 year) Emphasize fresh fruit and vegetables, legumes and minimally processed grains Intake of <10 g sugar alcohols per day is acceptable Up to 60 g of added fructose in place of an equal amount of sucrose is acceptable Fiber For most adults, aim for levels of 14 g fiber per 1000 kcal Aim for minimum g fiber per day; 50 g/day if tolerated Fiber no quantitative recommendation Increase to g fiber per day from a variety of sources including soluble and cereal fibers Glycemic index The use of glycemic index and glycemic load may provide a modest additional benefit over that observed when total carbohydrate is considered alone Choose foods with a low glycemic index and a low glycemic load Although stratifying foods into low, medium and high glycemic index values may be useful for some, it can also be misleading Within the same food category, consume low glycemic index foods in place of high glycemic index foods Protein Approximately 15 20% Approximately 20 30% Not >1 g/kg body weight per day 15 20% Fat and cholesterol Saturated fat <7% Minimize intake of trans-fats <200 mg cholesterol 2 servings of fish/week (with the exception of commercially fried fish fillets) Saturated fat <7% in individuals with LDL cholesterol >100 mg/dl PUFA up to 10% of total calories, MUFA 15 20% Avoid foods high in trans-fat <200 mg cholesterol if LDL cholesterol >100 mg/dl Aim for oily fish twice per week Total fat <35% of total calories Saturated fat and transfat <10% Fish once or twice per week, especially oily fish; fish oil supplements are not recommended Total fat <35% of total calories Saturated fat <7% of total calories Minimize intake of trans-fats Meal plans should favor monounsaturated fats and, when possible, include omega-3 fatty acids (fatty fish) and plant oils (canola, walnut, flax) LDL, Low-density lipoprotein; PUFA, polyunsaturated fatty acids; MUFA, monounsaturated fatty acids. to the notion that a lower carbohydrate intake should be the focus for diabetes management. It is not uncommon for people with type 2 diabetes to follow eating regimens that often severely restrict carbohydrate in an effort to lose weight and control glucose levels. Carbohydrate is found in an abundance of foods, such as breads, cereals, pasta, legumes, fruit, vegetables, milk, yogurt and sweets. Many of these carbohydrate-rich foods provide other, important nutrients needed for good health and disease prevention, including vitamins, minerals, fiber and phytonutrients, which are not found in protein and fat foods. Many patients with diabetes are advised to eat about the same amount of carbohydrate at meals and snacks in an effort to help balance carbohydrate intake with the action of diabetes medication. This approach, sometimes known as consistent carbohydrate counting, while sound- 50 International Diabetes Monitor Volume 21, Number 2, 2009
4 ing restrictive, does offer some flexibility in that patients can decide how they will use or spend their carbohydrate allotment at meals and snacks. For individuals taking premeal rapid-acting insulin, flexibility is even greater [10]. These patients can decide how much carbohydrate they wish to consume, and then, with instruction, determine how much insulin is needed to cover that amount of carbohydrate, using an insulin-tocarbohydrate ratio. This approach is sometimes called advanced carbohydrate counting. Both the amount and type of carbohydrate consumed have an effect on postprandial glucose levels. While decreasing carbohydrate intake can be beneficial for those with type 2 diabetes, what is not clear is to what extent, if at all, carbohydrate should be restricted. Before the advent of insulin, the diabetic diet consisted primarily of protein and fat. Even after insulin became available, lower carbohydrate diets were still prescribed. In fact, Elliott P. Joslin believed that the best diet for someone with diabetes was one that contained no more than 100 g carbohydrate per day [11]. Over the years, carbohydrate recommendations for people with diabetes have ranged from being on the somewhat high side (50 60% of calories from carbohydrate) to being on the low side (<50 g carbohydrate per day). The recommended dietary allowance for carbohydrate is currently 130 g/day for both adults and children [12]. The American Diabetes Association acknowledges, for the first time, that low carbohydrate diets (those that provide less than 130 g carbohydrate per day) can be beneficial for weight loss and diabetes control for up to 1 year [13, 14]. However, what is most important in meal planning for people with diabetes is to work collaboratively with the patient to determine a carbohydrate level that is realistic and achievable for that patient. What is most important in meal planning for people with diabetes is to work collaboratively with the patient to determine a carbohydrate level that is realistic and achievable for that patient Glycemic index and glycemic control The glycemic index is a tool used to further refine postprandial glucose levels [15]. The glycemic index is a ranking of carbohydrate foods according to how much they raise blood glucose in comparison with a reference food, such as 50 g glucose or 50 g bread. Foods with a low glycemic index (0 50), such as barley, legumes, oats, rye bread and apples, are therefore expected to produce less of a rise in postprandial glucose levels compared with higher glycemic index foods ( 70), which include white bread, potatoes and watermelon. Many factors affect the glycemic index of a food, such as how the food is prepared and in what form it is eaten. Also, eating a high glycemic index food with a high fat food helps to lower the glycemic value of that food. The multitude of considerations and exceptions when using the glycemic index makes this a tool to be used only by willing and able individuals. The effectiveness of using the glycemic index to reduce postprandial blood glucose excursions is somewhat conflicting in the literature [16 19], although evidence does show that in people who consume primarily a high glycemic index diet, switching to a low glycemic index diet can improve postprandial hyperglycemia. In fact, the Canadian Trial of Carbohydrates in Diabetes [20], which was a 1-year trial of low glycemic index carbohydrate in type 2 diabetes, found that, while long term HbA 1c was not affected by either the glycemic index or the amount of dietary carbohydrate, the low glycemic index eating plan did help to sustain reductions in postprandial glucose levels. Fiber intake and glycemic control Fiber is a type of carbohydrate that cannot be digested or absorbed by humans. Fiber has virtually no caloric value, nor does it contribute to the body s glucose supply. High fiber foods can be classified as being either insoluble or soluble. Insoluble fiber sources include bran cereal and whole wheat bread. Soluble fiber is found in oats, legumes, apples and citrus fruits. Many foods contain both types of fiber. The recommended intake of fiber for adults is 14 g per 1000 calories per day. Not surprisingly, most Americans with diabetes consume far less fiber than is recommended, along the lines of 8 g per 1000 calories per day [12]. While the health benefits of fiber have been documented, there is little evidence to support the role of fiber above recommended levels in glycemic control, although data suggest that intakes of approximately 50 g fiber per day may lower glucose levels in people with type 1 diabetes and can reduce hyperinsulinemia and lipid levels in people with type 2 diabetes [21]. Achieving a fiber intake of 50 g/day is challenging and often unattainable for most people consuming typical western diets. Volume 21, Number 2, 2009 International Diabetes Monitor 51
5 Protein intake and glycemic control The role of protein in diabetes management has typically focused on patients with diabetic nephropathy. The dietary reference intake for protein is 10 35% of total calorie intake; 15% of calories from protein is the average adult intake in the United States [12]. When calculating protein requirement for adults with diabetes, the recommended dietary allowance of 0.8 g highquality protein per kilogram of body weight per day is most frequently used. High-quality protein foods include meat, poultry, fish, eggs, milk, cheese and soy-based foods. Patients are encouraged to choose leaner cuts of meat and lower fat versions of dairy foods in an effort to limit saturated fat intake. Protein digestion does result in some glucose production but does not appear to increase blood glucose levels unless large amounts of protein are consumed. A protein intake of greater than 20% of total calorie intake may aid in weight and glucose control by reducing appetite and increasing satiety [22, 23]. A slightly higher protein intake can also help to preserve lean body mass when an individual is following a reduced calorie eating plan for weight control purposes. Fat intake and glycemic control Fat is a concentrated source of energy, providing 9 kcal/g. Fat is metabolized differently than carbohydrate and protein, and indirectly affects blood glucose levels. However, a meal with moderate to high amounts of fat can delay stomach emptying of carbohydrate, resulting in a slower rise in postprandial glucose levels [24]. Furthermore, a high fat meal can lead to high glucose levels hours after a meal. Adding fat to a meal lowers the glycemic index of a food. The main concern with fat intake, however, in people with diabetes is helping them to limit saturated fatty acids, trans-fatty acids and cholesterol intake, while aiming to increase intake of omega-3 fatty acids in the form of oily fish in an effort to reduce the risk of cardiovascular disease. Therefore current recommendations are to limit saturated fat intake to less than 7% of total calories, minimize intake of trans-fat and limit dietary cholesterol to less than 200 mg/day [4]. Because unsaturated fats are beneficial for heart health, food sources of these fats, such as vegetable oils, nuts and seeds, should be emphasized over more saturated choices, including butter, lard and margarine. It is also recommended that people with diabetes consume at least two non-fried fish meals per week in order to obtain omega-3 fatty acids. Omega-3 fatty acids can lower serum triglyceride levels and reduce the risk of sudden cardiac death [25, 26]. Weight management Weight loss in people who are overweight or obese has been shown to increase insulin sensitivity and improve glycemic control. BMI is a standard measurement to use when determining body weight in relation to height. The National Heart, Lung, and Blood Institute guidelines define overweight as BMI 25 kg/m 2 and obesity as BMI 30 kg/m 2. Waist circumference is also used, along with BMI, as a measure of visceral fat and to determine the risk for cardiovascular disease. A waist circumference of 40 inches (102 cm) for men or 35 inches (89 cm) for women indicates increased risk [27]. A first-line recommendation for overweight or obese individuals with type 2 diabetes is to aim for a moderate amount of weight loss, generally in the range of 5 7% of body weight. A 5% weight loss not only reduces insulin resistance but also improves glycemic, blood pressure and lipid control [28]. While there is no one weight loss method that is appropriate for everyone, evidence supports the use of structured, intensive lifestyle programs that focus on counseling, education, reduced calorie intake, physical activity and frequent follow-up [21]. Registered dietit ians are uniquely qualified to determine the best weight management strategy for patients seeking weight loss. The MNT process helps to individualize the treatment plan and reinforce the skills and behaviors needed to ensure success [10]. However, the entire medical team needs to be involved and must be supportive of the weight management plan. Calorie intake and weight management The number of calories an individual needs depends, in part, on the person s age, sex, activity level and body weight. Many methods and formulas are available to determine a person s calorie requirements for weight mainten - ance; from there, calorie intake can be adjusted upward or downward to help achieve the desired weight. A registered dietitian, as part of the MNT process, will determine the appropriate calorie level for each patient with diabetes, taking into consideration weight management goals. 52 International Diabetes Monitor Volume 21, Number 2, 2009
6 Most sound weight loss plans provide between 500 and 1000 fewer calories than needed for current weight maintenance, with the goal of losing kg of body weight per week. Weight loss exceeding this amount is possible, but unless the individual is participating in an intensively managed program, the weight is typically regained soon after. Joslin Diabetes Center s nutrition guidelines discourage calorie intakes below kcal for women and below kcal for men. Carbohydrate intake and weight management According to the American Diabetes Association, the optimal macronutrient distribution of weight loss diets has not been established [4]. Debate continues as to whether a low carbohydrate or a low fat eating plan is the best method for both losing weight and maintaining weight loss. Several studies have shown that individuals following a low carbohydrate diet lost more weight after 6 months than those following a low fat diet [13, 14]. Yet, after 1 year, there was no significant difference in weight loss between the two dietary approaches. However, interestingly, those following the low carbohydrate diet had improved levels of HDL cholesterol and triglyceride levels compared with those on the low fat diet. In addition, one of the studies demonstrated that HbA 1c levels were lower in those following the low carbohydrate plan compared with those on the low fat plan. For many years, most medical professionals were wary of low carbohydrate diets, based on the recommended dietary allowance for carbohydrate of 130 g/day. Weight loss plans, such as the Atkins Diet, were regarded, by some, with much skepticism, as this plan utilizes a very low carbohydrate approach. Given that the brain requires glucose for fuel, the concern was that ingesting fewer than 130 g carbohydrate per day could be dangerous [12]. Joslin Diabetes Center s nutrition guidelines for people with type 2 diabetes recommend approximately 40% of calories from carbohydrate, with the total not less than 130 g/day; for someone requiring 1500 calories, 40% of calories translates into no more than 150 g carbohydrate per day. It is likely that weight loss plans providing less than 130 g carbohydrate per day are relatively safe for up to 1 year, based on the available evidence. However, it should be recognized that such low carbohydrate plans are typically lacking in adequate dietary fiber, vitamins and minerals, and may not be realistic for people to follow in the long term. Glycemic index and weight management Is a low glycemic index eating plan more inducive to weight loss in people with type 2 diabetes compared with other types of diets? Results from the CALERIE Trial [29] showed that a low glycemic load diet led to more weight loss than a high glycemic load diet in individuals who were overweight and had high insulin secretion in response to a standard OGTT; however, the participants in this study did not have diabetes. Other studies have shown similar results in that a low glycemic load diet leads to more body weight and fat loss in comparison with higher glycemic load diets. Furthermore, a low glycemic index diet led to a reduction of HbA 1c by 19% and BMI by 8% in 21 subjects with type 1 or type 2 diabetes [30]. However, the results have not been duplicated. A study published in the journal Nutrition in 2008 concluded that there was no significant difference in weight loss between a low glycemic index diet and a more traditional (American Diabetes Association) diet [31]. Protein intake and weight management A few studies indicate that a protein intake of greater than 20% not only may reduce glucose and insulin levels but may also reduce appetite and increase satiety [22, 23, 32]. Joslin Diabetes Center s nutrition guidelines advocate a protein intake of between 20% and 30%. However, there are no long-term studies that have looked at the effectiveness and safety of higher protein diets. When a higher protein diet is indicated, it is important to emphasize high quality, low saturated fat sources of dietary protein, such as skinless poultry, fish, lean meat and soy products. High protein diets are not indicated in those with any degree of renal insufficiency. Fat intake and weight management The role of fat (primarily saturated fat and transfat) in the prevention and management of coronary heart disease in people with diabetes has been previously discussed. However, because fat is a concentrated source of calories, and therefore may impact weight management, many weight control programs focus on limiting total fat intake to no more than 30% of calories, as part of a structured lifestyle program [33]. A reduction in fat intake may be beneficial for some people who are aiming to lose weight, especially in people for whom a low carbohy- Volume 21, Number 2, 2009 International Diabetes Monitor 53
7 drate eating plan is unfeasible or undesired. Foster et al. [13] concluded that, while a low carbohydrate diet resulted in a greater weight loss compared with a low fat diet after 6 months, the differences between the two eating plans were not significant after 1 year. Joslin Diabetes Center s nutrition guidelines recommend that approximately 30 35% of calories come from fat, whereas the American Diabetes Association guidelines put more emphasis on limiting saturated fat and trans-fat. Summary Clearly diet does matter when it comes to glycemic as well as weight control. Although there are slight variations in nutrition guidelines from various groups, the bottom line is that nutrition therapy should be offered to all patients and by a trained professional who is familiar with both the clinical guidelines as well as counseling techniques that enhance behavior change. Effective meal planning requires collaborative goal setting as well as ongoing support and follow-up. In part II (see page 56) we will explore the evidence behind the effectiveness of nutritional interventions for the comorbid conditions of hyperlipidemia, hypertension and renal disease. References 1. Pastors JG, Warshaw H, Daly A et al. The evidence for the effectiveness of medical nutrition therapy in diabetes management. Diabetes Care 2002; 25: Franz MJ, Boucher JL, Green-Pastors J, Powers M. Evidence-based nutrition practice guidelines for diabetes and scope and standards of practice. J Am Diet Assoc 2008; 108 (4 suppl 1): S American Diabetes Association. Standards of medical care in diabetes Diabetes Care 2008; 31 (suppl 1): S American Diabetes Association. Nutrition recommendations and interventions for diabetes: a position statement of the American Diabetes Association. Diabetes Care 2008; 31 (suppl 1): S Delahanty LM, Nathan DM. Implications of the Diabetes Prevention Program and Look AHEAD clinical trials for lifestyle interventions. J Am Diet Assoc 2008; 108 (4 suppl 1): S Bantle JP, Wylie-Rosett J, Albright AL et al. Nutrition recommendations and interventions for diabetes 2006: a position statement of the American Diabetes Association. Diabetes Care 2006; 29(9): Joslin Diabetes Center and Joslin Clinic. Clinical nutrition guidelines for overweight and obese adults with type 2 diabetes, prediabetes or those at high risk for developing type 2 diabetes. Available at: Nutrition_Guideline_Graded.pdf. Accessed November 28, Diabetes UK. The implementation of nutritional advice for people with diabetes. Diabetic Med 2003; 20: Canadian Diabetes Association. Nutrition therapy. In: Canadian Diabetes Association 2008 Clinical Practice Guidelines for the Prevention and Management of Diabetes in Canada. Can J Diabetes 2008; 32 (suppl 1): S40-3. Available at: cpg2008/ cpg-2008.pdf. Accessed December 22, Nutrition Subcommittee of the Diabetes Care Advisory Committee of Diabetes UK. The implementation of nutritional advice for people with diabetes. Diabetic Med 2003; 20: Joslin EP. The diabetic diet. J Am Diet Assoc 1927; 3: Institute of Medicine of the National Academies. Dietary reference intakes for energy, carbohydrate, fiber, fat, fatty acids, cholesterol, protein, and amino acids. Washington, DC: National Academies Press, Foster GD, Wyatt HR, Hill JO et al. A randomized trial of a low-carbohydrate diet for obesity. N Engl J Med 2003; 348: Stern L, Iqbal N, Seshadri P et al. The effects of lowcarbohydrate versus conventional weight loss diets in severely obese adults: one-year follow-up of a randomized trial. Ann Intern Med 2004; 140: Jenkins DJ, Wolever TM, Taylor RH et al. Glycemic index of foods: a physiological basis for carbohydrate exchange. Am J Clin Nutr 1981; 34: Wolever TM, Jenkins DJ, Vuksan V et al. Beneficial effect of low-glycemic index diet in overweight NIDDM subjects. Diabetes Care 1992; 15: Brand JC, Colagiuri S, Crossman S et al. Low-glycemic index foods improve long-term glycemic control in NIDDM. Diabetes Care 1991; 14: Lafrance L, Rabasa-Lhoret R, Poisson D et al. Effects of different glycaemic index foods and dietary fibre intake on glycaemic control in type 1 diabetic patients on intensive insulin therapy. Diabetic Med 1998; 15: Heilbronn LK, Noakes M, Clifton PM. The effect of high- and low-glycemic index energy restricted diets on plasma lipid and glucose profiles in type 2 diabetic subjects with varying glycemic control. J Am Coll Nutr 2002; 21: Wolever TM, Gibbs AL, Mehling C et al. The Canadian Trial of Carbohydrates in Diabetes (CCD), a 1-y controlled trial of low-glycemic-index dietary carbohydrate in type 2 diabetes: no effect on glycated hemoglobin but reduction in C-reactive protein. Am J Clin Nutr 2008; 87: Franz MJ, Bantle JP, Beebe CA et al. Evidence-based nutrition principles and recommendations for the treatment and prevention of diabetes and related complications. Diabetes Care 2002; 25: Gannon MC, Nuttall FQ. Effect of a high-protein, lowcarbohydrate diet on blood glucose control in people with type 2 diabetes. Diabetes 2004; 53: Gannon MC, Nuttall FQ, Saeed A et al. An increase in dietary protein improves the blood glucose response in persons with type 2 diabetes. Am J Clin Nutr 2003; 78: Campbell AP, Beaser RS. Medical nutrition therapy. In: Beaser RS, ed. Joslin s diabetes deskbook: a guide for primary care providers. Boston, MA: Joslin Diabetes Center, 2007; Kris-Etherton PM, Harris WS, Appel LJ. Fish consumption, fish oil, omega-3 fatty acids, and cardiovascular disease. Circulation 2005; 106: Mozaffarian D, Bryson CL, Lemaitre RN et al. Fish intake and risk of incident heart failure. J Am Coll Cardiol 2005; 45: International Diabetes Monitor Volume 21, Number 2, 2009
8 27. National Heart, Lung, and Blood Institute. Clinical guidelines on the identification, evaluation and treatment of overweight and obesity in adults. Bethesda, MD: National Institutes of Health, Klein S, Sheard NF, Pi-Sunyer X et al. Weight management through lifestyle modification for the prevention and management of type 2 diabetes: rationale and strategies: a statement of the American Diabetes Association, the North American Association for the Study of Obesity, and the American Society for Clinical Nutrition. Diabetes Care 2004; 27: Pittas AG, Das SK, Hajduk CL et al. A low-glycemic load diet facilitates greater weight loss in overweight adults with high insulin secretion but not in overweight adults with low insulin secretion in the CALERIE Trial. Diabetes Care 2005; 28: Burani J, Longo PJ. Low glycemic index carbohydrates: an effective behavioral change for glycemic control and weight management in patients with type 1 and type 2 diabetes. Diabetes Educ 2006; 32: Ma Y, Olendzki BC, Merriam PA et al. A randomized clinical trial comparing low-glycemic index versus ADA dietary education among individuals with type 2 diabetes. Nutrition 2008; 24: Johnston CS, Tjonn SL, Swan PD. High-protein, lowfat diets are effective for weight loss and favorably alter biomarkers in healthy adults. J Nutr 2004; 134: Buse JB, Ginsberg HN, Bakris GL et al. Primary prevention of cardiovascular diseases in people with diabetes mellitus: a scientific statement from the American Heart Association and the American Diabetes Association. Circulation 2007; 115: Volume 21, Number 2, 2009 International Diabetes Monitor 55
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