Food-Based Ingredients to Modulate Blood Glucose

CHAPTER FIVE

Food-Based Ingredients to Modulate Blood Glucose Pariyarath Sangeetha Thondre1 Functional Food Centre, Faculty of Health and Life Sciences, Oxford Brookes University, Oxford, United Kingdom 1 Corresponding author: e-mail address: [email protected]

Contents 1. 2. 3. 4. 5. 6.

Introduction Maintaining Normal Blood Glucose Levels: The Role of Food Blood Glucose and Chronic Diseases Factors Affecting Glycemic Index of Food Dietary Fiber and Blood Glucose Cereal-Based Ingredients 6.1 Barley 6.2 Oats 6.3 Rye 7. Fruit-Based Ingredients 8. Spices 9. Legume-Based Ingredients 10. Effect of Protein and Fat on Blood Glucose 11. Sugars and Sugar Alcohols 12. Concluding Remarks References

182 183 185 189 190 193 193 197 200 202 208 210 213 216 217 217

Abstract Maintenance of normal blood glucose levels is important for avoiding chronic diseases such as type 2 diabetes, cardiovascular problems, and obesity. Type 2 diabetes is one of the major health problems affecting the world population and this condition can be exacerbated by poor diet, low physical activity, and genetic abnormalities. Food plays an important role in the management of blood glucose and associated complications in diabetes. This is attributed to the ability of food-based ingredients to modulate blood glucose without causing any adverse health consequences. This chapter focuses on four important food groups such as cereals, legumes, fruits, and spices that have active ingredients such as soluble dietary fiber, polyphenols, and antinutrients with the ability to reduce glycemic and insulin response in humans. Other food ingredients such as simple sugars, sugar alcohols, and some proteins are also discussed in moderation.

Advances in Food and Nutrition Research, Volume 70 ISSN 1043-4526 http://dx.doi.org/10.1016/B978-0-12-416555-7.00005-9

#

2013 Elsevier Inc. All rights reserved.

181

182

Pariyarath Sangeetha Thondre

1. INTRODUCTION Blood glucose is one of the simplest physiological measures that can be determined easily, using simple hand-held devices or advanced clinical analyses. It plays a significant role in the maintenance of a healthy body and also in preventing many chronic diseases. Maintaining healthy and normal blood glucose levels is important for avoiding cardiovascular diseases and obesity. The prevalence of cardiovascular diseases and obesity results in the development of hyperglycemia or high blood glucose. One of the major health problems associated with uncontrolled blood glucose levels is diabetes mellitus. There are different types of diabetes such as type 1, type 2, and gestational diabetes. Type 1 diabetes is caused by an autoimmune condition leading to defects in the insulin-secreting pancreatic b-cells resulting in the inability of the body to secrete sufficient amount of insulin (Diabetes UK, 2013a). On the other hand, type 2 diabetes develops due to the inability of the body to use the insulin produced by the pancreas effectively to manage the increase in blood glucose levels (Diabetes UK, 2013b). This condition can be exacerbated by poor diet, low physical activity, and genetic factors. Type 2 diabetes is a major health problem, not only in developed countries but also in developing countries all over the world due to changes in diet and lifestyle. Gestational diabetes is the type of diabetes that occurs in women during either the second or third trimester of pregnancy or becomes evident in the early stages of pregnancy because of its undetected existence before pregnancy (Diabetes UK, 2013c). In addition to these three types of diabetes, there is an emerging condition called prediabetes that is increasing in prevalence worldwide. Prediabetes is also known as impaired glucose tolerance or impaired fasting glucose, the condition in which the blood glucose levels are not high enough to be categorized as type 2 diabetes, but if left uncontrolled may progress to type 2 diabetes (Diabetes UK, 2013d). According to the International Diabetes Federation, there are around 371 million diabetic people worldwide (Diabetes Atlas, 2012). This number has been showing an increasing trend and furthermore there are a number of people undiagnosed for diabetes worldwide. A good majority of people with diabetes are living in low- and middle-income countries where the diet is not monitored or controlled to maintain a normal blood glucose level. Diabetes can result in a number of complications affecting several organs in the body (Table 5.1). Poor blood glucose control can also lead to psychological problems such as depression and impaired cognitive function (Anderson, Freedland, Clouse, & Lustman, 2001; Haffner, Lehto,

183

Food-Based Ingredients to Modulate Blood Glucose

Table 5.1 Diabetes-related complications (Diabetes Atlas, 2012) Complication Organ affected

Retinopathy

Eyes

Cerebrovascular diseases

Brain

Coronary heart diseases

Heart

Nephropathy

Kidney

Neuropathy

Nerves

Peripheral vascular disease

Limbs

Amputation

Lower limbs

Ronnemaa, Pyorala, & Laakso, 1998; Huxley, Barzi, & Woodward, 2006; Lustman & Clouse, 2005; Niskanen, Turpeinen, Penttila, & Usitupa, 1998; Ohkubo et al., 1995; UK Prospective Diabetes Group, 1998). Not only is the maintenance of normal fasting blood glucose important for the prevention of diabetes, but postprandial blood glucose monitoring is also important to prevent the microvascular complications arising due to diabetes. The WHO defines normal postprandial glucose tolerance as indicated by <7.8 mmol/l after 2 h following a 75-g glucose load in an oral glucose tolerance test (World Health Organization, 2006). Postprandial hyperglycemia is also a cause for oxidative stress and endothelial dysfunction as shown by many studies (Ceriello et al., 2004; Kawano et al., 1999).

2. MAINTAINING NORMAL BLOOD GLUCOSE LEVELS: THE ROLE OF FOOD Food plays an important role in the management of blood glucose in diabetes and associated complications. Carbohydrates are an integral part of our diet and it is recommended that they form one third of our daily diet. The blood glucose levels after consumption of different types of carbohydrates may vary and this can potentially have an impact on the development of many chronic diseases in the present-day world. Increase in plasma glucose is linked to cardiovascular diseases and type 2 diabetes along with other complications associated with it mediated by high insulin levels, high glycated hemoglobin, increased plasma triacylglycerols, endothelial dysfunction, and oxidative stress (Riccardi, Rivellese, & Giacco, 2008). Research has shown that not only is the quantity of carbohydrates important, but their quality is also equally important in maintaining optimal glucose levels. Both

184

Pariyarath Sangeetha Thondre

the chemical classification of carbohydrates into mono-, di-, oligo-, and polysaccharides as well as the physiological classification into glycemic and nonglycemic carbohydrates are relevant in their role in elevating or modulating blood glucose. Hence, determining the glycemic index (GI) of foods is a very useful technique for assessing the quality of carbohydrate foods. This simple and straightforward measure of carbohydrate quality needs to be promoted and adapted by clinicians while providing nutritional advice to diabetic patients not only for managing normal glycemic control but also to control the associated complications related to lipid profile, blood pressure, and weight management (Kirpitch & Maryniuk, 2011). GI may be defined as a measure of the ability of a food product to raise blood glucose. The glycemic effects of carbohydrates are measured by their ability to raise blood glucose levels above the baseline for 2–3 h after consumption. This measure of postprandial increase in blood glucose allows the derivation of a numerical value called GI that can be used for categorizing carbohydrate foods as beneficial or harmful for our health. GI is expressed as a percentage of the value obtained by calculating the ratio of the incremental area under the glucose curve for a food containing typically 50 g available carbohydrate to the incremental area under the glucose curve of 50 g of a reference food that is pure glucose ( Jenkins et al., 1981). Although the quality of carbohydrate is indicated by GI, the quantity of carbohydrate consumed is equally important and this led to the coining of another term called glycemic load (GL), which is the product of GI of a food and the amount of carbohydrates in a serving of that food. Burkitt and Trowell (1977) first proposed that the risk associated with metabolic diseases such as diabetes and coronary heart diseases may be reduced by increasing the consumption of slowly absorbed carbohydrates such as those in dietary fiber. Their “fiber hypothesis” was then extended into the concept of GI by Jenkins and coworkers ( Jenkins, Kendall, Augustin, Franceschi, et al., 2002; Jenkins, Kendall, Augustin, Martini, et al., 2002), who first published the index classifying 62 commonly consumed foods based on their effect on postprandial blood glucose in human subjects ( Jenkins et al., 1981). Ever since, a number of foods have been tested all over the world to generate the International Table of GI and GL values for 2487 individual food items, citing 205 separate studies (Atkinson, Foster-Powell, & Brand-Miller, 2008). This has served as the most comprehensive list of all food items allowing us to ensure normal glycemic control based on the published values of GI and GL in both healthy and diabetic subjects. GI is the measure of the change in blood glucose concentration following the consumption of a food based on a constant level of

Food-Based Ingredients to Modulate Blood Glucose

185

available carbohydrates. All the foods have to be compared based on the similar available carbohydrate levels, which is mostly 50 g using most foods and in some cases may be reduced to 25 g if the portion size of the food to be tested is too large with 50 g available carbohydrates. For this reason, this measure is dependent on the quality of carbohydrates rather than the quantity of the carbohydrates and does not always reflect the typical amount of carbohydrate that is normally present in a portion of a particular food item (Sheard et al., 2004). GI is calculated by measuring the postprandial glucose levels over 2 or 3 h after consumption of the test foods and comparing it with the blood glucose response following a reference food, such as glucose or white bread with equivalent amount of available carbohydrates (Jenkins et al., 1981). This value is then represented as a percentage to give the GI of the food. The blood glucose response is usually represented as the area under the blood glucose curve, which often shows a positive relation with the glycemic quality of the food. High-GI foods are characterized by greater glucose area under the curve and low-GI foods have lesser glucose area under the curve (Foster-Powell, Holt, & Brand-Miller, 2002). In order to consider both the quality and quantity of the foods in a typical serving of a food, another measure called GL was developed that allowed the determination of the glycemic response to a portion of the food (Beulens et al., 2007). GL is calculated as the product of the GI of a food and the available carbohydrate in a serving size of that food. This helps the general public to control the portion sizes of foods based on their GI values in order to achieve a low GL value. Irrespective of the availability of these two measures, GI and GL, at times it is sensible to compare different foods just based on their glycemic response postprandial because of their effects on other physiological characteristics such as insulin response and lipid profile (Schenk, Davidson, Zderic, Byerley, & Coyle, 2003).

3. BLOOD GLUCOSE AND CHRONIC DISEASES The effect of GI on health outcomes in intervention studies has reported improvements in insulin sensitivity, b-cell function, dyslipidemia, and thrombolytic function. However, there were mixed results due to studies varying in duration, sample size, subject type, and intervention diet that did not match for energy, macronutrient, or fiber content. The risk of developing type 2 diabetes has been found to be increased by 37% in men and women whose diet came under the highest quintiles of energy-adjusted GI compared with the lowest quintiles (Salmeron, Ascherio, et al., 1997; Salmeron, Manson, et al., 1997). However, in a 6-year follow-up of

186

Pariyarath Sangeetha Thondre

35,988 postmenopausal women from the Iowa Women’s Health Study, no relationship was found between GI and diabetes risks (Meyer et al., 2000). These inconsistent results may be due to the use of food-frequency questionnaires that were not designed to measure GI and thereby resulted in incorrect assessment of GI. Several studies have investigated the effects of a low-GI diet on insulin sensitivity. In 30 patients with advanced Coronary Heart Disease (CHD), a 10-unit reduction in dietary GI from 86 to 76 resulted in improved insulin sensitivity in 4 weeks in subjects in the low-GI group compared with the high-GI group (Frost, Keogh, Smith, Akinsanya, & Leeds, 1996). In another study, when GI was reduced by 24 units from 91 to 67 in the diet of 16 women at increased risk of CHD, insulin sensitivity was improved in those under a low-GI diet for 3 weeks, compared with the high-GI group (Frost, Leeds, Trew, Margara, & Dornhorst, 1998). An interesting result from this study was that the effects of lowering GI were not seen in control subjects with no parental history of CHD, suggesting that those subjects who already have some extent of insulin resistance might get the most benefits of a low-GI diet. This was supported by another study in which no effects of a low-GI diet on insulin sensitivity was observed in seven lean insulinsensitive men following nutrient-matched high- and low-GI diets (mean GI difference 24) for 30 days (Kiens & Richter, 1996). Further, Sloth et al. (2004) did not find any effect on insulin sensitivity or b-cell function in a 10-week parallel study of 45 overweight women who consumed lowor high-GI foods incorporated into ad libitum habitual diets. Low-GI diets were found to improve insulin secretion in some studies. Insulin secretion from pancreatic b-cells was found to be improved by a low-GI diet in subjects with impaired glucose tolerance after 4 months although the difference in mean GI from a high-GI diet was only 4 units (Wolever & Mehling, 2002). Although the authors remarked that this effect could be partly due to the high fiber intake with the low-GI diet, it must not be forgotten that presence of fiber in itself could lower GI of foods. A similar situation is evident in an 8-week crossover study in 20 postmenopausal women who consumed high-fiber rye bread and white wheat bread ( Juntunen, Laaksonen, Poutanen, Niskanen, & Mykkanen, 2003). The rye bread, which was high in fiber, phytates, and tannins, had a lower GI than wheat bread thereby resulting in enhanced insulin secretion suggesting an improvement in b-cell function. Low-GI foods produce an attenuated glucose response, which regulates the responses of other hormones such as insulin and glucagon. A high-insulin response generated by high-GI foods results in the glucose uptake and glycogen synthesis in skeletal

Food-Based Ingredients to Modulate Blood Glucose

187

muscle and liver, and increases lipogenesis in adipose tissue. Simultaneously, there is suppression of gluconeogenesis, glucose output by liver, and lipolysis. The rapid absorption of nutrients following a high-GI meal slows down the rate of entry of exogenous glucose into the circulation. However, the storage of nutrients continues and glucose mobilization from tissues remains suppressed due to the effects of high insulin and glucagon levels. This results in a hypoglycemic episode below fasting levels that triggers release of counter-regulatory hormones, including glucagon, adrenaline, and growth hormone. These hormones act to restore circulating fuel levels by increasing hepatic glucose output and decreasing glucose uptake by skeletal muscle alongside triggering lipolysis and causing an increase in circulating nonesterified fatty acid (NEFA) released by adipose tissue (Wolever, BentumWilliams, & Jenkins, 1995). Following the consumption of a low-GI meal, there is a prolonged and continued absorption of nutrients from the gastrointestinal tract, the hypoglycemic episode does not occur, and the return of blood glucose to the baseline level is delayed. This slower release of nutrients and gradual drop in blood glucose levels allow adjustment of hepatic glucose output to maintain circulating glucose levels without dramatic rises and falls, or a large rebound in NEFA levels. Low-GI diets therefore give a more stable diurnal profile, reducing postprandial hyperglycemia and hyperinsulinemia, and attenuating late postprandial rebounds in circulating NEFA, all factors that exacerbate various components of the metabolic syndrome (Aston, 2006). Low-GI diets may contribute to modest weight loss or reduction of weight gain via their effects on reductions in energy intake. Low-GI foods may increase satiety and delay the return of hunger in comparison with highGI foods, which may be translated into reduced energy intake at later meals. The hormonal environment following a high-GI meal reduces the availability of the two major metabolic fuels (glucose and fatty acids), signaling a fasted state. Hypoglycemia is a signal for hunger, and the rate of change of blood glucose may also be important, with more rapid falls triggering more rapid return of hunger (Pawlak, Ebbeling, & Ludwig, 2002). The hypoglycemic undershoot frequently seen following high-GI meals would therefore be predicted to trigger hunger. In one study by Ludwig et al. (1999), blood glucose levels strongly predicted the energy consumption at a subsequent meal with subjects eating more following a high-GI breakfast than following a low-GI breakfast. The variability in energy intake following breakfast of low- and high-GI was predicted also by circulating fatty acid levels in this study. Initial low levels of NEFA as a result of the high-insulin response to high-GI foods may also trigger hunger. Holt and Miller (1994)

188

Pariyarath Sangeetha Thondre

found similar results when they related grains at various levels of processing to satiety. Satiety was inversely related to the area under the insulin response curve for various meals, with increased processing of grains increasing glucose and insulin responses and decreasing satiety ratings. Another mechanism responsible for satiety effects of low-GI foods may be reduction in gastric emptying. Many low-GI foods are high in fiber, which prolongs distension of the gastrointestinal tract, causing increased and prolonged secretion of the gut peptides cholecystokinin, ghrelin, glucagon, glucagon-like-peptide-1, and glucose-dependent insulinotropic polypeptide, all of which have been suggested as potential satiety factors (Burton-Freeman, Davis, & Schneeman, 2002; Pawlak et al., 2002). Most of the short-term feeding studies that have investigated the effects of lowGI meals on subsequent satiety, hunger, and energy intake have used meals that differ in aspects other than GI, thereby resulting in inconsistent results. A meta-analysis of crossover studies investigating the effects of low- and high-GI preloads by Roberts (2000) has found a significant increase in energy intake following high-GI meals when compared with low-GI meals. Another review by Raben (2002) comparing studies using low-GI and highGI preloads found that low-GI meals decrease hunger or increase satiety in half of the studies compared. The effect of low-GI meals on lowering energy intake at a later meal was also evident in 6 of the 12 studies compared. Both the above-mentioned reports are reliable as the studies dealt with diets matched in energy, macronutrient, and fiber contents. However, these studies did not result in weight loss in any group. In a study in which a low-GI diet was compared with a standard hypoenergetic reduced-fat diet for 4 months in 107 obese, but otherwise healthy, children (Spieth et al., 2000), reductions in weight and BMI were achieved with the low-GI diet, but not with the standard treatment. The study was limited by the fact that there could have been selection bias resulting from no randomization of subjects. A limitation of diets that match energy content is that they reduce the possibility of effects via satiety mechanisms. Only a few studies have investigated effects of ad libitum low-GI diets on weight, which include a 10-week parallel trial in 45 overweight women (Sloth et al., 2004) subjects who were instructed to incorporate low- or high-GI versions of carbohydrate-rich foods into their diets, to replace 75% of the carbohydrate intake along with the rest of their ad libitum habitual diets. A reduction in GI by 24 units did not result in any significant weight loss, energy intake, or fat mass between the groups. Contradictory results were obtained in another study using 20 normal weight women who consumed ad libitum high-starch

Food-Based Ingredients to Modulate Blood Glucose

189

(high-GI) and high-sucrose (low-GI) diets (Raben, Holst, Madsen, & Astrup, 2001; Raben, Macdonald, & Astrup, 1997). The high-GI diet resulted in weight loss, which was attributed to the high-fiber content and low-energy density of the diet by the authors. In another randomized crossover study of overweight men for 5 weeks each on low- and high-GI foods showed a trend toward greater decreases in body weight and energy intake on the low-GI diet compared with the high-GI diet (Bouche et al., 2002). However, a significant decrease (P < 0.05) in fat mass and a tendency to increase lean mass more (P ¼ 0.07) on the low-GI diet were reported in this study in which the diets differed by 30 units in GI.

4. FACTORS AFFECTING GLYCEMIC INDEX OF FOOD A number of factors influence the GI of food. Some of these factors are associated with the food, but others are the inherent characteristics of the subjects who consume the food (Table 5.2). Processing of food can result in the disruption of the physical and botanical food structure and alter the Table 5.2 Factors that influence glycemic response to foods Food characteristics

Amount of carbohydrate Type of sugar (sucrose, fructose, glucose, lactose) Nature of the starch (amylose, amylopectin, resistant starch) Cooking and food processing (degree of starch gelatinization, particle size, cellular form) Food structure (compactness, continuous matrix, viscosity, gel formation) Other food components (fat, protein, natural substances that slow digestion— lectins, phytates, tannins, starch-protein, and starch-lipid combinations) Subject characteristics

Fasting and preprandial glucose concentrations The severity of glucose intolerance The second meal or lente effect Fraser et al. (1990), Gannon, Nuttall, Westphal, Fang, and Ercan-Fang (1998), Hughes, Atchison, Hazelrig, and Boshell (1989), Jarvi, Karlstrom, Granfeldt, Bjorck, and Vessby (1995), Jenkins et al. (1982), Nielsen and Nielsen (1989), O’Dea, Snow, and Nestel (1981), Parillo, Giacco, Ciardullo, Rivellese, and Riccardi (1996), Rasmussen and Hermansen (1991), Schvarcz, Palmer, Aman, Lindkvist, and Beckman (1993), Snow and O’Dea (1981), Wolever, Nguyen, and Chiasson (1994).

190

Pariyarath Sangeetha Thondre

texture of foods and affect the breakdown of the amylose chain resulting in alteration of postprandial glycemic and insulin response (Bjorck, Granfeldt, Liljeberg, Tovar, & Asp, 1994). Studies using various foods such as legumes, cereals, and fruits have demonstrated this effect of processing on carbohydrate availability, digestibility, and in vivo glycemic response (Bjorck et al., 1994). In cereal grains, the refining process removes the indigestible fiber, leaving a pure starchy carbohydrate thus affecting the carbohydrate quality and increasing the glycemic impact of the grain. When whole grain flour is processed to white flour, its energy density increases by 10% due to loss of most of the dietary fiber present (Durtschi, 2001). This indicates that the glycemic impact of a food is lowered by increasing the dietary fiber content of a food (Riccardi et al., 2008). Other factors related to dietary fiber that lower the glycemic impact of foods are the viscosity, resistant starch content, and the compactness of food structures as demonstrated in potato dumplings (Riccardi et al., 2008). These studies suggest the need of future research in food technology to develop low-GI foods. A study using simple starchy foods such as bread, pasta, and potatoes in type 2 diabetes patients has shown that isoglucidic portions of these foods can elicit different glycemic responses with bread showing 68% increase and potatoes showing 48% increase in blood glucose than spaghetti (Parillo, Giacco, Riccardi, Pacioni, & Rivellese, 1985). Glycemic response is also affected by the different cooking procedures such as frying, boiling, baking, etc. (Giacco et al., 2001) due to alteration of some of the compounds such as starch, due to change in the content of dietary fiber, resistant starch, or due to changes in the physical food structure. Including unavailable carbohydrate in our foods either by simple addition or by replacing glycemic carbohydrates may be a viable strategy to manage their GI and GL. Many mechanisms are responsible for this effect. The inclusion of unavailable or lente carbohydrate interferes with starch digestion and absorption due to their viscous nature by either inhibiting amylase enzyme or increasing insulin sensitivity (Jenkins et al., 2000).

5. DIETARY FIBER AND BLOOD GLUCOSE Fiber is a well-researched ingredient that can modulate blood glucose. However, the effects depend upon various physicochemical properties of fiber such as solubility, molecular weight, etc. There have been contradictory reports on the dose of fiber required to result in a beneficial effect of

Food-Based Ingredients to Modulate Blood Glucose

191

blood glucose. While one study using 27 g fiber did not find any effect on glycemic response, another study using a soluble fiber, guar gum, showed favorable effects on lowering blood glucose. Very high doses of about 50 g fiber have also shown considerable improvement in glycemic response (Chandalia et al., 2000; Hollenbeck, Coulston, & Reaven, 1986; Jenkins et al., 1976). Another polysaccharide called glucomannan in Konjac has also been known to lower fasting plasma glucose in type 2 diabetic subjects. A daily dose of 3.6 g for 28 days reduced the fasting plasma glucose by 12.3% and postprandial blood glucose by 12.2 % due to its unique rheological properties that reduce carbohydrate digestion and absorption (Hsiao-Ling, Sheu, Tai, Liaw, & Chen, 2003). There is an abundance of evidence stating the effect of soluble dietary fiber sources in modulating glycaemia, the mechanism by which it causes the effect is sometimes controversial and highly debated. Food characteristics such as viscosity and fiber content along with the physical structure of food can all influence glycemic response dependent on their effects on starch accessibility (Riccardi et al., 2008). Bjorck and colleagues stated that dietary fiber lowers glycemic response due to its ability to increase gastrointestinal viscosity hampering postprandial glucose absorption rate and gastric emptying (Bjorck et al., 1994), thus leading to greater glycemic control (Chandalia et al., 2000) and improved insulin sensitivity (Ha & Lean, 1998). Chandalia et al. (2000) also showed that a high-fiber bolus can reduce gastrointestinal absorption of cholesterol by 10% and can lead to fat malabsorption. Ou and coworkers studied the soluble dietary fibers wheat bran, carboxymethyl cellulose, guar gum, and xanthan gum in vitro and highlighted increased gastrointestinal viscosity as one of the three mechanisms that could lower postprandial serum glucose levels, along with the binding of fiber to glucose and decreasing the glucose concentration available for uptake and the inhibition of a-amylase action by fiber through encapsulation of starch and direct inhibition of a-amylase, when testing in vitro (Ou, Kwok, Li, & Fu, 2001). The increase in gastrointestinal viscosity and decrease in gastric emptying rate increases satiety, which can lower overall energy intake, which can be indirectly linked to reducing obesity prevalence (Brown, Rosner, Willett, & Sacks, 1999). The viscosity properties of soluble dietary fiber are therefore most likely to be therapeutically useful in modifying postprandial hyperglycemia (Jenkins et al., 1978). There are a number of research studies showing the use of various natural soluble dietary fiber sources to modulate glycemia. Some of the popularly used soluble fibers in the food industry include guar gum, locust bean

192

Pariyarath Sangeetha Thondre

gum, and xanthan gum. In specific studies that determined the effect of guar gum in attenuating postprandial glycaemia, it was found that 5 g guar gum in bread and 5 g guar gum in soup significantly reduced both postprandial glucose and insulin, compared to their respective controls (Roberts, 2011; Wolever, Jenkins, Nineham, & Alberti, 1979). Similar results were obtained for the soluble fiber from fruits, pectin (Wolever, Spadafora, & Eshuis, 1991). Locust bean gum incorporated into food matrices significantly reduced its glycemic response and index, but the improvement in insulin response was not significant (Feldman et al., 1995). The mixed effect of soluble fire on glycemic response has also been investigated by Edwards et al. (1987), who showed that xanthan gum alone and mixed with locust bean gum at a ratio of 1:1 exhibited reduced postprandial glycemic response. Human studies have not reported the use of the soluble fiber, Gum arabic. But, in animal studies, the Arabic gum that elicited significant hypoglycemic effects on normal rats, however, failed to produce hypoglycemic effects on rats induced with diabetes (Grover, Yadav, & Vats, 2002). Further investigation in rabbits showed evidence that the hypoglycemic effect was due to the initiation of insulin release from pancreatic b-cells (Grover et al., 2002), and thus its application is useful in insulin improvement. Plantago psyllium mucilage has been shown to reduce GI of bread and postprandial glycemic response in normal and type 2 diabetic humans (Munari, Benitez-Pinto, Araiza-Andraca, & Casarrubias-Moises, 1998). The use of 5 g of yellow mustard bran containing yellow mustard mucilage in a soup meal has shown reduction in glycemic response compared with a matched control in healthy male volunteers (Lett, Thondre, & Rosenthal, 2013). The beneficial effect may not be due to the fat content of the meal but due to the presence of the mucilaginous compound. Fiber in general was thought to modulate glycemic response. However, there are some reports that did not show positive results. For example, when type 2 diabetes subjects were given a 3-month intervention with 19 g/day cereal fiber from wheat and compared with a low-fiber (4 g/day) control phase of same duration, no effect was noticed in blood glucose or HbA1c levels suggesting the need to increase the duration of the study ( Jenkins, Jenkins, Zdravkovic, Wu¨rsch, et al., 2002; Jenkins, Kendall, Augustin, Franceschi, et al., 2002; Jenkins, Kendall, Augustin, Martini, et al., 2002). Another important factor to consider is the lack of viscosity generation property in insoluble fiber from wheat bran. Although there are a number of food ingredients that have the ability to modulate blood glucose, this chapter will focus on four important food

Food-Based Ingredients to Modulate Blood Glucose

193

groups such as cereals, legumes, fruits, and spices that have active ingredients with the ability to reduce glycemic and insulin response in humans.

6. CEREAL-BASED INGREDIENTS Cereals are an important staple consumed worldwide in different forms such as breads, breakfast cereals, porridges, bakery products, etc. Some cereals are rich in specific ingredients that have the ability to influence the blood glucose levels. While common cereals such as rice and wheat are not regarded as containing functional ingredients, less-common cereals such as oats, barley, and rye are reported to be rich in soluble fiber and phytochemicals that can help maintain blood glucose and insulin levels. Insoluble fiber has also shown some effect on modulating blood glucose especially after the second meal. When a high-fiber cereal was compared with a low-fiber cereal and white bread and then followed by an ad libitum meal after 75 min, the blood glucose response before the ad libitum meal was not different. But, after the ad libitum pizza meal, the blood glucose was modulated in the case of the high-fiber cereal (Samra & Anderson, 2007). The high-fiber cereal had 33 g insoluble fiber compared to the low fiber, which had just 1 g and may have resulted in favorable results even after the second meal for reasons unknown. A comparison of the common starchy foods in China showed that brown rice had a high GI value compared to some other foods such as taro, adlay, yam, and mung bean noodles (Lin, Wu, Lu, & Lin, 2010). The result for brown rice was surprising irrespective of its high-fiber and resistant starch content. However, the authors assumed that the soaking process preceding cooking might have resulted in starch gelatinization and increase in glycemic response in healthy subjects. As expected, the mung bean noodles had low GI and other foods had medium GI.

6.1. Barley A healthy diet rich in dietary fiber could play an important role in the prevention of diabetes. b-Glucan is a soluble dietary fiber present in cereals as linear homopolymers of glucose linked via b-(1 ! 4) and b-(1 ! 3) linkage. Barley is an excellent source of b-glucan. b-Glucan incorporated into various food matrices has been shown to lower the GI of foods (Keogh, Lau, Noakes, Bowen, & Clifton, 2007; Poppitt, van Drunen, McGill, Mulvey, & Leahy, 2007). b-Glucan increases the viscosity in the stomach and small intestine thereby slowing gastric emptying and controlling nutrient

194

Pariyarath Sangeetha Thondre

absorption (Lazaridou & Billaderis, 2007; Ma¨kela¨inen et al., 2007). The efficacy of b-glucan as a potential functional food ingredient may be related to its structure, molecular weight, and rheological characteristics, which in turn can be affected by cooking and storage (Aman, Rimsten, & Andersson, 2004; Andersson et al., 2004). The use of barley b-glucan in foods with high GI could result in lowering the glycemic response and maintaining healthy blood glucose levels in people with IGT. However, the long-term effects of barley b-glucan on fasting blood glucose and HbA1c levels need to be tested to substantiate its role in maintaining healthy blood glucose levels. Cereal test meals with 0, 1, or 2 g b-glucan from barley were tested in overweight men and women (Kim, Behall, Vinyard, & Conway, 2006). The 2 g b-glucan test meals showed a significant lowering of glucose Area under the curve (AUC) in women only with no difference in the glycemic response of men. The authors did not explain the mechanism involved and suggested that unlike in men, a higher dose of b-glucan may be required to see a significant difference in postprandial glycemia. Barley and rye kernels as breakfast cereals have also been shown to reduce blood glucose postprandially and then for the whole day showing second meal effect (Nilsson, ¨ stman, Granfeldt, & Bjo¨rck, 2008). In this study, they were compared O with white bread, wheat kernels, oat kernels, whole-grain barley flour porridge, and white bread with barely dietary fiber. The beneficial effects of barley and rye kernels on the whole-day glucose tolerance were due to the high-fiber and indigestible starch content of those test meals, due to the presence of both soluble and insoluble fiber and also due to the specific food form in the form of kernels. In countries like Japan where high-GI food such as rice is used as a staple, mixing barley is a viable strategy to reduce the blood glucose response to meals. Sakuma et al. (2009) tested white rice mixed with 30% and 50% barley along with pure white rice and pure barley meals equivalent to 75 g available carbohydrate. The glucose and insulin areas under the curve were decreased dose-dependently using the barley-mixed rice meals that the authors attributed to the viscous soluble fiber content in barley. However, this is surprising given that the total dietary fiber content was only between 3% and 10% for the barley-based meals and studies using pure barley b-glucan has shown efficacy at 3% or above concentration. Hence, it may be assumed that the efficiency of b-glucan varies when it is in barley grain compared to when it is extracted and purified. Although high viscosity is usually reported to be responsible for the efficacy of barley b-glucan, some studies have reported the successful use of

Food-Based Ingredients to Modulate Blood Glucose

195

low-viscosity b-glucan for improvement in glucose tolerance and insulin sensitivity. When beverages formulated to supply 3 g or 6 g/day b-glucan were supplied to overweight and obese individuals for 12 weeks, there was a significant reduction in the glucose area under the curve following an oral glucose tolerance test, fasting insulin values, and also insulin resistance at the end of the intervention period (Bays et al., 2011). In addition to the b-glucan content in barley, the proportion of amylose and amylopectin has also been reported to be responsible for its low GI (King, Noakes, Bird, Morell, & Topping, 2008). A high-amylose barley called Himalaya 292 with high-fiber content was prepared into a breakfast cereal and compared with a traditional commercial barley cereal with three times less fiber content. When tested in healthy subjects, the GI of Himalaya 292 was 50 compared to 77 for the commercial barley cereal. Moreover, the high-amylose barley cereal reduced insulin response by 26% compared with the commercial barley cereal thereby substantiating its use in prevention and management of type 2 diabetes. This high GI for a commercial barley cultivar is not expected because barley is often referred to as a low-GI cereal. The same cereal Himalaya 292 was used in preparing bread and muffin and compared with similar test meals made of wheat in an earlier study (Keogh et al., 2007). However, this study did not show a significant effect on blood glucose but showed a significant lowering of insulin response in healthy subjects. These differences may have been due to the difference in food matrices, and the presence of other ingredients in making bread and muffin compared to just preparing a breakfast cereal. The beneficial effect of amylose on blood glucose response is due to its structural characteristics as a linear polymer of glucose less susceptible to gelatinization compared to the branched polymer amylopectin. Amylose also quickly undergoes retrogradation during cooling resulting in slow digestion and absorption. The type of starch with low amylose content is often termed as waxy starch. The use of normal and waxy starch from barley has also been tried in bread-making to evaluate their glycemic response. Finocchiaro et al. (2012) substituted 40% of wheat flour with the barley flour and found that in the presence of low amylose starch, the effect of b-glucan (6%) was not evident on the glycemic response of bread. The normal starch barley with the same amount of b-glucan (6%) reduced the GI of the bread while the waxy starch barley did not do so in the presence of b-glucan. This showed that even in the presence of b-glucan, the type of starch and the proportion of amylose and amylopectin have an important role in determining the glycemic response to food items such as bread.

196

Pariyarath Sangeetha Thondre

Addition of other ingredients such as lactic acid has shown further benefits on day-long glucose tolerance. Ostman, Liljeberg Elmsta˚hl, and Bjorck (2002) compared standard barley bread with a barley bread containing lactic acid in healthy subjects. They tested the glycemic response to a standard high-GI lunch after 4 h of consuming this low-GI breakfast. The results showed a significant reduction in glycemic and insulin response after the lunch following the barley bread with lactic acid. This showed the ability of lactic acid to lower glycemic response to a second meal. This may be in addition to the postprandial glycemic lowering effect after the breakfast although the authors did not measure it. Not all studies using barley b-glucan have demonstrated a lowering of glycemic response (Keogh et al., 2003; Smith, Queenan, Thomas, Fulcher, & Slavin, 2008). Differences in molecular weight and degree of purity of b-glucan have demonstrated contradictory results in glycemic response studies. In a randomized controlled trial, healthy human subjects consumed unleavened Indian flatbreads called chapatis containing highmolecular weight barley b-glucan at doses of 0, 2, 4, 6, and 8 g on different occasions (Thondre & Henry, 2009). The incremental area under the glucose curve values for all the five different types of chapatis were significantly low (P < 0.001) compared with reference food glucose. The GI values of chapatis with 4 and 8 g b-glucan were 43–47% lower (GI, 30 and 29, respectively) compared with chapatis without b-glucan (GI, 54). In another trial using a similar study design, healthy subjects who consumed flatbreads with a low-molecular-weight high-purity b-glucan did not show any significant difference in their blood glucose response (Thondre & Henry, 2011). Further in vitro studies investigating the mechanisms behind the above-mentioned glycemic response effects highlighted the role of this specific high-molecular weight-soluble dietary fiber in slowing down the particle breakdown of starchy foods such as flatbreads (Thondre, Monro, Mishra, & Henry, 2010). There was an inverse relation between the rate of in vitro starch digestion and amount of b-glucan in chapatis. The rate of starch digestion was influenced by the ability of chapatis to resist particle breakdown. This property along with the increase in viscosity of the food bolus was found responsible for the glycemic response effects of high-molecular weight barley b-glucan. The effect of high-purity barley b-glucan with low molecular weight was also tested on in vitro starch digestibility of chapatis. There was no significant difference in the amount of glucose released after in vitro digestion or in the glycemic response to chapatis with 0, 4, and 8% b-glucan (P > 0.05). It may be concluded that low-molecular-weight

Food-Based Ingredients to Modulate Blood Glucose

197

barley b-glucan, although of 75% purity, was not effective in lowering glycemic response possibly due to its inability to influence starch digestion and particle breakdown during in vitro digestion. The differences in the glycemic response to high- and low-molecular-weight barley b-glucan has been consistently found positive in a variety of food matrices used in further studies (Chillo, Ranawana, & Henry, 2011; Chillo, Ranawana, Pratt, & Henry, 2011; Clegg & Thondre, 2012). These results confirmed the efficacy of high-molecular weight b-glucan in lowering postprandial glycemic response irrespective of the food matrices, processing or cooking method involved. This allows the application of barley b-glucan in various foods and supplements for long-term trials. Although long-term maintenance or achievement of normal blood glucose concentrations is a beneficial physiological effect, the effect of b-glucan consumption on the long-term maintenance or achievement of normal blood glucose concentrations has not been proved by studies using barley grains or barley b-glucan preparations (EFSA, 2010).

6.2. Oats Oats and barley are two cereals researched extensively for their effect on glycemic response. Both the grains are rich in the soluble fiber b-glucan that has a gel-forming ability that delays gastric emptying and nutrient absorption in the intestine. The pioneering work on soluble fiber was by Jenkins et al. (1978) who tested gums added to glucose solution in healthy subjects and reported a correlation between the viscosity of the test meal and blood glucose concentration. Oat b-glucan-enriched products have been used in various forms. Tapola et al. tested oat bran flour in two different serving sizes consisting of 4.6 and 9.4 g b-glucan and compared it with oat bran crisps with 3 g b-glucan in type 2 diabetes subjects. While the oat bran flour reduced the glycemic response, the oat bran crisp had similar glycemic response as pure glucose load. When the oat bran flour was tested with and without a glucose drink, the addition of oat bran flour reduced the glycemic response to the glucose drink showing the effect of high b-glucan content in it (Tapola, Karvonen, Niskanen, Mikola, & Sarkkinen, 2005). This raised interest in the use of oats in different forms such as rolled oats, boiled rolled oats, boiled intact oat kernels, etc. for modulating blood glucose (Granfeldt, Hagander, & Bjo¨rck, 1995). Their results showed that the intact kernels were beneficial for lowering glucose and insulin levels than rolled oats suggesting the role of food structure rather than partial gelatinization of starch or the presence of viscous b-glucan. This indicated that a less disruptive process such as rolling of steamed oats could result in increased

198

Pariyarath Sangeetha Thondre

blood glucose response in comparison with intact whole grains of oats. The effect of food processing on glycemic response has also been well researched in oat-based foods. Granfeldt, Eliasson, and Bjo¨rck (2000) investigated the effect of increased starch gelatinization by food disruption on glycemic response in healthy subjects. They believed that oat and barley flakes prepared by incomplete gelatinization will lower the glycemic response. But, although there were differences between barley and oats, both the thin and thick flakes resulted in high glycemic response (Granfeldt, Eliasson, et al., 2000). Most of the breakfast cereals have a high GI as reported in the International Table of GI and GL values. But, simple changes to the processing methods could change their rate of starch gelatinization resulting in slow-release breakfast cereals. Although oats has high fat content, research has shown that the glycemic response attributed to oats is not dependent on the fat content (Tuomasjukka, Viitanen, & Kallio, 2007). They tested the effect of rolled oats, defatted rolled oats, rolled whole wheat cereal, and rolled whole wheat cereal with oat fat in healthy subjects. The rolled oats had 6.1% fat compared with 2.1% in wheat and defatted oat cereals. All the products had similar glycemic response suggesting that fat in oats has no role in its low-GI value. Research in the 1990s by Tappy et al. looked at the use of oat branenriched breakfast cereals with 4, 6, and 8 g of b-glucan in type 2 diabetes subjects. They found an inverse relationship between the dose of b-glucan and the glucose AUC in addition to the decrease in insulin compared to a control continental breakfast (Tappy Gugolz, & Wursch 1996). Long-term studies in type 2 diabetics lasting for 12 weeks were also carried out by using bread products with oat bran concentrate containing around 22% b-glucan. Both glycemic and insulin responses were improved at the end of the intervention period by the well-accepted bread products (Pick et al., 1996). Jenkins, Jenkins, Zdravkovic, Wu¨rsch, et al. (2002), Jenkins, Kendall, Augustin, Franceschi, et al. (2002), and Jenkins, Kendall, Augustin, Martini, et al. (2002) went on to quantify the extent of GI lowering on a wt. by wt. basis of b-glucan from oat products. Using two functional food products in the form of oat b-glucan-rich breakfast cereal and bar containing in comparison with a commercial oat-based cereal, they found that for each 1 g of b-glucan, the GI of foods could be lowered by approximately 4 units. This study in type 2 diabetes subjects resulted in low GI for both the products and demonstrated the potential of using this fiber-rich ingredient for management of blood glucose in type 2 diabetic subjects ( Jenkins, Jenkins, Zdravkovic, Wu¨rsch, et al., 2002; Jenkins, Kendall, Augustin,

Food-Based Ingredients to Modulate Blood Glucose

199

Franceschi, et al., 2002; Jenkins, Kendall, Augustin, Martini, et al., 2002). An additional ingredient that modulated glycemic response in these products was fructose used as a sweetener in these functional food products. The properties of b-glucan that resulted in reduced glycemic response include molecular weight, solubility, and viscosity. Oat bran muffins prepared with different concentration of b-glucan were tested in healthy subjects by Tosh, Brummer, Wolever, and Wood (2008). They noticed a dose-dependent effect of b-glucan with the 8 g samples showing a more positive effect on glycemia than a 4-g sample. There was a significant effect of molecular weight noticed on the peak blood glucose concentration, thus illustrating the importance of maintaining the molecular weight of b-glucan in the food samples during processing, cooking, and storage. A recent study on oat-based extruded cereals with b-glucan of varying molecular weight also showed an inverse relationship between the glucose AUC and the log10 molecular weight of b-glucan and log10 viscosity of the cereal extracts (Brummer, Duss, Wolever, & Tosh, 2012). Ma¨kela¨inen et al. looked at the effect of oat b-glucan in the form of a drink reconstituted from a powder on glycemic and insulin effects in healthy subjects. Oat bran powder with 2, 4, and 6 g b-glucan were also frozen to study the effect of freezing and thawing on the GI and II of the products. The 4 g dose was the best in lowering the GI and II of the drinks and the study showed that rather than the actual b-glucan content, the extractable b-glucan was better correlated to the glycemic and insulin response suggesting the possible role of solubility and the effect of freezing on the b-glucan availability (Ma¨kela¨inen et al., 2007). A recent study looked at the effect of food processing on the molecular weight, solubility, and viscosity of oat b-glucan and its effect on glycemic response in healthy subjects (Regand, Tosh, Wolever, & Wood, 2009). Different test meals such as crisp bread, porridge, granola, and pasta with 4 g b-glucan were used, among which porridge and granola were effective in maintaining the b-glucan molecular weight and lowering the postprandial glycemic response. The pasta and bread products were not as effective probably due to the depolymerization of b-glucan. The particle size of a test meal is also important in determining its effect on blood glucose response. Behall, Scholfield, and Hallfrisch (2005) compared oat flakes and flour in overweight women and found no effect of particle size on glycemic response. Although both the oat products reduced the glucose AUC by 29–36% and barley products (59–65%), the oat products did not have an effect on insulin response. The difference in b-glucan

200

Pariyarath Sangeetha Thondre

may have been responsible for this effect because the barley products had four times more b-glucan than the oat test meals. Unlike the effect of particle size noted in wheat bran products (Holt & Miller, 1994), in oat and barley products, the b-glucan effect surpassed the particle size effect. A difference in glycemic response has been reported for porridges made of steel cut oats and rolled oats. Steel cut oats resulted in lower glycemic response suggesting that the degree of processing may also play an important role in the glycemic response of oats (Gonzalez & Stevenson, 2011). Difference in the processing method during extraction of oat b-glucan could in turn affect its viscosity and the resultant glycemic response. Panahi, Ezatagha, Temelli, Vasanthan, and Vuksan (2007) compared an enzymatically extracted b-glucan and b-glucan extracted by aqueous method and found that the former was more effective in preserving the viscosity of the b-glucan thereby resulting in a 19.6% reduction in the glucose AUC compared to the latter b-glucan.

6.3. Rye Increased blood glucose and insulin are risk factors for metabolic syndrome in adults. Subjects showing symptoms of metabolic syndrome were assigned to a diet containing rye bread and pasta or oat and wheat bread and potato for 12 weeks (Laaksonen et al., 2005). There was no difference in the glucose measurements after an on oral glucose tolerance test in the subjects at the end of the intervention period. However, there was a small improvement in their insulin sensitivity following the rye bread consumption, probably due to increased pancreatic b-cell function. In an earlier study by the same group comparing different types of rye bread such as endosperm rye bread, traditional rye bread, and high-fiber rye bread prepared by sourdough fermentation, the blood glucose responses to the rye breads were similar to the wheat bread (Juntunen, Laaksonen, Autio, et al., 2003; Juntunen, Laaksonen, Poutanen, et al., 2003). However, the insulin responses to rye breads were significantly lower than the wheat bread. The fiber content was different between the four test breads with 2.7 g in wheat bread, 6.1 g in the endosperm rye bread, 15.2 g in the traditional rye bread, and 29 g in the high-fiber rye bread. There was no obvious effect of difference in fiber content between the rye breads, probably because the difference was mainly in the insoluble fiber levels rather than the soluble fiber content. The difference observed between wheat and rye breads was thus attributed to their different structure of the food matrix resulting in a compact structure in rye compared to a gluten-mixed network of starch forming a continuous phase in the wheat bread. Some differences in the particle size of the bread

Food-Based Ingredients to Modulate Blood Glucose

201

were also observed following chewing of the two breads due to difference in this food structure, which made the starch accessibility different in the two breads. The difference in response to insulin rather than glucose has also been highlighted in a study comparing rye products with other cereal grain products from wheat and oats. Juntunen et al. (2002) tested whole kernel rye bread, whole meal rye bread with oat b-glucan concentrate, dark durum wheat pasta, and white wheat bread in healthy subjects. The rye kernel bread had 60% rye kernels and the whole meal bread had 20% oat b-glucan concentrate. The whole kernel rye bread had significantly lower insulin response compared to the other test breads thus emphasizing the role of structure of food on physiological responses. The response was similar to that of the pasta with less fiber but a compact structure compared to the other two test breads. A long-term study using rye bread against white bread for 8 weeks in postmenopausal women also showed increased insulin secretion, which was attributed to the slow-digesting properties of the rye carbohydrates and also to the polyphenol compounds in rye that may serve as insulin stimulants (Juntunen, Laaksonen, Autio, et al., 2003; Juntunen, Laaksonen, Poutanen, et al., 2003). In women with impaired glucose tolerance and with history of gestational diabetes, low-GI breads were supplied for 3 weeks to see the effect on glucose and insulin response (Ostman, Frid, Groop, & Bjorck, 2006). There was a light and dark version of the test breads, the light containing sour dough, rye kernels, and oat bran concentrate with oat b-glucan. The dark bread also contained rye kernel and sourdough but no b-glucan from oats. Both the breads lowered the insulin response to a glucose tolerance test in the women after 3 weeks. However, there was no difference in the fasting plasma glucose or insulin. Foods that modulate blood glucose response can improve insulin sensitivity and reduce the incidence of metabolic syndrome. However, there are a number of reports that discuss the methodologies used for determination of the glucose response to a particular food. Hatonen et al. (2006) compared the use of capillary and venous blood sampling methods for determination of glycemic response to rye bread, oat meal porridge, and instant mashed potatoes. They found that the GIs calculated based on capillary blood glucose AUC were lower than that calculated using venous blood glucose measurements. However, another disadvantage with venous blood samples was the high individual variation compared to the capillary blood samples. Like many other studies, this trial also highlighted the need to use glucose as the reference food rather than white bread. Rye bread showed a high GI in this study and showed a lower insulin response. Contrary to many studies

202

Pariyarath Sangeetha Thondre

that show low-GI values for oat meal porridge, this study resulted in a highGI value. The instant mashed potato also showed a high-GI value similar to some of the previous studies. The study thus supported others reiterating the efficacy of capillary blood sampling and the repeated testing of the reference food, glucose or white bread, at least twice. Table 5.3 summarizes the studies that used cereal-based ingredients for modulating blood glucose in healthy subjects, and Table 5.4 illustrates the effect of cereal-based ingredients on the blood glucose levels in type 2 diabetic subjects.

7. FRUIT-BASED INGREDIENTS Other sources of polyphenols are also known to affect blood glucose in healthy and diabetic subjects. The effect of polyphenol-rich fruits is sometimes more evident in the insulin response than on glycemia. A fermented oatmeal drink enriched with 47% bilberries has been shown to reduce insulin index (II) significantly (Granfeldt & Bjo¨rck, 2011). This low insulin demand was attributed to increased glucose uptake, which is characteristic of some other fermented products as well. The presence of polyphenols such as anthocyanins may also have induced an effect on an enhanced insulinindependent pathway for glucose uptake similar to the one reported for cinnamon and other berries. Polyphenols are present in abundance in a number of fruits and vegetables. Adding extracts of berries to various foods may be a useful and viable strategy to attenuate blood glucose and insulin response. One of the earlier studies was on the effect of berries on glycemic response to sucrose. A berry puree (150 g) made of bilberries, blackcurrants, cranberries and strawberries, and sweetened with 35 g sucrose was given to healthy subjects and compared with 35 g sucrose alone mixed with fructose and glucose to match the sugar composition (To¨rro¨nen, Sarkkinen, Tapola, Hautaniemi, & Niskanen, 2010). Although the mechanisms behind this result are not clear, it may be attributed to the high-fiber content and polyphenol content of the berry meal. However, a similar study using berries with pancakes did not show any effect on glycemic response (Clegg, Pratt, Meade, & Henry, 2011). Although the authors used control pancakes with matched sugar profile, they themselves had low GI indicating the effect of another ingredient, probably fat or protein, in the pancakes that lowered its GI. The study did not show any effect of the berries probably due to the masking effect of fat present in the pancakes. Hence, there is a need to carefully look at the interaction between various ingredients present in the test meals while designing a trial to look at the effect of specific compounds such as polyphenols. The

203

Food-Based Ingredients to Modulate Blood Glucose

Table 5.3 Summary of studies using cereal-based ingredients for modulating blood glucose in healthy subjects Study Subjects Food Outcome

Ostman et al. (2002)

Healthy Barley bread with subjects lactic acid

Reduced glycemic response by 23% and insulin response by 21% to a second high-GI meal

Ma¨kela¨inen et al. (2007)

Low glycemic index Healthy Oat bran powder subjects with 4 g beta glucan and insulin index in water

Keogh et al. (2007)

Low insulin area under Healthy Bread and Muffin the curve by 32% subjects prepared using a high-amylose barley, Himalaya 292

Panahi et al. (2007)

Healthy 6 g of enzymatically subjects extracted beta glucan with 75 g glucose drink

King et al. (2008)

Healthy High-amylose barley Low glycemic index. subjects as breakfast cereal Reduced insulin response by 26% compared to a commercial barley cereal

Tosh et al. (2008)

Healthy Oat bran muffins 44  5% reduction in subjects with 8 g beta glucan peak blood glucose rise

Sakuma et al. (2009)

Decreased blood Healthy Barley mixed with subjects rice at 30% and 50%; glucose and insulin response in a dose100% pure barley dependent manner

Thondre and Henry (2009)

Healthy Unleavened Reduced glycemic subjects flatbreads with 4 and index by 43% and 47%, 8 g high-molecular respectively weight beta glucan

Granfeldt and Bjo¨rck (2011)

Healthy Oatmeal fermented subjects drink with 47% bilberries

19.6% more reduction in glycemic response compared to beta glucan extracted by aqueous method

No effect on glycemic index but reduced the insulin index significantly Continued

204

Pariyarath Sangeetha Thondre

Table 5.3 Summary of studies using cereal-based ingredients for modulating blood glucose in healthy subjects—cont'd Study Subjects Food Outcome

Gonzalez and Stevenson (2011)

Only steel cut oats Healthy Steel cut vs. rolled subjects oats as porridge with reduced the glycemic response milk and honey

Chillo, Ranawana, and Healthy Spaghetti with 10% Henry (2011) and subjects high-molecular weight beta glucan Chillo, Ranawana, Pratt, et al. (2011) Finocchiaro et al. (2012)

Reduced glycemic index by 52%

Healthy Bread with 40% Reduced glycemic subjects normal starch barley index of wheat bread by with 6% beta glucan 25 units

Brummer et al. (2012) Healthy Oat bran-enriched Low glycemic index subjects extruded cereals with <50 8.3–8.7 g beta glucan

berry meal showed a significantly lower blood glucose response at 15 and 30 min compared to the sucrose reference. When healthy subjects consumed a basic blackcurrant juice and also a variant fortified with 100 g/l crowberry extract rich in anthocyanins, their blood glucose and insulin responses were slightly attenuated and sustained with no significant difference in incremental AUC (To¨rro¨nen et al., 2012). This kind of results with polyphenol-rich extracts have been noticed previously with other compounds as well, probably due to increased insulin release. Most of the fruits have low GI due to the presence of fructose as the primary sugar and also due to the high-fiber content in them. Various grape products have been used to test the glycemic and insulin response in both healthy and type 2 diabetes subjects. The consumption of a dealcoholized muscadine grape wine by type 2 diabetics resulted in reduced insulin response and improved insulin sensitivity compared to muscadine grape juice or wine (Banini, Boyd, Allen, Allen, & Sauls, 2006). Zunino has detailed the polyphenols present in grapes such as resveratrol, quercetin, catechins, and anthocyanins and indicated them as potential compounds for reducing glycemic response in type 2 diabetics. However, the review focuses more on animal studies and does not give enough evidence of such an effect in humans (Zunino, 2009). Hoover-Plow, Savesky, and Dailey (1987) compared the glycemic response to six different fruits along with a standard meal in type 2 diabetics. The fruits tested were apple, banana, honeydew, orange, grapes, and strawberries with a no-fruit control meal with green beans, rice,

Food-Based Ingredients to Modulate Blood Glucose

205

Table 5.4 Summary of studies using cereal-based ingredients for blood glucose control in overweight and type 2 diabetes subjects Study Subjects Food Outcome

Tappy et al. (1996)

Type 2 diabetes subjects

Oat bran-enriched 60% reduction in breakfast cereal with glucose area under 6 and 8 g beta glucan the curve compared with a continental breakfast

Pick et al. (1996)

Type 2 diabetic women 12-week period

Oat bran bread Reduced the glucose products with 22.8% area under the curve by 42% compared to beta glucan the white bread

Jenkins, Jenkins, Type 2 Zdravkovic, Wu¨rsch, diabetes et al. (2002), Jenkins, subjects Kendall, Augustin, Franceschi, et al. (2002), and Jenkins, Kendall, Augustin, Martini, et al. (2002)

Oat bran-enriched extruded cereal and breakfast bar

Low glycemic index of 52 and 43 for the products

Tapola et al. (2005)

Type 2 diabetes subjects

Oat bran flour with 9.4 g beta glucan

Reduced the glucose area under the curve by 71 mmol min/l

Behall et al. (2005)

Overweight Oat flour and flakes subjects with 3.23 g beta glucan; betaglucan-rich barley flour and flakes with 12 g beta glucan

Reduced the glycemic response by 29–36% by oats; 59–65% by barley products

Kim et al. (2006)

Overweight Cereals with 2 g subjects barley beta glucan

Reduced glycemic response only in women and not in men

Bays et al. (2011)

Overweight Low-viscosity barley Reduce blood glucose area under and obese beta glucan in beverages (6 g/day) the curve, fasting subjects insulin, and insulin resistance

206

Pariyarath Sangeetha Thondre

turkey, and margarine. They found reduced glycemic response to apple and banana test meal compared to the other fruits. In a later study in type 2 diabetic subjects, when raisins were compared with white bread, seedless grapes, and banana, the glycemic response of raisins and banana was comparable whereas the seedless grapes had higher glycemic response (Wilson et al., 2012). The authors believed that this effect may have been due to the high water content of seedless grapes that accelerated the gastric emptying rates and thereby resulted in rapid absorption of glucose into the blood stream. The white bread’s glycemic response was similar to the raisins and bananas due to the effect of freezing and thawing on resistant starch formation or starch retrogradation in bread. The GI of fruits may be affected by various factors such as degree of ripeness, type of sugars present, other polyphenols present, the presence of fiber, and also the acidity of the fruit as well as the physical structure of the fruit. When the GI of chico, mango, pineapple, and papaya were tested in type 2 diabetes subjects, mango and chico showed lower GI compared to papaya and pineapple. Tropical fruits are generally reported to be of high GI values compared to the temperate fruits. The amount of antinutrients such as phytic acid, tannins, lectins, saponins, etc. can result in a low glycemic response due to reduced rate of digestion (Guevarra & Panlasigui, 2000). Acids such as malic, citric, and tartaric acids present in fruits are also known to reduce their glycemic response. Cranberries are also another group of fruits that are rich in polymeric polyphenols such as proanthocyanidins. Wilson et al. experimented the use of raw and dried cranberries against a white bread control in type 2 diabetics. The dried cranberries included a sweetened version using sugar and also a low-sugar version with polydextrose. The plasma glucose was low for the raw cranberries whereas the plasma insulin response was low for the raw cranberries and for the low-sugar-dried cranberries in comparison with the white bread and the dried sweetened cranberries (Wilson et al., 2010). Cranberry juice has also been shown to influence the glycemic response in diabetic subjects. However, there was a significant difference in the effect between a conventional sweetened version and a low calorie version of the juice (Wilson, Meyers, Singh, Limburg, & Vorsa, 2008). However, this study could not substantiate the effect of the polyphenols identified in the cranberry juice such as quercetin, myricetin, anthocyanins, and proanthocyanidins because the low-calorie control with dextrose also resulted in a low glycemic response compared to the normal calorie version of the juice and control. A bioflavonoid extracted from sugar cane has been shown to decrease the GI of a high-GI meal of milk and wheat biscuits. This specific flavonoid that

207

Food-Based Ingredients to Modulate Blood Glucose

showed in vitro inhibition on alpha glucosidase and alpha amylase enzymes reduced the mean GI to 57 at 15 mg concentration, 46 by 50 mg concentration, and 54 by 100 mg concentration. There was no significant effect of the dose of the extract on the GI reduction (Holt, de Jong, Faramus, Lang, & Brand Miller, 2003). The effect of polyphenols on insulin sensitivity was also reported in a trial where a mixed spice blend was used in overweight men (reference). A control meal of cheese bread, coconut chicken, and dessert biscuit was compared with a test meal of the same foods with added spice mix. The spices used included black pepper, cinnamon, cloves, garlic powder, ginger, oregano, rosemary, paprika, and turmeric. The test meal with spices reduced insulin response with no effect on glucose response similar to many other polyphenols. However, due to the complexity of the spice ingredients, the effect could be due to any of the active compounds in them. Table 5.5 is a summary of the research trials using fruit-based ingredients for blood glucose modulation in healthy and type 2 diabetic subjects. Table 5.5 Summary of studies using honey, nut, and fruit-based ingredients for blood glucose control in healthy and type 2 diabetes subjects Study Subjects Food Outcome

Banini et al. (2006)

Type 2 diabetes subjects

Improved insulin Dealcoholized muscadine grape sensitivity and reduced insulin response wine

Jenkins et al. (2006)

Healthy subjects

60 g raw unblanched almonds with white bread

Reduced postprandial glycemic response Low glycemic index 55

Ahmad, Azim, Mesaik, Healthy and Khan (2008) subjects

Natural honey (1 g/kg body weight)

Reduced postprandial glycaemia

Choudhary, Kothari, and Sharma (2009)

Type 2 diabetic women

Raw almonds 10 g/day for 4 weeks

Reduced fasting and postprandial glycemic response

Torronen, Sarkkinen, Tapola, Hautaniemi, and Niskanen (2010)

Healthy subjects

Berry meal with 35 g sucrose

Reduced glycemic response at 1 and 30 min

Granfeldt and Bjo¨rck (2011)

Healthy subjects

Oatmeal fermented drink with 47% bilberries

No effect on glycemic index but reduced the insulin index significantly

208

Pariyarath Sangeetha Thondre

8. SPICES Other than macronutrients, there are other phytochemicals that are known to lower glycemic response by various mechanisms. Spices are one such food group that have been shown to have hypoglycemic and hypoinsulinemic effects. Cinnamon has been used for many studies in both nondiabetic and diabetic subjects. An active ingredient of cinnamon called methyl hydroxychalcone polymer (MHCP) has been proven to mimic insulin and promote glucose disposal into the skeletal muscle ( Jarvill-Taylor, Anderson, & Graves, 2001). This mechanism is due to upregulation of insulin signaling cascade by phosphorylation of the insulin receptor substrate as shown in animal studies (Qin et al., 2003). Khan, Safdar, Ali Khan, Khattak, and Anderson (2003) was the first to report the beneficial effect of cinnamon on glycemic profile of diabetic subjects. However, a study in postmenopausal overweight type 2 diabetic women did not give an effect of cinnamon consumption for 6 weeks at a dose of 1.5 g/day. This may be due to the effect of some subject characteristics on the mechanism by which cinnamon influences insulin levels (Vanschoonbeek, Thomassen, Senden, Wodzig, & van Loon, 2006). The use of herbal teas has shown a significant effect on reducing the GI of white bread (Faqih & Al-Nawaiseh, 2006). Four types of herbal teas such as cinnamon tea, fenugreek seed tea, black tea, and anise tea were compared in two doses per cup in healthy subjects. The cinnamon tea at 4 and 8 g/cup reduced the GI of white bread by 50% with no dose-dependent effect. The effect of cinnamon was attributed to the presence of the polyphenol compound MHCP in cinnamon. The fenugreek tea was the one that reduced the GI considerably with a high dose of 10 g/cup. The lower dose of 6 g/cup resulted in a 40% reduction in GI and the higher 10 g/cup dose resulted in a 60% reduction in GI of white bread. In fenugreek, the hypoglycemic effect is often due to the presence of galactomannan fiber and also a specific amino acid called 4-hydroxy isoleucine that has insulin-stimulating action. The black tea was used at lower doses of 1.5 g and 2.5 g/cup and both reduced the GI of white bread but the GI was still in the high GI range. Again this effect is also attributed to the polyphenols in tea, specifically EGCG that has hepatic glucose-inhibition effect and insulin-stimulating effect. The aniseed tea was tried in 6 and 10 g doses and both retained the GI at high category for the white bread.

Food-Based Ingredients to Modulate Blood Glucose

209

Adding 1 or 3 g cinnamon to a rice pudding test meal did not result in lowering the glycemic response in healthy subjects, but the insulin AUC was significantly reduced by the 3 g dose of cinnamon (Hlebowicz et al., 2009). This effect was probably due to an increase in glucose uptake by stimulation of insulin receptor rather than a reduced gastric emptying rate earlier hypothesized by the authors. In a 2-week trial using 3 g cinnamon consumption by healthy patients, their glucose and insulin response to Oral glucose tolerance test (OGTT) was improved and the insulin sensitivity was also improved on the 14th day (Solomon & Blannin, 2009). However, a longer term intervention of 4 months in type 2 diabetic subjects who consumed 3 g of cinnamon extract and a placebo capsule resulted in a significant difference in fasting plasma glucose pre- and postintervention in both the groups. Although the effect cinnamon extract was 7% more than the placebo, the levels of HbA1c did not show any difference between the groups attributing the response to a placebo effect (Mang et al., 2006). Fenugreek seeds have been reported to reduce fasting blood sugar in type 2 diabetic patients. There was a 25% reduction in fasting blood sugar when fenugreek powder (10 g/day) was mixed with hot water and no significant effect was noticed when consumed with yogurt. This may have been due to the solubility effect of the active galactomannan polysaccharide in fenugreek (Kassaian, Azadbakht, Forghani, & Amini, 2009). Additional benefits of lipid profile were also obtained by using this herbal supplement. Losso et al. (2009) have reported the development of a bread product with fenugreek as a method of administering to type 2 diabetic subjects. The product was acceptable and compared to the commercial bread in sensory properties and resulted in a significant reduction in insulin response. In a study in Japan, the green tea consumption was shown to reduce the risk of diabetes by 33% with no effect shown by oolong or black teas (Iso, Date, Wakai, Fukui, & Tamakoshi, 2006). In another US-based study that looked at the effect of flavonoid-rich foods on development of type 2 diabetes, the researchers reported a beneficial effect of tea consumption equivalent to more than four cups a day in only women compared to those women who did not drink tea (Song, Manson, Buring, Sesso, & Liu, 2005). Irrespective of these results, two large prospective cohort studies, the Health Professionals study, and the Nurse’s Health Study did not find any effect of tea on the development of type 2 diabetes. A 30-day intervention with oolong tea in Taiwan resulted in a reduction in fasting plasma glucose and fructosamine in type 2

210

Pariyarath Sangeetha Thondre

diabetes subjects (Hosoda et al., 2003), but the authors were not able to explain the effect completely. In healthy subjects, 1 g instant black tea reduced the blood glucose response to 75 g glucose but increased the insulin response (Bryans, Judd, & Ellis, 2007). An 8-week trial in Japan with green tea extract resulted in a significant reduction in the HbA1c levels of adults who had borderline diabetes (Fukino et al., 2008). Another study looking at the dose and frequency of green tea consumption in healthy subjects showed reduced fasting blood glucose and fructosamine levels in those consuming 3% green tea against those who consumed 1% concentration of green tea (Maruyama, Iso, Sasaki, & Fukino, 2009). There was no effect noted for frequency of green tea consumption on any of the blood glucose parameters. However, not all studies have shown a beneficial effect of green tea. A 300-ml green tea with breakfast consisting of white bread and turkey did not show any effect on glucose or insulin levels in healthy subjects (Josic, Olsson, Wickeberg, Lindstedt, & Hlebowicz, 2010). In type 2 diabetes patients also, no effect of 9 g green tea consumption for 4 weeks was noticed on glucose concentration, insulin concentration, or insulin resistance. Table 5.6 gives a summary of studies carried out using spice-based ingredients for normal levels blood glucose and insulin management.

9. LEGUME-BASED INGREDIENTS Legumes are also important food groups that are known to reduce postprandial glycemic response. Many factors are responsible for this such as their rigid cotyledon walls, less susceptibility of their starch to enzyme digestion, high levels of nondigestible carbohydrates such as resistant starch, oligosaccharides, nonstarch polysaccharides and protein, and also the presence of a-amylase inhibitors and other polyphenols in the legumes ¨ stman, 2000a). Goni and Valentı´n-Gamazo (Bjo¨rck, Liljeberg, and O (2003) prepared spaghetti with chick pea flour (25%) and compared it with wheat spaghetti and white bread in healthy female subjects. They noticed a significant reduction of 14 units in the GI of the chick pea flour spaghetti compared to the wheat pasta. Pasta itself is a food product showing reduced glycemic response compared to other starchy foods. Different pasta products such as spaghetti, macaroni, spaghetti porridge, and bread made of spaghetti ingredients were compared with mashed potatoes in a study using healthy subjects (Granfeldt & Bjo¨rck, 1991). The authors noticed low GI for the spaghetti products compared to the bread and potatoes due to the compact structure of the pasta products that restrict the enzyme access to the starch.

211

Food-Based Ingredients to Modulate Blood Glucose

Table 5.6 Summary of studies using spices and legumes for blood glucose control in healthy and type 2 diabetes subjects Study Subjects Food Outcome

Goni and Valentı´nGamazo (2003)

Healthy subjects Chick pea flour spaghetti (25%)

Reduction in glycemic index compared to wheat spaghetti by 14 units

Khan et al. (2003)

Type 2 diabetic Cinnamon 1, 3, or 6 g daily in capsule form for 40 days

18–29% reduction in fasting plasma glucose

Vanschoonbeek Postmenopausal Cinnamon 1.5 g/ et al. (2006) overweight type day for 6 weeks 2 diabetic women

No reduction in plasma glucose, insulin, or HbA1c

Kassaian et al. (2009)

25% reduction in fasting blood sugar

Type 2 diabetic Fenugreek powder 10 g/day in hot water

Hlebowicz et al. Healthy subjects 3 g of cinnamon (2009) with 300 g rice pudding Udani et al. (2009)

No effect on glycemic response but 3 g significantly reduced insulin response

Healthy subjects 3000 mg of white 34% reduction in kidney bean extract glycemic index of the control with white bread and butter

Among the pasta products, the GI was higher for the spaghetti porridge showing that ruining the compact structure results in increased glycemic response. A flour blend with chick pea, psyllium husk, and fenugreek powder called “atta mix” flour has been used for preparing flatbreads similar to the way it is produced using wheat flour (Radhika et al., 2010). This study in healthy subjects showed a significant reduction in blood glucose following the atta mix flatbread compared to the whole wheat flatbreads. Although both the flatbreads had low GI, the GI of atta mix flatbreads was reduced to 27 compared to 45 for the whole wheat flatbreads. Thompson et al. attributed the beneficial effect of legumes on glycemic response to their polyphenol levels. When leguminous and nonleguminous foods were tested in healthy and diabetic individuals, a negative correlation was observed between the polyphenol intake and the GI values for the foods

212

Pariyarath Sangeetha Thondre

(Thompson, Yoon, Jenkins, Wolever, & Jenkins, 1984). A recent study examined the effect of various types of beans such as pinto beans, black beans, and kidney beans with rice on the glycemic response in type 2 diabetes subjects (Thompson, Winham, & Hutchins, 2012). All the three beans and rice meals reduced the glycemic response to the rice meal alone. This effect may be attributed to the high-fiber or protein content of the beans or due to other phytonutrients such as phytic acid that binds to calcium and inhibits its availability as a cofactor for alpha amylase activity on starch ( Josse, Kendall, Augustin, Ellis, & Jenkins, 2007). A recent systematic review and meta-analysis showed that the pulses alone reduce fasting blood glucose and insulin in both diabetic and nondiabetic subjects (Sievenpiper et al., 2009). The use of pulses with low-GI diets was reported to reduce the amount of glycosylated hemoglobin and fructosamine that are markers of long-term maintenance of blood glucose. When pulses were used with high-fiber diets, the effect was even more beneficial with a decrease in both fasting blood glucose and glycosylated proteins. A number of factors that affected the outcome measures were identified by the authors who included the type of the pulse, amount of the pulse, physical state of the pulse, and also other participant characteristics and study design characteristics. In most of the studies, it is believed that the low-GI effect of pulses is due to the high-fiber content and the slow-digesting starch characteristics in pulses. However, a study using yellow pea showed that the protein in it is prominent in its effect on glycemia (Smith, Mollard, Luhovyy, & Anderson, 2012). The authors fed two concentrations (10 and 20 g) of pea protein and fiber in healthy subjects and then fed an ad libitum pizza meal to the subjects after 30 min. They found that both the 10 and 20 g protein dose suppressed the glycemic response after the test meal and the pizza meal. But, the higher 20 g dose had an effect on the glycemic response after the ad libitum second meal as well. Mollard et al. (2012) also tested the effect of different pulses on the glycemic response to a pasta and tomato sauce meal. They reported reduction in glycemic response soon after the meal and also after a second meal with difference in the effect depending on the type of pulse. While chick peas, lentils, and navy beans reduced the glycemia after the pasta and tomato sauce whereas chick peas alone was responsible for the reduction of glycemic response after a second ad libitum meal as well. The glycemic response to pulses has been shown to be affected by the recipes used and not by different processing techniques. Wong, Mollard, Zafar, Luhovyy, and Anderson (2009) compared canned and homemade navy beans and reported that both lowered the glycemic response compared

Food-Based Ingredients to Modulate Blood Glucose

213

to a high-GI bread meal, but there was difference depending on the addition of other ingredients such as molasses and sugar. In addition to the fiber compounds from various sources, other ingredients such as amylase inhibitors from foods have also been used to modulate glycemic response of refined carbohydrate foods. One such ingredient is a white kidney bean extract called Phase 2, which is an alpha amylase inhibitor (Udani, Singh, Barrett, & Preuss, 2009). The extract was used in capsule form or powder form at three different doses 1500, 2000, and 3000 mg in healthy individuals who consumed it with white bread and butter as breakfast. The only dose that significantly reduced the GI of the test meal was 3000 g in powder form. Although the authors have not commented about the inability of the extract to lower GI at all doses, it may be assumed that the use of butter with the white bread due to its low-GI effect may have masked any effect of Phase 2 on GI of the test meals. Table 5.6 gives a summary of studies carried out using legume-based ingredients for normal level blood glucose and insulin management.

10. EFFECT OF PROTEIN AND FAT ON BLOOD GLUCOSE Proteins may modulate blood glucose and specific proteins from specific sources may have beneficial effects. Whey protein was shown to have an effect on insulin response of type 2 diabetic subjects (Frid, Nilsson, Holst, & Bjorck, 2005). Milk protein modulates blood glucose by specifically affecting insulin secretion due to its insulinotropic amino acid content or due to its effect on GIP and GLP-1 hormones. Intake of milk and milk products are also known to have an effect on controlling chronic diseases associated with insulin resistance (Pereira et al., 2002). Hoyt, Hickey, and Cordain (2005) attempted to determine whether the difference in GI and II of milk is due to their differences in fat content. They tested skimmed and whole milk in healthy participants and found a similar insulin response for both skimmed and whole milk. This confirmed that the insulinotropic effect of milk is not due to fat and may be due to characteristic proteins in milk. Although fat and protein both lower glycemic response, the effect is independent of each other when used in combination. Although there was a linear dose-dependent effect of both fat and protein on glycemic response, a greater weight by weight effect is noticed for protein than fat (Moghaddam, Vogt, & Wolever, 2006). Some of the subject characteristics

214

Pariyarath Sangeetha Thondre

had an important role in the effect of protein and fat. A relation between protein levels, waist circumference, and fiber intake was observed whereas the effect of fat was more dependent on fasting plasma insulin levels of the subjects. Several mechanisms are responsible for the effect of fat and protein. Some of these are the delayed gastric emptying, effect of GIP and GLP-1 on gastric emptying and insulin secretion, or due to specific amino acids effect on insulin secretion. Almond is a food rich in monounsaturated fatty acids and fiber well known to have beneficial effects on lipid profile. Consumption of 10 g/ day raw almonds for 4 weeks has been shown to reduce fasting and postprandial blood glucose response in type 2 diabetic women. The positive effects on lowering fasting and postprandial glycemia were evident from week 1 and continued to week 4 (Choudhary et al., 2009). Jenkins et al. reported a decreased risk of oxidative damage to proteins resulting from the low glycemic effect of almonds. Healthy subjects consumed 60 g raw unblanched almonds with white bread and compared their postprandial glycemic response with a rice meal and potato meal. The addition of almonds reduced the postprandial glycemic response to bread along with supplying additional antioxidants in the meal ( Jenkins et al., 2006). Fermentation is a process that affects glycemic response of foods. Milk and milk products have been shown to produce varied glycemic response depending on the extent of fermentation that they are subjected to. This is due to the presence of acids such as lactic acid in the fermented products. Ostman, Liljeberg Elmsta˚hl, Bjo¨rck (2001) compared the glycemic response of fermented, pickled, and nonfermented milk products with white bread as a reference food. Milk products themselves show reduced glycemic response due to the presence of the sugar lactose, which is not easily digested and converted into glucose. The milk products showed reduced GI and II compared to the white bread but there was no difference between the fermented and regular milk products. But the presence of acid in the form of yogurt and pickled cucumber reduced the GI and II of white bread. The insulinotropic effect of milk and milk products may be explained by certain types of amino acids present in the milk that can influence insulin response. All milk products generally have the property to reduce glycemic response compared to starchy foods. In a recent study comparing human and bovine milk with reconstituted bovine whey and casein drinks and white bread, all the milk products showed reduced glycemic response ¨ stman, & Bjo¨rck, 2012). The authors were expecting (Gunnerud, Holst, O to see a change in the response to human milk due to its high whey protein

Food-Based Ingredients to Modulate Blood Glucose

215

content. The results showed slightly higher insulin economy for the human milk per protein amount in the milk and the effect may be attributed to the amino acid profile of the proteins. Proteins from various plant and animal sources were compared in a study to identify their variations on insulinotropic effect (Nilsson, Stenberg, Frid, Holst, & Bjo¨rck, 2004). Reconstituted milk, cheese, whey, cod, and wheat gluten with equivalent quantities of lactose were used as test meals in comparison with white bread as reference. The reconstituted milk and whey protein meals resulted in reduced glucose response, but the insulin response was higher than that of the reference meal. The effect was more for the whey protein meal and probably due to increase in specific amino acids such as leucine, valine, isoleucine, lysine, and threonine, which were increased after the whey meal. All the other protein meals were considered poor in increasing insulin response. Bread is a very common food consumed all over the world especially in large quantities in the Western countries. White bread is usually considered as high-GI food because of its effect on rapid increase in blood glucose. Whole grain bread on the other hand has the ability to reduce the blood glucose response and hence they are considered as medium- or low-GI food. Sourdough fermentation is a process used in preparing bread that could result in low glycemic response due to the formation of organic acids during the fermentation process. Scazzina, Rio, Pellegrini, and Brighenti (2009) used sourdough fermentation on white and whole meal flour and used two different leavening techniques using sourdough and Saccharomyces cerevisiae to test the glycemic response to the two types of breads. They found that sourdough-fermented breads using both whole and white flour resulted in reduced glycemic response compared to the yeast-leavened bread probably due to increased resistant starch content resulting from the starch retrogradation caused by the organic acids formed by sourdough fermentation. Sourdough fermentation is also used in the preparation of ready-to-eat breakfast cereals. When wheat flakes were modified by introducing a sourdough prefermentation step by suppressing the steam cooking and reducing the sucrose content and compared with the standard wheat flakes and also a white wheat bread, the glycemic response of the modified wheat flakes was less than the standard wheat flakes, but not significantly different (Lioger et al., 2009). However, there was a small improvement in the insulin response of the modified wheat flakes. This study showed that the food structure is more important than the effect on starch gelatinization.

216

Pariyarath Sangeetha Thondre

Adding 18, 23, or 28 g vinegar to white bread has shown an inverse dosedependent reduction in both glycemic and insulin response in healthy subjects (Ostman, Granfeldt, Persson, Bjo¨rck, 2005). However, there was no significant effect on the GI calculated for the meals. This was in contrast to the earlier result from the same research group where vinegar was used in the form of a sauce with olive oil. In that study, there was a significant reduction in GI and II that was attributed to different rates of gastric emptying (Liljeberg & Bjo¨rck, 1998). Reducing the volume of bread was also reported to be an important strategy to reduce the blood glucose response in humans. Burton and Lightowler (2006) altered the proving method to reduce the volume of the bread loaves tested in healthy subjects. The bread with the lowest volume had low GI (38), whereas the other three breads with higher loaf volumes had higher GI values (72, 86, and 100). Other cereals related to wheat such as spelt with high protein and fiber content than wheat has also been used to investigate its influence on glycemic response. However, the glucose AUC was similar to that of wheat bread in healthy subjects irrespective of high oligofructose in the spelt bread (Marques et al., 2007).

11. SUGARS AND SUGAR ALCOHOLS Fructose is a naturally occurring sugar that can lower the postprandial glycemic response compared to sucrose, glucose, or starch (Bantle, Swanson, Thomas, & Laine, 1992; Crapo, Kolterman, & Henry, 1986). Although natural foods such as fruits and honey rich in fructose are recommended, high intake of pure fructose may lead to adverse effects on lipid profile and leads to complications such as nonalcoholic fatty liver and high cholesterol levels (Swanson, Laine, Thomas, & Bantle, 1992). The effect of honey may not be just due to the fructose content. A study conducted by consuming 1 g/kg body wt. natural honey or simulated honey with identical sugar profile showed that natural honey only reduced postprandial glycemic response in healthy subjects. This attenuated glycemic response following honey consumption may be due to the presence of various phytochemicals, fermentable carbohydrates, and hydrogen peroxide (Ahmad et al., 2008). Sugar alcohols constitute another group of ingredients that can modulate blood glucose more than other conventional sugars such as fructose, sucrose, or glucose (Akgun & Ertel, 1980; Natah, Hussien, Tuominen, & Koivisto, 1997). However, they are reported to cause side effects such as diarrhea if consumed in excess (Payne, Craig, & Williams, 1997).

Food-Based Ingredients to Modulate Blood Glucose

217

12. CONCLUDING REMARKS This chapter has highlighted a few food groups that have ingredients with the ability to modulate blood glucose either by direct effects on carbohydrate digestion and absorption or by indirect effects on insulin hormone or its receptor. Most of these effects have been proven in both healthy and diabetic subjects demonstrating their efficacy in managing glucose tolerance using diet-based interventions. Although there are no claims approved for the health benefits exhibited by these ingredients, inclusion of these food groups in our diet may be a viable strategy to achieve normal blood glucose levels to control the susceptibility to chronic diseases such as type 2 diabetes, cardiovascular diseases, and obesity.

REFERENCES Ahmad, A., Azim, M. K., Mesaik, M. A., & Khan, R. A. (2008). Natural honey modulates physiological glycemic response compared to simulated honey and D-glucose. Journal of Food Science, 73, H165–H167. Akgun, S., & Ertel, N. H. (1980). A comparison of carbohydrate metabolism after sucrose, sorbitol, and fructose meals in normal and diabetic subjects. Diabetes Care, 3, 582–585. Aman, P., Rimsten, L., & Andersson, R. (2004). Molecular weight distribution of b-glucan in oat-based foods. Cereal Chemistry, 81, 356–360. Anderson, R. J., Freedland, K. E., Clouse, R. E., & Lustman, P. J. (2001). The prevalence of comorbid depression in adults with diabetes: A meta-analysis. Diabetes Care, 24, 1069–1078. Andersson, A. M., Armo, E., Grangeon, E., Fredriiksson, H., Andersson, R., & Aman, P. (2004). Molecular weight and structure units of (1 ! 3, 1 ! 4) b-D glucans in dough and bread made from hull-less barley fractions. Journal of Cereal Science, 40, 194–204. Aston, L. M. (2006). Glycemic index and metabolic disease risk. The Proceedings of the Nutrition Society, 65, 125–134. Atkinson, F. S., Foster-Powell, K., & Brand-Miller, J. C. (2008). International table of glycemic index and glycemic load values. Diabetes Care, 31, 2281–2283. Banini, A. E., Boyd, L. C., Allen, J. C., Allen, H. G., & Sauls, D. L. (2006). Muscadine grape products intake, diet and blood constituents of non-diabetic and type 2 diabetic subjects. Nutrition, 22, 1137–1145. Bantle, J. P., Swanson, J. E., Thomas, W., & Laine, D. C. (1992). Metabolic effects of dietary fructose in diabetic subjects. Diabetes Care, 15, 1468–1476. Bays, H., Frestedt, J. L., Bell, M., Williams, C., Kolberg, L., Schmelzer, W., et al. (2011). Reduced viscosity barley beta-glucan versus placebo: A randomized controlled trial of the effects on insulin sensitivity for individuals at risk for diabetes mellitus. Nutrition and Metabolism, 8, 58. Behall, K. M., Scholfield, D. J., & Hallfrisch, J. (2005). Comparison of hormone and glucose responses of overweight women to barley and oats. Journal of the American College of Nutrition, 24, 182–188. Beulens, J. W. J., de Bruijne, L. M., Stolk, R. P., Peeters, P. H. M., Bots, M. L., Grobbee, D. E., et al. (2007). High dietary glycemic load and glycemic index increase

218

Pariyarath Sangeetha Thondre

risk of cardiovascular disease among middle-aged women: A population-based follow-up study. Journal of the American College of Cardiology, 50, 14–21. Bjorck, I., Granfeldt, Y., Liljeberg, H., Tovar, J., & Asp, N. G. (1994). Food properties affecting the digestion and absorption of carbohydrates. The American Journal of Clinical Nutrition, 59, 699–705. ¨ stman, E. (2000). Low glycemic-index foods. British Journal of Bjo¨rck, I., Liljeberg, H., & O Nutrition, 83, S149–S155. Bouche, C., Rizkalla, S. W., Luo, J., Vidal, H., Veronese, A., Pacher, N., et al. (2002). Fiveweek, low-glycemic index diet decreases total fat mass and improves plasma lipid profile in moderately overweight nondiabetic men. Diabetes Care, 25, 822–828. Brown, L., Rosner, B., Willett, W. W., & Sacks, F. M. (1999). Cholesterol-lowering effects of dietary fiber: A meta-analysis. The American Journal of Clinical Nutrition, 69, 30–42. Brummer, Y., Duss, R., Wolever, T. M. S., & Tosh, S. M. (2012). Glycemic response to extruded oat bran cereals processed to vary in molecular weight. Cereal Chemistry, 89, 255–261. Bryans, J. A., Judd, P. A., & Ellis, P. R. (2007). The effect of consuming instant black tea on postprandial plasma glucose and insulin concentrations in healthy humans. Journal of the American College of Nutrition, 26, 471–477. Burkitt, D. P., & Trowell, H. C. (1977). Dietary fiber and western diseases. Irish Medical Journal, 70, 272–277. Burton, P., & Lightowler, H. J. (2006). Influence of bread volume on glycemic response and satiety. The British Journal of Nutrition, 96, 877–882. Burton-Freeman, B., Davis, P. A., & Schneeman, B. O. (2002). Plasma cholecystokinin is associated with subjective measures of satiety in women. The American Journal of Clinical Nutrition, 76, 659–667. Ceriello, A., Quagliaro, L., Piconi, L., Assaloni, R., Da Ros, R., Maier, A., et al. (2004). Effect of postprandial hypertriglyceridemia and hyperglycemia on circulating adhesion molecules and oxidative stress generation and the possible role of simvastatin treatment. Diabetes, 53, 701–710. Chandalia, M., Garg, A., Lutjohann, D., von Bergmann, K., Grundy, S. M., & Brinkley, L. J. (2000). Beneficial effects of high dietary fiber intake in patients with type 2 diabetes mellitus. The New England Journal of Medicine, 342, 1392–1398. Chillo, S., Ranawana, D. V., & Henry, C. J. K. (2011). Effect of two barley b-glucan concentrates on in vitro glycemic impact and cooking quality of spaghetti. LWT - Food Science and Technology, 44, 940–948. Chillo, S., Ranawana, D. V., Pratt, M., & Henry, C. J. K. (2011). Glycemic response and glycemic index of semolina spaghetti enriched with barley b-glucan. Nutrition, 27, 653–658. Choudhary, P., Kothari, S., & Sharma, V. (2009). Almond consumption decreases fasting and post prandial blood glucose level in female type 2 diabetes subject. American Journal of Infectious Diseases, 5, 109–111. Clegg, M. E., Pratt, M., Meade, C. M., & Henry, C. J. K. (2011). The addition of raspberries and blueberries to a starch-based food does not alter the glycemic response. The British Journal of Nutrition, 106, 335–338. Clegg, M. E., & Thondre, P. S. (2012). The influence of barley b-glucan on satiety, glycemic response and energy expenditure. The Proceedings of the Nutrition Society, 71, E72. Crapo, P. A., Kolterman, O. G., & Henry, R. R. (1986). Metabolic consequence to twoweek fructose feeding in diabetic subjects. Diabetes Care, 9, 111–119. Diabetes Atlas. (2012). 5th ed. International Diabetes Federation. Available at http://www. idf.org/sites/default/files/5E_IDFAtlasPoster_2012_EN.pdf. Diabetes UK. (2013a). http://www.diabetes.org.uk/Guide-to-diabetes/Type-1-diabetes/.

Food-Based Ingredients to Modulate Blood Glucose

219

Diabetes UK. (2013b) http://www.diabetes.org.uk/Guide-to-diabetes/Type-2-diabetes/. Diabetes UK. (2013c). http://www.diabetes.org.uk/Guide-to-diabetes/Introduction-todiabetes/What_is_diabetes/Gestational_diabetes/. Diabetes UK. (2013d). http://www.diabetes.org.uk/Guide-to-diabetes/Introduction-todiabetes/What_is_diabetes/Prediabetes/. Durtschi, A. (2001). Nutritional content of whole grains versus their refined flours. Data source: USDA Economic Research Service. Edwards, C. A., Blackburn, N. A., Cragien, L., Davison, P., Tomlin, J., Sugden, K., et al. (1987). Viscosity of food gums determined in vitro related to their hypoglycemic actions. The American Journal of Clinical Nutrition, 46, 72–77. EFSA (2010). Scientific opinion on the substantiation of health claims related to beta glucans and maintenance or achievement of normal blood glucose concentrations (ID 756, 802, 2935) pursuant to Article 13(1) of Regulation (EC) No 1924/2006 2010. EFSA Journal, 8, 1482. Faqih, A. M., & Al-Nawaiseh, F. Y. (2006). The immediate glycemic response to four herbal teas in healthy adults. The Jordan Medical Journal, 40, 266–275. Feldman, N., Norenberg, C., Voet, H., Manor, E., Berner, Y., & Madar, Z. (1995). Enrichment of an Israeli ethnic food with fibers and their effects on glycemic and insulinaemic responses in subjects with mom-insulin dependent diabetes mellitus. The British Journal of Nutrition, 74, 681–688. Finocchiaro, F., Ferrari, B., Gianinetti, A., Scazzina, F., Pellegrini, N., Caramanico, R., et al. (2012). Effects of barley b-glucan-enriched flour fractions on the glycemic index of bread. International Journal of Food Science and Nutrition, 63, 23–29. Foster-Powell, K., Holt, S. H. A., & Brand-Miller, J. C. (2002). International table of glycemic index and glycemic load values. The American Journal of Clinical Nutrition, 76, 5–56. Fraser, R. J., Horowitz, M., Maddox, A. F., Harding, P. E., Chatterton, B. E., & Dent, J. (1990). Hyperglycemia slows gastric emptying in type 1 (insulin-dependent) diabetes mellitus. Diabetologia, 33, 675–680. Frid, A. H., Nilsson, M., Holst, J. J., & Bjorck, I. M. E. (2005). Effect of whey on blood glucose and insulin responses to composite breakfast and lunch meals in type 2 diabetic subjects. The American Journal of Clinical Nutrition, 82, 69–75. Frost, G., Keogh, B., Smith, D., Akinsanya, K., & Leeds, A. (1996). The effect of lowglycemic carbohydrate on insulin and glucose response in vivo and in vitro in patients with coronary heart disease. Metabolism, 45, 669–672. Frost, G., Leeds, A., Trew, G., Margara, R., & Dornhorst, A. (1998). Insulin sensitivity in women at risk of coronary heart disease and the effect of a low glycemic diet. Metabolism, 47, 1245–1251. Fukino, Y., Ikeda, A., Maruyama, K., Aoki, N., Okubo, T., & Iso, H. (2008). Randomized controlled trial for an effect of green tea-extract powder supplementation on glucose abnormalities. European Journal of Clinical Nutrition, 62, 953–960. Gannon, M. C., Nuttall, F. Q., Westphal, S. A., Fang, D., & Ercan-Fang, N. (1998). Acute metabolic response to high-carbohydrate, high starch meals compared with moderate carbohydrate, low-starch meals in subjects with type 2 diabetes. Diabetes Care, 21, 1619–1626. Giacco, R., Brighenti, F., Parillo, M., Capuano, M., Ciardullo, A. V., Rivieccio, A., et al. (2001). Characteristics of some wheat-based foods of the Italian diet in relation to their influence on postprandial glucose metabolism in type 2 diabetic patients. The British Journal of Nutrition, 85, 33–40. Goni, I., & Valentı´n-Gamazo, C. (2003). Chickpea flour ingredient slows glycemic response to pasta in healthy volunteers. Food Chemistry, 81, 511–515. Gonzalez, J. T., & Stevenson, E. J. (2011). Glycemic and appetitive responses to porridge made from oats differing by degree of processing. The Proceedings of the Nutrition Society, 70, E121.

220

Pariyarath Sangeetha Thondre

Granfeldt, Y., & Bjo¨rck, I. (1991). Glycemic response to starch in pasta: A study of mechanisms of limited enzyme availability. Journal of Cereal Science, 14, 47–61. Granfeldt, Y. E., & Bjo¨rck, I. M. E. (2011). A bilberry drink with fermented oatmeal decreases postprandial insulin demand in young healthy adults. Nutrition Journal, 10, 57. Granfeldt, Y., Eliasson, A.-C., & Bjo¨rck, I. (2000). An examination of the possibility of lowering the glycemic index of oat and barley flakes by minimal processing. The Journal of Nutrition, 130, 2207–2214. Granfeldt, Y., Hagander, B., & Bjo¨rck, I. (1995). Metabolic responses to starch in oat and wheat products. On the importance of food structure, incomplete gelatinization or presence of viscous dietary fiber. European Journal of Clinical Nutrition, 49, 189–199. Grover, J. K., Yadav, S., & Vats, V. (2002). Medicinal plants of India with anti-diabetic potential. Journal of Ethnopharmacology, 81, 81–100. Guevarra, M. T. B., & Panlasigui, L. N. (2000). Blood glucose responses of diabetes mellitus type II patients to some local fruits. Asia Pacific Journal of Clinical Nutrition, 9, 303–308. ¨ stman, E., & Bjo¨rck, I. (2012). The glycemic, insulinemic and Gunnerud, U., Holst, J. J., O plasma amino acid responses to equi-carbohydrate milk meals, a pilot- study of bovine and human milk. Nutrition Journal, 11, 83. Ha, T. K. K., & Lean, M. E. J. (1998). Technical review: Recommendations for the nutritional management of patients with diabetes mellitus. European Journal of Clinical Nutrition, 52, 467–481. Haffner, S. M., Lehto, S., Ronnemaa, T., Pyorala, K., & Laakso, M. (1998). Mortality from coronary heart disease in subjects with type 2 diabetes and in nondiabetic subjects with and without prior myocardial infarction. The New England Journal of Medicine, 339, 229–234. Hatonen, K. A., Simila¨, M. E., Virtamo, J. R., Eriksson, J. G., Hannila, M., Sinkko, H. K., et al. (2006). Methodologic considerations in the measurement of glycemic index: Glycemic response to rye bread, oatmeal porridge, and mashed potato. The American Journal of Clinical Nutrition, 84, 1055–1061. Hlebowicz, J., Hlebowicz, A., Lindstedt, S., Bjorgell, O., Hoglund, P., & Holst, J. J. (2009). Effects of 1 and 3 g cinnamon on gastric emptying, satiety, and postprandial blood glucose, insulin, glucose-dependent insulinotropic polypeptide, glucagon-like peptide 1, and ghrelin concentrations in healthy subjects. The American Journal of Clinical Nutrition, 89, 815–821. Hollenbeck, C. B., Coulston, A. M., & Reaven, G. M. (1986). To what extent does increased dietary fiber improve glucose and lipid metabolism in patients with noninsulin dependent diabetes mellitus (NIDDM)? The American Journal of Clinical Nutrition, 43, 16–24. Holt, S., de Jong, V., Faramus, E., Lang, T., & Brand Miller, J. (2003). A bioflavonoid in sugar cane can reduce the postprandial glycemic response to a high-GI starchy food. Asia Pacific Journal of Clinical Nutrition, 12, S66. Holt, S. H., & Miller, J. B. (1994). Particle size, satiety and the glycemic response. European Journal of Clinical Nutrition, 48, 496–502. Hoover-Plow, J., Savesky, J., & Dailey, G. (1987). The glycemic response to meals with six different fruits in insulin-dependent diabetics using a home blood-glucose monitoring system. The American Journal of Clinical Nutrition, 45, 92–97. Hosoda, K., Wang, M. F., Liao, M. L., Chuang, C. K., Iha, M., Clevidence, B., et al. (2003). Antihyperglycemic effect of oolong tea in type 2 diabetes. Diabetes Care, 26, 1714–1718. Hoyt, G., Hickey, M. S., & Cordain, L. (2005). Dissociation of the glycemic and insulinaemic responses to whole and skimmed milk. The British Journal of Nutrition, 93, 175–177. Hsiao-Ling, C. H., Sheu, W. H., Tai, T., Liaw, Y., & Chen, Y. (2003). Konjac supplement alleviated hypercholesterolemia and hyperglycemia in type 2 diabetic subjects—A randomized double-blind trial. Journal of the American College of Nutrition, 22, 36–42.

Food-Based Ingredients to Modulate Blood Glucose

221

Hughes, T. A., Atchison, J., Hazelrig, J. B., & Boshell, B. R. (1989). Glycemic responses in insulin-dependent patients with diabetes: Effect of food composition. The American Journal of Clinical Nutrition, 49, 658–666. Huxley, R., Barzi, F., & Woodward, M. (2006). Excess risk of fatal coronary heart disease associated with diabetes in men and women: Meta-analysis of 37 prospective cohort studies. British Medical Journal, 332, 73–78. Iso, H., Date, C., Wakai, K., Fukui, M., & Tamakoshi, A. (2006). The relationship between green tea and total caffeine intake and risk for self-reported type 2 diabetes among Japanese adults. Annals of Internal Medicine, 144, 554–562. Jarvi, A., Karlstrom, B., Granfeldt, Y., Bjorck, I., & Vessby, B. (1995). The influence of food structure on postprandial metabolism in patients with NIDDM. The American Journal of Clinical Nutrition, 61, 837–842. Jarvill-Taylor, K. J., Anderson, R. A., & Graves, D. J. (2001). A hydroxychalcone derived from cinnamon functions as a mimetic for insulin in 3 T3-L1 adipocytes. Journal of the American College of Nutrition, 20, 327–336. Jenkins, D. J. A., Axelsen, M., Kendall, C. W. C., Augustin, L. S. A., Vuksan, V., & Smith, U. (2000). Dietary fiber, lente carbohydrates and the insulin-resistant diseases. The British Journal of Nutrition, 83, S157–S163. Jenkins, A. L., Jenkins, D. J. A., Zdravkovic, U., Wu¨rsch, P., & Vuksan, V. (2002). Depression of the glycemic index by high levels of beta-glucan fiber in two functional foods tested in type 2 diabetes. European Journal of Clinical Nutrition, 56, 622–628. Jenkins, D. J., Kendall, C. W. C., Augustin, L. S. A., Franceschi, S., Hamidi, M., Marchie, A., et al. (2002). Glycemic index: Overview of implications in health and disease. The American Journal of Clinical Nutrition, 76, 266S–273S. Jenkins, D. J. A., Kendall, C. W. C., Augustin, L. S. A., Martini, M. C., Axelsen, M., Faulkner, D., et al. (2002). Effect of wheat bran on glycemic control and risk factors for cardiovascular disease in type 2 diabetes. Diabetes Care, 25, 1522–1528. Jenkins, D. J. A., Kendall, C. W. C., Josse, A. R., Salvatore, S., Brighenti, F., Augustin, L. S. A., et al. (2006). Almonds decrease postprandial glycaemia, insulinemia, and oxidative damage in healthy individuals. The Journal of Nutrition, 136, 2987–2992. Jenkins, D. J. A., Goff, D. V., Leeds, A. R., Alberti, K. G. M. M., Wolever, T. M. S., Gassull, M. A., et al. (1976). Unabsorbable carbohydrates and diabetes: Decreased postprandial hyperglycemia. The Lancet, 2, 172–174. Jenkins, D. J. A., Wolever, T. M. S., Leeds, A. R., Gassull, M. A., Haisman, P., & Dilawari, J. (1978). Dietary fibers, fiber analogues, and glucose tolerance: Importance of viscosity. British Medical Journal, 1, 1392–1394. Jenkins, D. J., Wolever, T. M., Taylor, R. H., Barker, H., Fielden, H., Baldwin, J. M., et al. (1981). Glycemic index of foods: A physiological basis for carbohydrate exchange. The American Journal of Clinical Nutrition, 34, 362–366. Jenkins, D. H. A., Wolever, T. M. S., Taylor, R. H., Griffiths, C., Krzeminska, K., & Lawrie, J. A. (1982). Slow release carbohydrate improves second meal tolerance. The American Journal of Clinical Nutrition, 35, 1339–1346. Josic, J., Olsson, A. T., Wickeberg, J., Lindstedt, S., & Hlebowicz, J. (2010). Does green tea affect postprandial glucose, insulin and satiety in healthy subjects: A randomized controlled trial. Nutrition Journal, 9, 63. Josse, A. R., Kendall, C. W. C., Augustin, L. S. A., Ellis, P. R., & Jenkins, D. J. A. (2007). Almonds and postprandial glycaemia—A dose–response study. Metabolism, 56, 400–404. Juntunen, K. S., Laaksonen, D. E., Autio, K., Niskanen, L. K., Holst, J. J., Savolainen, K. E., et al. (2003). Structural differences between rye and wheat breads but not total fiber content may explain the lower postprandial insulin response to rye bread. The American Journal of Clinical Nutrition, 78, 957–964.

222

Pariyarath Sangeetha Thondre

Juntunen, K. S., Laaksonen, D. E., Poutanen, K. S., Niskanen, L. K., & Mykkanen, H. M. (2003). High-fiber rye bread and insulin secretion and sensitivity in healthy postmenopausal women. American Journal of Clinical Nutrition, 77, 385–391. Juntunen, K. S., Niskanen, L. K., Liukkonen, K. H., Poutanen, K. S., Holst, J. J., & Mykka¨nen, H. M. (2002). Postprandial glucose, insulin, and incretin responses to grain products in healthy subjects. The American Journal of Clinical Nutrition, 75, 254–262. Kassaian, N., Azadbakht, L., Forghani, B., & Amini, M. (2009). Effect of fenugreek seeds on blood glucose and lipid profiles in type 2 diabetic patients. International Journal of Vitaminology and Nutrition Research, 79, 34–39. Kawano, H., Motoyama, T., Hirashima, O., Hirai, N., Miyao, Y., Sakamoto, T., et al. (1999). Hyperglycemia rapidly suppresses flow-mediated endothelium-dependent vasodilation of brachial artery. Journal of the American College of Cardiology, 34, 146–154. Keogh, G. F., Cooper, G. J. S., Mulvey, T. B., McArdle, B. H., Coles, G. D., Monro, J. A., et al. (2003). Randomized controlled crossover study of the effect of a highly b-glucanenriched barley on cardiovascular disease risk factors in mildly hypercholesterolemic men. The American Journal of Clinical Nutrition, 78, 711–718. Keogh, J. B., Lau, C. W. H., Noakes, M., Bowen, J., & Clifton, P. M. (2007). Effects of meals with high soluble fiber, high amylose barley variant on glucose, insulin, satiety and thermic effect of food in healthy lean women. European Journal of Clinical Nutrition, 61, 597–604. Khan, A., Safdar, M., Ali Khan, M. M., Khattak, K. N., & Anderson, R. A. (2003). Cinnamon improves glucose and lipids of people with type 2 diabetes. Diabetes Care, 26, 3215–3218. Kiens, B., & Richter, E. A. (1996). Types of carbohydrate in an ordinary diet affect insulin action and muscle substrates in humans. The American Journal of Clinical Nutrition, 63, 47–53. Kim, H., Behall, K. M., Vinyard, B., & Conway, J. M. (2006). Short term satiety and glycemic response after consumption of whole grains with various amounts of beta-glucan. Cereal Foods world, 51, 29–33. King, R. A., Noakes, M., Bird, A. R., Morell, M. K., & Topping, D. L. (2008). An extruded breakfast cereal made from a high amylose barley cultivar has a low glycemic index and lower plasma insulin response than one made from a standard barley. Journal of Cereal Science, 48, 526–530. Kirpitch, A. R., & Maryniuk, M. D. (2011). The 3 R’s of glycemic index: Recommendations, research, and the real world. Clinical Diabetes, 29, 155–159. Laaksonen, D. E., Toppinen, L. K., Juntunen, K. S., Autio, K., Liukkonen, K., Poutanen, K. S., et al. (2005). Dietary carbohydrate modification enhances insulin secretion in persons with the metabolic syndrome. The American Journal of Clinical Nutrition, 82, 1218–1227. Lazaridou, A., & Billaderis, C. G. (2007). Molecular aspects of cereal b-glucan functionality: Physical properties, technological applications and physiological effects. Journal of Cereal Science, 46, 101–108. Lett, A. M., Thondre, P. S., & Rosenthal, A. J. (2013). Yellow mustard bran attenuates glycemic response of a semi-solid food in young healthy men. International Journal of Food Sciences and Nutrition, 64, 140–146. Liljeberg, H. G. M., & Bjo¨rck, I. M. E. (1998). Delayed gastric emptying rate may explain improved glycaemia in healthy subjects to a starchy meal with added vinegar. European Journal of Clinical Nutrition, 52, 368–371. Lin, M. A., Wu, M., Lu, S., & Lin, J. (2010). Glycemic index, glycemic load and insulinemic index of Chinese starchy foods. World Journal of Gastroenterology, 21, 4973–4979. Lioger, D., Fardet, A., Foassert, P., Davicco, M.-J., Mardon, J., Gaillard-Martinie, B., et al. (2009). Influence of sourdough prefermentation, of steam cooking suppression and of

Food-Based Ingredients to Modulate Blood Glucose

223

decreased sucrose content during wheat flakes processing on the plasma glucose and insulin responses and satiety of healthy subjects. Journal of the American College of Nutrition, 28, 30–36. Losso, J. N., Holliday, D. L., Finley, J. W., Martin, R. J., Rood, J. C., Yu, Y., et al. (2009). Fenugreek bread: A treatment for diabetes mellitus. Journal of Medicinal Food, 12, 1046–1049. Ludwig, D. S., Majzoub, J. A., Al-Zahrani, A., Dallal, G. E., Blanco, I., & Roberts, S. B. (1999). High glycemic index foods, overeating, and obesity. Pediatrics, 103, E26. Lustman, P. J., & Clouse, R. E. (2005). Depression in diabetic patients: The relationship between mood and glycemic control. Journal of Diabetes Complications, 19, 113–122. Ma¨kela¨inen, H., Anttila, H., Sihvonen, J., Hietanen, R.-M., Tahvonen, R., Salminen, E., et al. (2007). The effect of beta-glucan on the glycemic and insulin index. European Journal of Clinical Nutrition, 61, 779–785. Mang, B., Wolters, M., Schmitt, B., Kelb, K., Lichtinghagen, R., Stichtenoth, D. O., et al. (2006). Effects of a cinnamon extract on plasma glucose, HbA1c, and serum lipids in diabetes mellitus type 2. European Journal of Clinical Investigation, 36, 340–344. Marques, C., D’auria, L., Cani, P. D., Baccelli, C., Rozenberg, R., & Ruibal-Mendieta, N. L. (2007). Comparison of glycemic index of spelt and wheat bread in human volunteers. Food Chemistry, 100, 1265–1271. Maruyama, K., Iso, H., Sasaki, S., & Fukino, Y. (2009). The association between concentrations of green tea and blood glucose levels. Journal of Clinical Biochemistry and Nutrition, 44, 41–45. Meyer, K. A., Kushi, L. H., Jacobs, D. R., Jr., Slavin, J., Sellers, T. A., & Folsom, A. R. (2000). Carbohydrates, dietary fiber, and incident type 2 diabetes in older women. The American Journal of Clinical Nutrition, 71, 921–930. Moghaddam, E., Vogt, J. A., & Wolever, T. M. S. (2006). The effects of fat and protein on glycemic responses in nondiabetic humans vary with waist circumference, fasting plasma insulin and dietary fiber intake. The Journal of Nutrition, 136, 2506–2511. Mollard, R. C., Zykus, A., Luhovyy, B. L., Nunez, M. F., Wong, C. L., & Anderson, G. H. (2012). The acute effects of a pulse-containing meal on glycemic responses and measures of satiety and satiation within and at a later meal. The British Journal of Nutrition, 108, 509–517. Munari, F., Benitez-Pinto, A. C., Araiza-Andraca, W., & Casarrubias-Moises, R. (1998). Lowering glycemic index of food by acarbose and Plantago psyllium mucilage. Archives of Medical Research, 29, 137–141. Natah, S. S., Hussien, K. R., Tuominen, J. A., & Koivisto, V. A. (1997). Metabolic response to lactitol and xylitol in healthy men. The American Journal of Clinical Nutrition, 65, 947–950. Nielsen, P. H., & Nielsen, G. L. (1989). Pre-prandial blood glucose values: Influence on glycemic response studies. The American Journal of Clinical Nutrition, 53, 1243–1246. ¨ stman, E. M., Granfeldt, Y., & Bjo¨rck, I. M. E. (2008). Effect of cereal test Nilsson, A. C., O breakfasts differing in glycemic index and content of indigestible carbohydrates on daylong glucose tolerance in healthy subjects. The American Journal of Clinical Nutrition, 87, 3645–3654. Nilsson, M., Stenberg, M., Frid, A. H., Holst, J. J., & Bjo¨rck, I. M. E. (2004). Glycaemia and insulinemia in healthy subjects after lactose-equivalent meals of milk and other food proteins: The role of plasma amino acids and incretins. The American Journal of Clinical Nutrition, 80, 1246–1253. Niskanen, L., Turpeinen, A., Penttila, I., & Usitupa, M. I. (1998). Hyperglycemia and compositional lipoprotein abnormalities as predictors of cardiovascular mortality in type 2 diabetes: A 15-year follow-up from the time of diagnosis. Diabetes Care, 21, 1861–1869.

224

Pariyarath Sangeetha Thondre

O’Dea, K., Snow, P., & Nestel, P. (1981). Rate of starch hydrolysis in vitro as a predictor of metabolic responses to complex carbohydrate in vivo. The American Journal of Clinical Nutrition, 34, 1991–1993. Ohkubo, Y., Kishikawa, H., Araki, E., Miyata, T., Isami, S., Motoyashi, S., et al. (1995). Intensive insulin therapy prevents the progression of diabetic microvascular complications in Japanese patients with non-insulin-dependent diabetes mellitus: A randomized prospective 6-year study. Diabetes Research and Clinical Practise, 28, 103–117. Ostman, E. M., Frid, A. H., Groop, L. C., & Bjorck, I. M. E. (2006). A dietary exchange of common bread for tailored bread of low glycemic index and rich in dietary fiber improved insulin economy in young women with impaired glucose tolerance. European Journal of Clinical Nutrition, 60, 334–341. ¨ stman, E., Granfeldt, Y., Persson, L., & Bjo¨rck, I. (2005). Vinegar supplementation lowers O glucose and insulin responses and increases satiety after a bread meal in healthy subjects. European Journal of Clinical Nutrition, 59, 983–988. ¨ stman, E. M., Liljeberg Elmsta˚hl, H. G., & Bjo¨rck, I. M. (2001). Inconsistency between O glycemic and insulinemic responses to regular and fermented milk products. The American Journal of Clinical Nutrition, 74, 96–100. Ostman, E. M., Liljeberg Elmsta˚hl, H. G., & Bjorck, I. M. (2002). Barley bread containing lactic acid improves glucose tolerance at a subsequent meal in healthy men and women. The Journal of Nutrition, 132, 1173–1175. Ou, S., Kwok, K., Li, Y., & Fu, L. (2001). In vitro study of possible role of dietary fiber in lowering postprandial serum glucose. Journal of Agriculture and Food Chemistry, 49, 1026–1029. Panahi, S., Ezatagha, A., Temelli, F., Vasanthan, T., & Vuksan, V. (2007). b-Glucan from two sources of oat concentrates affect postprandial glycemia in relation to the level of viscosity. Journal of the American College of Nutrition, 26, 6639–6644. Parillo, M., Giacco, R., Ciardullo, A. V., Rivellese, A. A., & Riccardi, G. (1996). Does a high-carbohydrate diet have different effects in NIDDM patients treated with diet alone or hypoglycemic drugs? Diabetes Care, 19, 498–500. Parillo, M., Giacco, R., Riccardi, G., Pacioni, D., & Rivellese, A. (1985). Different glycemic responses to pasta, bread, and potatoes in diabetic patients. Diabetic Medicine, 2, 374–377. Pawlak, D. B., Ebbeling, C. B., & Ludwig, D. S. (2002). Should obese patients be counselled to follow a low-glycemic index diet? Yes. Obesity Reviews, 3, 235–243. Payne, M. L., Craig, W. J., & Williams, A. C. (1997). Sorbitol is a possible risk factor for diarrhea in young children. Journal of the American Dietetic Association, 97, 532–534. Pereira, M. A., Jacobs, D. R., Van Horn, L., Slattery, M. L., Kartashov, A. I., & Ludwig, D. S. (2002). Dairy consumption, obesity, and the insulin resistance syndrome in young adults: The CARDIA Study. Journal of the American Medical Association, 287, 2081–2089. Pick, M. E., Hawrysh, Z. J., Gee, M. I., Toth, E., Garg, M. L., & Hardin, R. T. (1996). Oat bran concentrate bread products improve long-term control of diabetes: A pilot study. Journal of the American Dietetic Association, 96, 1254–1261. Poppitt, S. D., van Drunen, J. D. E., McGill, A., Mulvey, T. B., & Leahy, F. E. (2007). Supplementation of a high-carbohydrate breakfast with barley b-glucan improves postprandial glycemic response for meals but not beverages. Asia Pacific Journal of Clinical Nutrition, 16, 16–24. Qin, B., Nagasaki, M., Ren, M., Bajotto, G., Oshida, Y., & Sato, Y. (2003). Cinnamon extract (traditional herb) potentiates in vivo insulin-regulated glucose utilization via enhancing insulin signaling in rats. Diabetes Research in Clinical Practise, 62, 139–148. Raben, A. (2002). Should obese patients be counselled to follow a low-glycemic index diet? No. Obesity Reviews, 3, 245–256.

Food-Based Ingredients to Modulate Blood Glucose

225

Raben, A., Holst, J. J., Madsen, J., & Astrup, A. (2001). Diurnal metabolic profiles after 14 d of an ad libitum high-starch, high-sucrose, or high-fat diet in normal-weight neverobese and post obese women. The American Journal of Clinical Nutrition, 73, 177–189. Raben, A., Macdonald, I., & Astrup, A. (1997). Replacement of dietary fat by sucrose or starch: Effects on 14 d ad libitum energy intake, energy expenditure and body weight in formerly obese and never-obese subjects. International Journal of Obesity and Related Metabolic Disorders, 21. Radhika, G., Sumathi, C., Ganesan, A., Sudha, V., Henry, C. J. K., & Mohan, V. (2010). Glycemic index of Indian flatbreads (rotis) prepared using whole wheat flour and ‘atta mix’-added whole wheat flour. The British Journal of Nutrition, 103, 1642–1647. Rasmussen, I., & Hermansen, K. (1991). Preprandial blood glucose values and glycemic responses in insulin-dependent diabetes mellitus at constant insulinemia. The American Journal of Clinical Nutrition, 53, 520–523. Regand, A., Tosh, S. M., Wolever, T. M. S., & Wood, P. J. (2009). Physicochemical properties of b-glucan in differently processed oat foods influence glycemic response. Journal of Agriculture and Food Chemistry, 57, 8831–8838. Riccardi, G., Rivellese, A. A., & Giacco, R. (2008). Role of glycemic index and glycemic load in the healthy state, in pre-diabetes and in diabetes. The American Journal of Clinical Nutrition, 87, 269–274. Roberts, S. B. (2000). High-glycemic index foods, hunger, and obesity: Is there a connection. Nutrition Reviews, 58, 163–169. Roberts, K. T. (2011). The physiological and rheological effects of foods supplemented with guar gum. Food Research International, 44, 1109–1114. Sakuma, M., Yamanaka-Okumura, H., Naniwa, Y., Matsumoto, D., Tsunematsu, M., Yamamoto, H., et al. (2009). Dose-dependent effects of barley cooked with white rice on postprandial glucose and desacyl ghrelin levels. Journal of Clinical Biochemistry and Nutrition, 44, 151–159. Salmeron, J., Ascherio, A., Rimm, E. B., Colditz, G. A., Spiegelman, D., Jenkins, D. J., et al. (1997). Dietary fiber, glycemic load, and risk of NIDDM in men. Diabetes Care, 20, 545–550. Salmeron, J., Manson, J. E., Stampfer, M. J., Colditz, G. A., Wing, A. L., & Willett, W. C. (1997). Dietary fiber, glycemic load, and risk of non-insulin-dependent diabetes mellitus in women. Journal of the American Medical Association, 277, 472–477. Samra, R. A., & Anderson, G. H. (2007). Insoluble cereal fiber reduces appetite and shortterm food intake and glycemic response to food consumed 75 min later by healthy men. The American Journal of Clinical Nutrition, 86, 972–979. Scazzina, F., Rio, D. D., Pellegrini, N., & Brighenti, F. (2009). Sourdough bread: Starch digestibility and postprandial glycemic response. Journal of Cereal Science, 49, 419–421. Schenk, S., Davidson, C. J., Zderic, T. W., Byerley, L. O., & Coyle, E. F. (2003). Different glycemic indexes of breakfast cereals are not due to glucose entry into blood but to glucose removal by tissue. The American Journal of Clinical Nutrition, 78, 742–748. Schvarcz, E., Palmer, M., Aman, J., Lindkvist, B., & Beckman, K. W. (1993). Hypoglycemia increases gastric emptying rate in patients with type 1 diabetes mellitus. Diabetes Medicine, 10, 660–663. Sheard, N. F., Clark, N. G., Brand-Miller, J. C., Franz, M. J., Pi-Sunyer, F. X., & MayerDavis, E. (2004). Dietary carbohydrate (amount and type) in the prevention and management of diabetes: A statement by the American Diabetes Association. Diabetes Care, 27, 2266–2271. Sievenpiper, J. L., Kendall, C. W. C., Esfahani, A., Wong, J. M. W., Carleton, A. J., & Jiang, H. Y. (2009). Effect of non-oil-seed pulses on glycemic control: A systematic review and meta-analysis of randomized controlled experimental trials in people with and without diabetes. Diabetologia, 52, 1479–1495.

226

Pariyarath Sangeetha Thondre

Sloth, B., Krog-Mikkelsen, I., Flint, A., Tetens, I., Bjorck, I., Vinoy, S., et al. (2004). No difference in body weight decrease between a low-glycemic-index and a highglycemic-index diet but reduced LDL cholesterol after 10-wk ad libitum intake of the low-glycemic-index diet. The American Journal of Clinical Nutrition, 80, 337–347. Smith, C. E., Mollard, R. C., Luhovyy, B. L., & Anderson, G. H. (2012). The effect of yellow pea protein and fiber on short-term food intake, subjective appetite and glycemic response in healthy young men. The British Journal of Nutrition, 108, S74–S80. Smith, K. N., Queenan, K. M., Thomas, W., Fulcher, R. G., & Slavin, J. L. (2008). Physiological effects of concentrated barley b-glucan in mildly hypercholesterolemic adults. Journal of the American College of Nutrition, 27, 434–440. Snow, P., & O’Dea, K. (1981). Factors affecting the rate of hydrolysis of starch in food. The American Journal of Clinical Nutrition, 34, 2721–2727. Solomon, T. P., & Blannin, A. K. (2009). Changes in glucose tolerance and insulin sensitivity following 2 weeks of daily cinnamon ingestion in healthy humans. European Journal of Applied Physiology, 105, 969–976. Song, Y., Manson, J. E., Buring, J. E., Sesso, H. D., & Liu, S. (2005). Associations of dietary flavonoids with risk of type 2 diabetes, and markers of insulin resistance and systemic inflammation in women: A prospective study and cross-sectional analysis. Journal of the American College of Nutrition, 24, 376–384. Spieth, L. E., Harnish, J. D., Lenders, C. M., Raezer, L. B., Pereira, M. A., Hangen, S. J., et al. (2000). A low-glycemic index diet in the treatment of pediatric obesity. Archives of Pediatrics & Adolescent Medicine, 154, 947–951. Swanson, J. E., Laine, D. C., Thomas, W., & Bantle, J. P. (1992). Metabolic effects of dietary fructose in healthy subjects. The American Journal of Clinical Nutrition, 55, 851–856. Tapola, N., Karvonen, H., Niskanen, L., Mikola, M., & Sarkkinen, E. (2005). Glycemic responses of oat bran products in type 2 diabetic patients. Nutrition, Metabolism, and Cardiovascular Diseases, 15, 255–261. Tappy, L., Gugolz, E., & Wursch, P. (1996). Effects of breakfast cereals containing various amounts of beta-glucan fibers on plasma glucose and insulin responses in NIDDM subjects. Diabetes Care, 19, 831–834. Thompson, S. V., Winham, D. M., & Hutchins, A. M. (2012). Bean and rice meals reduce postprandial glycemic response in adults with type 2 diabetes: A cross-over study. Nutrition Journal, 11, 23. Thompson, L. U., Yoon, J. H., Jenkins, D. J., Wolever, T. M., & Jenkins, A. L. (1984). Relationship between polyphenol intake and blood glucose response of normal and diabetic individuals. The American Journal of Clinical Nutrition, 39, 745–751. Thondre, P. S., & Henry, C. J. K. (2009). High-molecular-weight barley b-glucan in chapattis (unleavened Indian flatbread) lowers glycemic index. Nutrition Research, 29, 480–486. Thondre, P. S., & Henry, C. J. K. (2011). Effect of a low molecular weight, high-purity b-glucan on in vitro digestion and glycemic response. International Journal of Food Sciences and Nutrition, 62, 678–684. Thondre, P. S., Monro, J. A., Mishra, S., & Henry, C. J. K. (2010). High molecular weight barley beta-glucan decreases particle breakdown in chapattis (Indian flat breads) during in vitro digestion. Food Research International, 43, 1476–1481. To¨rro¨nen, R., McDougall, G. J., Dobson, G., Stewart, D., Hellstro¨m, J., Mattila, P., et al. (2012). Fortification of blackcurrant juice with crowberry: Impact on polyphenol composition, urinary phenolic metabolites, and postprandial glycemic response in healthy subjects. Journal of Functional Foods, 4, 746–756. To¨rro¨nen, R., Sarkkinen, E., Tapola, N., Hautaniemi, E., & Niskanen, L. (2010). Berries modify the postprandial plasma glucose response to sucrose in healthy subjects. The British Journal of Nutrition, 103, 1094–1097.

Food-Based Ingredients to Modulate Blood Glucose

227

Tosh, S. M., Brummer, Y., Wolever, T. M. S., & Wood, P. J. (2008). Glycemic response to oat bran muffins treated to vary molecular weight of b-glucan. Cereal Chemistry, 85, 211–217. Tuomasjukka, S., Viitanen, M., & Kallio, H. (2007). The glycemic response to rolled oat is not influenced by the fat content. The British Journal of Nutrition, 97, 744–748. Udani, J. K., Singh, B. B., Barrett, M. L., & Preuss, H. G. (2009). Lowering the glycemic index of white bread using a white bean extract. Nutrition Journal, 8, 52. UK Prospective Diabetes Group (1998). Intensive blood glucose control with sulphonylureas or insulin compared with conventional treatment and risk of complications in patients with type 2 diabetes. The Lancet, 352, 837–853. Vanschoonbeek, K., Thomassen, B. J., Senden, J. M., Wodzig, W. K., & van Loon, L. J. (2006). Cinnamon supplementation does not improve glycemic control in postmenopausal type 2 diabetes patients. The Journal of Nutrition, 136, 977–980. Wilson, T., Anderson, J. A., Andersen, K. F., Heimerman, R. A., Larson, M. M., & Freeman, M. R. (2012). Glycemic response of type 2 diabetics to raisins. Food and Nutrition Sciences, 3, 1162–1166. Wilson, T., Luebke, J. L., Morcomb, E. F., Carrell, E. J., Leveranz, M. C., Kobs, L., et al. (2010). Glycemic responses to sweetened dried and raw cranberries in humans with type 2 diabetes. Journal of Food Science, 75, H218–H223. Wilson, T., Meyers, S. L., Singh, A. P., Limburg, P. J., & Vorsa, N. (2008). Favorable glycemic response of type 2 diabetics to low-calorie cranberry juice. Journal of Food Science, 73, H241–H245. Wolever, T. M., Bentum-Williams, A., & Jenkins, D. J. (1995). Physiological modulation of plasma free fatty acid concentrations by diet metabolic implications in nondiabetic subjects. Diabetes Care, 18, 962–970. Wolever, T. M. S., Jenkins, D. J. A., Nineham, R., & Alberti, K. G. M. M. (1979). Guar gum and reduction of postprandial glycaemia: Effect of incorporation into solid food, liquid food and both. The British Journal of Nutrition, 41, 505–510. Wolever, T. M., & Mehling, C. (2002). High-carbohydrate-low-glycemic index dietary advice improves glucose disposition index in subjects with impaired glucose tolerance. The British Journal of Nutrition, 87, 477–487. Wolever, T. M. S., Nguyen, P. M., & Chiasson, J. L. (1994). Determinants of diet glycemic index calculated retrospectively from diet records of 342 individuals with noninsulin-dependent diabetes mellitus. The American Journal of Clinical Nutrition, 59, 1265–1269. Wolever, T. M. S., Spadafora, P., & Eshuis, H. (1991). Interaction between colonic acetate and propionate in Humans. The American Journal of Clinical Nutrition, 53, 681–687. Wong, C. L., Mollard, R. C., Zafar, T. A., Luhovyy, B. L., & Anderson, G. H. (2009). Food intake and satiety following a serving of pulses in young men: Effect of processing, recipe, and pulse variety. Journal of the American College of Nutrition, 28, 5543–5552. World Health Organization. (2006). Definition and diagnosis of diabetes mellitus and intermediate hyperglycemia. Report of a WHO/IDF Consultation (pp. 1–46). Available at: http://www.who.int. Zunino, S. J. (2009). Type 2 diabetes and glycemic response to grapes or grape products. The Journal of Nutrition, 139, 1794S–1800S.