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1 Pi-Sunyer FX: Glycemic index and disease. Am J Clin Nutr 2002;76:290S-298S.

2 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;25:148-198.

3 Sheard NF, Clark NG, Brand-Miller JC, et al: Dietary carbohydrate (amount and type) in the prevention and management of diabetes. A statement by the American Diabetes Association. Diabetes Care 2004;27:2266-2271.

4 Salmeron J, Manson JE, Stampfer MJ, et al: Dietary fiber, glycemic load and risk of non-insulin-dependent diabetes mellitus in women. JAMA 1997;277:472-477.

5 Salmeron J, Ascherio A, Rimm EB, et al: Dietary fiber, glycemic load, and risk of NIDDM in men. Diabetes Care 1997;20:545-550.

6 Liese A, Schulz M, Fang F, et al: Dietary glycemic index and glycemic load, carbohydrate and fiber intake, and measures of insulin sensitivity, secretion, and adiposity in the Insulin Resistance Atherosclerosis Study. Diabetes Care 2005;28:2832-2838.

7 Gilbertson HR, Brand-Miller JC, Thorburn AW, et al: The effect of flexible low glycemic index dietary advice versus measured carbohydrate exchange diets on glycemic control in children with type 1 diabetes. Diabetes Care 2001;24:1137-1143.

8 Wolever TM, Vorster HH, Bjorck I, et al: Determination of the glycaemic index of foods: inter-laboratory study. Eur J Clin Nutr 1998;52:924-928.

9 Fernandes G, Velangi A, Wolever TMS: Glycemic index of potatoes commonly consumed in North America. J Am Diet Assoc 2005;105:557-562.

10 Foster-Powell K, Holt SHA, Brand-Miller JC: International table of glycemic index and glycemic load values: 2002. Am J Clin Nutr 2002;76:5-56.

11 Franz MJ: Protein and diabetes: much advice, little research. Curr Diab Rep 2002;2:457-464.

12 Holt SHA, Brand-Miller JC, Petocz P: An insulin index of foods: the insulin demand generated by 1000-kg portions of common foods. Am J Clin Nutr 1997;66:1264-1276.

13 Wolever TMS, Chiasson J-L, Hunt JA, et al: Similarity of relative glycaemic but not relative insulinaeic responses in norm, IGT, and diabetic subjects. Nutr Res 1998;18:1667-1676.

14 Collier GR, Giudici S, Kalmusky J, et al: Low glycaemic index starchy foods improve glucose control and lower serum cholesterol in diabetic children. Diabetes Nutr Metab 1988;1: 11-19.

15 Fontveille AM, Acosta M, Rizkalla SW, et al: A moderate switch from high to low glycaemic-index diets for 3 weeks improve metabolic control of type I (IDDM) diabaetic subjects. Diabetes Nutr Metab 1988;1:139-143.

16 Fontvieille AM, Rizkalla SW, Penformis A, et al: The use of low glycaemic index foods improves metabolic control of diabetic subjects over five weeks. Diabet Med 1992;9: 444-450.

17 Lafrance L, Rabasa-Lhoret R, Poisson D, et al: The effects of different glycaemic index foods and dietary fibre intake on glycaemic control in type 1 diabetic patients on intensive insulin therapy. Diabet Med 1998;15:972-978.

18 Jenkins DJA, Wolever TMS, Buckley G, et al: Low glycemic index starchy foods in the diabetic diet. Am J Clin Nutr 1988;48:248-254.

19 Brand JC, Colagiuri S, Crossman D, et al: Low glycemic index foods improve long-term glycemic control in NIDDM. Diabetes Care 1991;14:95-101.

20 Wolever TMS, Jenkins DJA, Vuksan V, et al: Beneficial effects of low-glycemic index diet in type 2 diabetes. Diabet Med 1992;9:451-458.

21 Wolever TMS, Jenkins DJA, Vuksan V, et al: Beneficial effect of low-glycaemic index diet in overweight NIDDM. Diabetes Care 1992;15:562-564.

22 Frost G, Wilding S, Beecham J: Dietary advice based on the glycaemic index improves dietary profiles and metabolic control in type 2 diabetic patients. Diabet Med 1994;11:397-401.

23 Luscome ND, Noakes M, Clifton PM: Diets high and low in glycemic index versus high monounsaturated fat diets: effects on glucose and lipid metabolism in NIDDM. Eur J Clin Nutr 1999;53:473-478.

24 Jarvi A, Karlstrom B, Grandfeldt Y, et al: Improved glycaemic control and lipid profile and normalized fibrinolytic activity on a low glycemic index diet in type 2 diabetic patients. Diabetes Care 1999;22:10-18.

25 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 202:21:120-127.

26 Komindr S, Lerdvutrisopon N, Ingsriswang S, et al: Effect of long-term intake of Asian food with different glycemic indices on diabetic control and protein conservation in type 2 diabetic patients. J Med Assoc Thai 2001;84:85-97.

27 Rizkalle SW, Taghrid L, laromiguiere M, et al: Improved plasma glucose control, whole-body glucose utilization, and lipid profile on a low-glycemic index diet in type 2 diabetic men. Diabetes Care 2004;27:1866-1872.

28 Jimenez-Cruz A, Bacardi-Gascon M, Turnbull WH, et al: A flexible, low-glycemic index Mexican-style diet in overweight and obese subjects with type 2 diabetes improves metabolic parameters during a 6-week treatment period. Diabetes Care 2003;26:1967-1970.

29 Brand-Miller J, Hayne S, Petocz P, Colagiuri S: Low-glycemic index diets in the management of diabetes: a meta-analysis of randomized controlled trials. Diabetes Care 2003;26: 2466-2468.

30 Giacco R, Pariool M, Rivellese AA, et al: Long-term dietary treatment with increased amounts of fiber-rich, low-glycemic index natural foods improves blood glucose control and reduces the number of hypoglycemic events in type 1 diabetic patients. Diabetes Care 2000;23: 1461-1466.

31 Meyer KA, Kushi LH, Jacobs DR Jr, et al: Carbohydrates, dietary fiber, and incident type 2 diabetes in older women. Am J Clin Nutr 2000;71:921-930.

32 Feskens EJ, Loeber JG, Kromhout D: Diet and physical activity as determinants of hyperinsu-linemia: the Zutphen Elderly Study. Am J Epidemiol 1994;140:350-360.

33 McKeown NM, Meigs JB, Liu S, et al: Carbohydrate nutrition, insulin resistance, and the prevalence of the metabolic syndrome in the Framingham Offspring Cohort. Diabetes Care 2004;27:538-546.

34 Stevens J, Ahn K, Juhaeri, et al: Dietary fiber intake and glycemic index and incidence of diabetes in African-American and white adults: the ARIC study. Diabetes Care 2002;25: 1715-1721.

35 Lau C, Faerch K, Glumer C, et al: Dietary glycemic index, glycemic load, fiber, simple sugars, and insulin resistance: the Inter99 study. Diabetes Care 2005;28:1397-1403.

36 Crapo PA, Reaven G, Olefsky J: Postprandial plasma-glucose and -insulin responses to different complex carbohydrates. Diabetes 1977;26:1178-1183.

37 Raben A: Should obese patients be counseled to follow a low-glycaemic index diet? No. Obes Rev 2002;3:245-256.

38 Pawlak DB, Ebbeling CB, Ludwig DS: Should obese patients be counseled to follow a low-glycaemic index diet? Yes. Obes Rev 2002;3:235-243.

39 Pastors JG, Franz MJ, Warshaw H, et al: How effective is medical nutrition therapy in diabetes care? J Am Diet Assoc 2003;103:827-831.

40 UK Prospective Diabetes Study 7: Response of fasting plasma glucose to diet therapy in newly presenting type II diabetic patients, UKPDS Group. Metabolism 1990;39:905-912.

41 Franz MJ, Monk A, Barry B, et al: Effectiveness of medical nutrition therapy provided by dietitians in the management of non-insulin-dependent diabetes mellitus: a randomized, controlled clinical trial. J Am Diet Assoc 1995;95:1009-1017.

42 Goldhaber-Fiebert JD, Goldhaber-Fiebert SN, Tristan ML, Nathan DM: Randomized controlled community-based nutrition and exercise intervention improves glycemia and cardiovascular risk factors in type 2 diabetic patients in rural Costa Rica. Diabetes Care 2003;26: 24-29.

43 Ziemer DC, Berkowitz KJ, Panayioto RM, et al: A simple meal plan emphasizing healthy food choices is as effective as an exchange-based meal plan for urban African Americans with type 2 diabetes. Diabetes Care 2003;26:1719-1724.

44 Lemon CC, Lacey K, Lohse B, et al: Outcomes monitoring of health, behavior, and quality of life after nutrition intervention in adults with type 2 diabetes. J Am Diet Assoc 2004; 104: 1805-1815.

45 Sadur CN, Moline N, Costa M, et al: Diabetes management in a health maintenance organization. Efficacy of care management using cluster visits. Diabetes Care 1999;22: 2011-2017.

46 Rickheim PL, Weaver TW, Flader JL, Kendall DM: Assessment of group versus individual diabetes education: a randomized study. Diabetes Care 2002;25:269-274.

47 Polonsky WH, Earles J, Smith S, et al: Integrating medical management with diabetes self-management training: a randomized control trial of the Diabetes Outpatient Intensive Treatment program. Diabetes Care 2003;26:2048-2053.

48 Banister NA, Jastrow ST, Hodges V, et al: Diabetes self-management training program in a community clinic improves patient outcomes at modest cost. J Am Diet Assoc 2004; 104: 807-810.

49 Delahanty LM, Halford BN: The role of diet behaviors in achieving improved glycemic control in intensively treated patients in the Diabetes Control and Complications Trial. Diabetes Care 1993;16:1453-1458.

50 Kulkarni K, Castle G, Gregory R, et al: Nutrition Practice Guidelines for Type 1 Diabetes Mellitus positively affect dietitian practices and patient outcomes. The Diabetes Care and Education Dietetic Practice Group. J Am Diet Assoc 1998;98:62-70.

51 Pieber TR, Brunner GA, Schnedl WJ, et al: Evaluation of a structured outpatient group education program for intensive insulin therapy. Diabetes Care 1995;18:625-630.

52 DAFNE Study Group: Training in flexible, intensive insulin management to enable dietary freedom in people with type 1 diabetes: dose adjustment for normal eating (DAFNE) randomised controlled trial. BMJ 2002;325:746.

53 Franz MJ: The glycemic index: not the most effective nutrition therapy intervention. Diabetes Care 2003;26:2466-2468.

Discussion

Dr. Katsilambros: Ms. Franz and Dr. Slama, I understand that existing studies in humans comparing low versus high glycemic index (GI) diets do not show any real weight change. However, during the previous discussion I mentioned that there are experimental animal studies that do show a weight change between low and high GI diets. I have found the slide from the study and with your permission I would like to show it.

Ms. Franz: While Dr. Katsilambros gets ready to show the slide, I would like to make a comment on satiety studies. Although subjects may report feeling more satisfied after consuming different meals, this doesn't always translate into eating fewer calories. For example, Stubbs et al. [1] in a 1-day study reported that although subjective hunger was less after a high protein breakfast compared to a high fat or high carbohydrate breakfast, lunch time intake 5 h later and energy intake for the rest of the day were similar after all three breakfasts. Currently the majority of research on satiety is very short-term and the effect of satiety on future calorie intake is rarely studied. While we wait for the slide does anyone else have a comment or questions?

Dr. Slama: I would like to make three brief comments and ask you one question. To be fair you should quote Razels and Crapo and for European people Otto and Spater who published these results in 1973. They were first published in German and then in French, but they can still be found in Medline. The second thing is you said something which seems wrong to me: you say that adding milk to a portion of cereals will decrease the blood glucose. If you add a portion of skin milk to 50 g cereal, this will increase but not decrease blood glucose, unless you are using caribou milk which is very rich in lipids.

Ms. Franz: Thank you for your comment. What I meant to say is that if you combine a high GI cereal with milk, a low GI food, you lower the GI of the meal. The high GI of the cereal or the low GI of milk is not maintained and instead you have a moderate GI response.

Dr. Slama: My third remark is that we proponents of the low GI do not claim that the GI concept should be substituted by another concept, but it should be added to another concept. So my question is: how as a clinician can you make this claim if you have not tried it yourself?

Ms. Franz: I have used the concept of differing glycemic responses from foods with many patients. For example, when examining food and glucose records you often find glucose responses that do not seem to make sense by just looking at the total amount of carbohydrate eaten. A possible explanation may be that different carbohydrate foods do have differing glucose responses even when the total amount of carbohydrate is the same. If persons with diabetes observe that some foods consistently cause their post-meal glucose response to be higher than other foods, even when keeping the carbohydrate amount consistent, the next time they eat that food they can try eating less of it or, if on insulin, increase their insulin dose. So I agree with the concept that foods with equal amounts of carbohydrate may have differing post-meal glucose responses which can be helpful to patients. They can use their food and glucose test records to make food choices that can beneficially lower their post-meal glucose responses.

Dr Slama: You don't need to explain your concept to the patient. You only have to say eat that rather than that when you have the occasion or the choice. You don't have to explain the area under the curve and the ratio and to multiply by the age. You only have to give some very simple advice.

Ms. Franz: As a clinician, I am reluctant to suggest to patients that they should not eat potatoes because they have a high GI when I am not confident this is true. For example, while potatoes from Australia appear to have a high GI of 87-101, potatoes tested in the US and Canada had a moderate GI of 56-77 [2]. Therefore, my problem with the GI is with the variability and reliability of the published GI values.

Dr. Slama: Try it yourself and you will be convinced.

Dr. Katsilambros: This is a slide published in 2002 and these are rats studied over 32 weeks, not for 1 week. You see an enormous difference in weight, about 75 g at the end of 30 weeks. The upper line is high GI, the lower line is low GI. 75 g in a rat is something like 20 kg in a man. Still I absolutely agree and I expect that in humans this is not the case. But again in humans we are not absolutely sure how strictly the diet can be kept unless it is made in the laboratory and under close supervision. Finally I absolutely agree with you and Dr. Slama that this is an additive dietary treatment, it is not an alternative.

Dr. Mooradian: What was the strain of rats used in the study?

Dr. Katsilambros: I don't remember.

Dr. Mooradian: Because the strain makes a difference in terms of growth. One has to interpret these data as favorable in terms of weight reduction versus stunting of growth.

Ms. Franz: Were the diets comparable in digestible or available carbohydrate and calories?

Dr. Mooradian: I guess to be able to interpret that slide you need to know whether the rats were pair-fed and had exactly the same amount of calorie intake.

Dr. Katsilambros: Yes, I show isoenergetic.

Dr. Eshki: When looking at nutrition tools for diabetes, such as the carbohydrate count, GI and other nutrition tools, I believe all these methods are very effective. When providing consultation to patients, their diet must be customized. For instance, when an individual visits a tailor to have a suit made, the tailor is going to take the measurements and all other factors before customizing the suit. With my patients, I look at several factors, such as culture, lifestyle conditions, the patient's onset, peak and duration of medication and the dietary history, and based on that I customize the proper diet. I see all nutrition tools as useful and don't deny the effectiveness of one over the other. My question is, do you think the GI can be helpful in some way?

Ms. Franz: Yes, as I mentioned previously the GI can be a helpful tool for patients who keep food and blood glucose records. However, as a clinician my first priority is to provide a framework that patients can use to plan food choices and meals and that is based on what the individual with diabetes feels is feasible and realistic for them to implement. In managing diabetes, how much a person eats is more important than what he/she eats. Just because a food has a low GI does not mean people with diabetes can eat unlimited portions of that food without affecting their blood glucose levels. Portions do count! I have found it helpful if patients understand what foods contain carbohydrate; what are average carbohydrate portion sizes, and how many carbohydrate servings to eat for meals or snacks, if desired. To plan food choices and meals people with diabetes can use carbohydrate counting, exchange lists, or experience. People with diabetes use their own experience to determine what works for them and what doesn't, and the GI concept may help explain some of their experiences. If target blood glucose goals are not being met, decisions need to be made to determine if changes in food intake or in medical therapy (i.e. medications) are needed.

Dr. Hill: It is very interesting to have these two talks back to back. While we can change people's diets in the short-term, it is difficult to do this over the long-term. The question in my mind is whether the GI is a useful tool for long-term improvement of diets. Are people following the GI diet eating healthily? Do people know what to do with the message given by the GI? Are people able to stick with this concept more than other concepts? The best example is the recent Atkins diet craze which in the short-term is great at producing weight loss but in the long-term it doesn't seem to be able to do this.

Ms. Franz: There is little, if any, evidence that people with diabetes can in the long-term change the GI of their usual diet. In a 1-year study, children in the low GI group did have significantly better HbAlc levels than the group using a carbohydrate exchange diet [3]. However, the study reported no differences in mean GI between the 2 groups at study end and even the authors stated it was difficult to attribute the difference in HbAlc to diet when there was no apparent difference in the mean GI. The majority of studies comparing low and high GI diets have been short-term. Furthermore, it is likely that most people already eat a moderate GI diet and it is not known if this can be changed long-term to a low GI diet.

Dr. Hill: Some people have suggested putting the GI on food labels. As an educator, how do you think the population would handle that?

Ms. Franz: You would have to ask somebody from a country where GI values are included on a food label as to the usefulness of this information. As an educator, I find the most useful information on the food label to be the serving size expressed in portions that patients can understand and the total grams of carbohydrate in that serving size. Total calories and grams of fat, saturated fat and protein in the serving size are also useful information.

Dr Slama: I would like to make some comments on what has been said. First of all we do not promote chocolate, ice cream, pizza, because they have a low GI. We do not leave people with a list of low GI food, but with a list of low GI healthy food. If time is short one must do what one can, but for me nutritional education is a long running process. I do not tell my patient's right away that now they have to learn what the GI is. I come with it later on when I want to tune the results. So really it is a process which we have to take with precaution and time.

Ms. Franz: I would agree with you. Most patients need support long-term to make and maintain lifestyle changes and part of that support over time may be fine tuning some of their food choices using the GI concept. My concern is when low GI foods are promoted to the public as being healthy food choices, and low GI food become 'good' foods and high GI foods become 'bad' foods.

Dr. Slama: I agree that you have to take care of the amount of carbohydrate. But already diagnosed diabetic people are eating less carbohydrate than they should, and not too much.

Ms. Franz: That is an interesting comment about how much carbohydrate people with diabetes should be and are eating. In this regard, I find the report from the United Kingdom Prospective Diabetes Study on estimated dietary intakes of interest. The intent of the nutrition intervention was to encourage patients to eat 50-55% of their energy intake as carbohydrate, protein 10-15%, and fat 30-35%. Despite the intensive intervention, patients reported a similar proportion of their energy intake as carbohydrate (43%) as the general population, protein intake 21%, and fat 37% [4]. Males reported an estimated energy intake of ~ 1,800 kcal/day and females ~ 1,450 kcal/day. This suggests that people with diabetes eat a moderate carbohydrate diet and do not eat either a high or a low carbohydrate diet.

Dr. Gerasimidi-Vazeou: Regarding type-1 diabetic patients, taking only carbohydrate measurement and GI into consideration and omitting fat consumption is not sufficient to improve glycemic control. This is also true judging from the experience at our center. We live in a real world and our patients do not always follow our suggestions. Perhaps we should also take fat consumption into consideration because we know that in Western countries the latter is over 30% of the daily calorie intake.

Ms. Franz: I certainly agree with you. Patients with both type-1 and type-2 diabetes need also to pay attention to total caloric intake as well as the total meat and fat servings they eat. You can't just focus on carbohydrates.

References

1 Stubbs RJ, van Wyk MC, Johnstone AM, Harbron CG: Breakfasts high in protein, fat or carbohydrate: effect on within-day appetite and energy balance. Eur J Clin Nutr 1996;50:409-417.

2 Fernandes G, Velangi A, Wolever TM: Glycemic index of potatoes commonly consumed in North America. J Am Diet Assoc 2005;105:557-562.

3 Gilbertson HR, Brand-Miller JC, Thorburn AW, et al: The effect of flexible low glycemic index dietary advice versus measured carbohydrate exchange diets on glycemic control in children with type 1 diabetes. Diabetes Care 2001;24:1137-1143.

4 Eeley EA, Stratton IM, Hadden DR, et al: UKPDS 18: estimated dietary intake in type 2 diabetic patients randomly allocated to diet, sulphonylurea or insulin therapy. UK Prospective Diabetes Study Group. Diabet Med 1996;13:656-662.

Bantle JP, Slama G (eds): Nutritional Management of Diabetes Mellitus and Dysmetabolic Syndrome. Nestlé Nutr Workshop Ser Clin Perform Program, vol 11, pp 73-81, Nestec Ltd., Vevey/S. Karger AG, Basel, © 2006.

Low Glycemic Index Foods Should Play a Role in Improving Overall Glycemic Control in Type-1 and Type-2 Diabetic Patients and, More Specifically, in Correcting Excessive Postprandial Hyperglycemia

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