PRESENTATION

Can Whole Grain Help in Weight Management? Frank Thielecke, PhD*w and Satya S. Jonnalagadda, PhDzy

Background: Evidence from epidemiological studies suggests that higher whole grain intake is associated with improvements in body weight measures. Evidence from randomized controlled intervention studies is controversial.

METHODOLOGY

hole grains have received increased attention for their potential role in weight regulation. Epidemiological evidence shows that higher whole grain intake, when compared with lower whole grain intake, is associated with lower BMI, body weight, and abdominal adiposity, smaller waist circumference and smaller weight gain over time.1–4 However, the evidence from randomized controlled studies is less consistent. The objective of this review was to assess the scientific evidence, both from epidemiological and randomized controlled studies, related to the effects of whole grain on weight management using a descriptive systematic approach.

A systematic literature search in Medline and Scopus was conducted. Studies were included in the review if they were epidemiological studies and randomized controlled intervention studies of whole grain versus a non–whole grain control in adults. The period under review was from 1980 to date; the search was completed in July 2013. Two researchers assessed abstracts independently using hierarchically targeted selection criteria:  Full text in English.  Original research (no comments, no letters), including secondary analyses, reviews, and meta-analyses.  Human studies.  Relevant to research question (Effects of whole grain on obesity/weight management).  For epidemiological studies and intervention studies, outcomes, population, and statistical analyses were reported. For intervention studies, in addition to the above, randomization and type of intervention had to be described. When no abstract was available titles, source, and key words were reviewed. The decisions were recorded and compared. When necessary, the reviewers reconciled differences of opinion. Exclusion criteria were documented. At this stage, articles were included if requested by one of the two reviewers. The obtained full text of the remaining articles was peer-reviewed with the same criteria. If additional articles were suggested during the peer-review process, they went through the same screening process as the original articles. The basic search strategy was developed using the National Library of Medicine Medical Subject Headings (MeSH) key word nomenclature developed for MEDLINE. The same strategy was used to search in Scopus. An initial search was performed limited to titles, key words, and abstracts to assess the potential yield of the search strategy. On the basis of the results, search terms were modified (eg, wild characters) or additional terms were included. A subsequent search included MeSH terms or controlled terms, respectively. The search was further limited using the key word “Human.” The search terms were grouped into 2 different concepts (Table 1), which were combined with Boolean term “AND.” Terms within each concept were combined with the Boolean term “OR.”

From the *Cereal Partners Worldwide S.A.; wNestle´ Research Centre, Nestec Ltd, Vers-chez-les-Blanc, Lausanne, Switzerland; zGeneral Mills Bell Institute of Health and Nutrition, Golden Valley, MN; and yKerry Ingredients & Flavours, Beloit, WI. F.T. was an employee of Cereal Partners World and S.S.J. of General Mills at the time this project was conducted. Cereal Partners Worldwide and General Mills produce whole grain food products. Reprints: Frank Thielecke, PhD, Nestle´ Research Centre, Nestec Ltd, Vers-chez-les-Blanc, 1000 Lausanne 26, Switzerland (e-mail: [email protected]). Copyright r 2014 by Lippincott Williams & Wilkins

After the initial search of the bibliographic databases Medline, and Scopus, and after checking for duplicates, a total of 1993 articles were retrieved. Two reviewers read the abstracts of these articles against the selection criteria. When no abstract was available, title, source, and key words were reviewed. At this stage, articles were included if requested by 1 of the 2 reviewers, resulting in 75 articles. The general study selection process that was applied for the bibliographic

Objective: To assess the scientific evidence, using a descriptive systematic approach, related to the relationship/effects of whole grain on weight management. Methods: Medicine Medical Subject Headings (MeSH) were used to search in Medline and Scopus, dating from 1980 to July 2013. Subsequently, 2 researchers assessed independently the resulting abstracts, using hierarchically targeted selection criteria. Results: A moderate body of evidence from epidemiological studies consistently demonstrates that a higher intake of whole grains is associated with lower body weight, BMI, waist circumference, abdominal adiposity, and weight gain. The evidence from intervention studies is, in comparison, limited and less consistent. Current evidence fails to clearly demonstrate that whole grain intake can contribute to weight loss independent of hypocaloric diets. The lack of consistency in intervention studies may partly be explained by heterogeneity in study duration, types and amounts of whole grain foods included, population, and sample sizes. Conclusions: Future epidemiological and intervention studies are needed to address the limitations observed in the current body of evidence, importantly using a consistent definition of whole grain foods, and the amount of whole grains consumed. Furthermore, studies need to be conducted on diets that potentially include single grains. Key Words: whole grain, weight management, systematic review

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Can Whole Grain Help in Weight Management?

TABLE 1. Search Terms and Concepts

Concept 1 2

Search Terms Whole grain, wholegrain, wholemeal, whole wheat, whole rye, whole barley, whole corn, whole rice, brown rice Weight loss, weight reduction, weight gain, BMI, body composition, body fat, fat tissue, fat mass, abdominal fat, waist circumference, WHR ratio, overweight, obese, obesity, satiety, hunger, fat oxidation, nutrient utilization, energy expenditure, energy intake, adiposity

databases is summarized in Figure 1. Reasons for exclusion were full text not available (n = 4), not original research (n = 17), or missing baseline values (n = 37). The studies applied a variety of measures used to assess body weight (actual body weight; weight gained or lost over time; BMI; abdominal adiposity as measured by waist circumference; waist-to-hip ratio; and body composition analysis by DEXA, CAT, etc.). In addition, researchers designing the studies controlled for other dietary/nutritional and lifestyle factors (eg, calories, fat, dietary fiber, physical activity, etc.) to negate any potential influence that may have been implied by their presence on the relationship between whole grain and healthy body weight. For example, what people consumed in addition to whole grain, such as a low fat diet, did not influence the outcome of the studies.

Epidemiological Evidence Of the 31 epidemiology studies, 8 prospective and 19 cross-sectional studies show an inverse association between whole grain consumption and weight management outcomes. One cross-sectional study did not show a benefit of whole grain consumption, and 3 epidemiological studies

were not applicable for this review as they did not report weight-related outcomes. In general, these epidemiological studies show that higher intake of whole grains, a daily intake of B3 servings (serving being 16 g whole grain), is associated with lower BMI (kg/m2) in adults, smaller waist circumferences, and smaller waist-to-hip ratio. Generally, an B1-unit difference in BMI was observed between the highest and lowest whole grain intakes. Harland and Garton,5 in a systematic review of the evidence, showed modest reduction in BMI (0.63 kg/m2) and waist circumference (2.7 cm) with the consumption of 3 servings/d of whole grains. Koh-Banerjee et al6 estimated that for every 40-g increase in daily whole grain intake, the 8-years weight gain was lower by 1.1 kg. Recently, Ye et al4 in a systematic review of longitudinal studies reported an inverse association between whole grain and weight gain over time. Ye and colleagues found that compared with never/rare consumers of whole grains, those consuming 48 to 80 g whole grain/d (3 to 5 servings/d) had consistently less weight gain during 8 to 13 years (1.27 vs. 1.64 kg; P = 0.001). A few studies have shown that higher intakes of whole grain foods were associated, in a dose-dependent manner, with lower abdominal fat and subcutaneous and visceral adipose tissue volume; in the study by McKeown et al7 whole grain intake in the top quintile was 3 servings/d compared with 0.5 servings/d in the lowest quintile. In contrast, no significant relationship was observed with refined-grain intake. These prospective studies suggest that weight gain and increases in abdominal adiposity over time are lower in people who consume more whole grains. These observational epidemiology studies highlight an association between higher whole grain intake and lower body measures (Table 2), but do not demonstrate causality. It should be noted that majority of these studies were conducted in US cohorts and among adults. It is possible that the observed beneficial associations between higher whole grain intake and body TABLE 2. Summary of Observed Whole Grain Effects on Weight Management Outcomes

Show an Association

Type of Studies

FIGURE 1. Study selection process. r

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Epi studies Prospective Cross-sectional Intervention studies Satiety studies Weight loss studies Satiety & weight loss combination study Meta-analyses Review Total

Not Applicable (No Weight Management–related Number Yes No Outcome) 31 10 21 37 21 15 1 2 5 75

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Nutritional Research Clinical Nutrition Obesity (Silver Spring) Proceedings of the Nutrition Society

Appetite Cereal Foods World Nutritional Research

American Journal of Clinical Nutrition

Journal of Nutrition

Nutrition Journal European Journal of Clinical Nutrition Nutrition Journal Food & Nutrition Research Nutricion Hospitalaria

Nutrition Journal

Public Health Nutrition Regulatory Peptides

European Journal of Clinical Nutrition The American Journal of Clinical Nutrition The American Journal of Clinical Nutrition Journal of the American Dietetic Association Journal of the American College of Nutrition

Public Health Nutrition

American Journal of Epidemiology

Journal of Human Nutrition International Journal of Obesity

The British Journal of Nutrition The British Journal of Nutrition

Obesity Research Journal of the American Dietetic Association Archives of Pediatrics & Adolescent Medicine

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Dietary intake of whole and refined-grain breakfast cereals and weight gain in men Whole-Grain Diets Reduce Blood Pressure in Mildly Hypercholesterolemic Men and Women Use of a DASH food group score to predict excess weight gain in adolescent girls in the National Growth and Health Study Short-term effects of whole-grain wheat on appetite and food intake in healthy adults: a pilot study Markers of cardiovascular risk are not changed by increased whole-grain intake: The WHOLEheart study, a randomised, controlled dietary intervention Wholemeal bread and satiety Glycemic index, cholecystokinin, satiety and disinhibition: Is there an unappreciated paradox for overweight women? Relation of dietary glycemic index, glycemic load, and fiber and whole-grain intakes during puberty to the concurrent development of percent body fat and body mass index Intake of wholegrain products is associated with dietary, lifestyle, anthropometric and socio-economic factors in Denmark Whole-grain consumption and the metabolic syndrome: A favorable association in Tehranian adults Whole-grain intake and the prevalence of hypertriglyceridemic waist phenotype in Tehranian adults Use of an expanded-whole-wheat product in the reduction of body weight and serum lipids in obese females. Carbohydrate quantity and quality in relation to body mass index Whole grain consumption and body mass index in adult women: an analysis of NHANES 1999-2000 and the USDA pyramid servings database Whole-grain intake as a marker of healthy body weight and adiposity Plasma ghrelin levels after two high-carbohydrate meals producing different insulin responses in patients with metabolic syndrome Effect of commercial breakfast fibre cereals compared with corn flakes on postprandial blood glucose, gastric emptying and satiety in healthy subjects: A randomized blinded crossover trial The botanical integrity of wheat products influences the gastric distention and satiety in healthy subjects Particle size, satiety and the glycaemic response Rye kernel breakfast increases satiety in the afternoon - an effect of food structure Whole grain rye porridge breakfast improves satiety compared with refined wheat bread breakfast The use of low glycemic and high satiety index food dishes in Mexico: a low cost approach to prevent and control obesity and diabetes Putting the whole Grain Puzzle Together: Health benefits associated with whole grains-summary of American Society for Nutrition 2010 satellite symposium The effects of a whole grain-enriched hypocaloric diet on cardiovascular disease risk factors in men and women with metabolic syndrome Food intake, postprandial glucose, insulin and subjective satiety responses to three different bread-based test meals Short-term satiety and glycemic response after consumption of whole grains with various amounts of Iˆ2-glucan Meal replacement with mixed rice is more effective than white rice in weight control, while improving antioxidant enzyme activity in obese women Intake of brown rice lees reduces waist circumference and improves metabolic parameters in type 2 diabetes Breakfast cereals and risk of hypertension in the Physicians’ Health Study I Breakfast cereals and risk of type 2 diabetes in the Physicians’ Health Study I Whole grain consumption and weight gain: A review of the epidemiological evidence, potential mechanisms and opportunities for future research Changes in whole-grain, bran, and cereal fiber consumption in relation to 8-years weight gain among men

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References

TABLE 3. Literature Identified by Both Authors

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Nutritional Research

Journal of Nutrition

The American Journal of Clinical Nutrition The American Journal of Clinical Nutrition

Diabetes Care

The New England Journal of Medicine Pakistan Journal of Nutrition

Journal of the American Dietetic Association

Journal of Nutrition The American Journal of Clinical Nutrition

Journal of Nutrition The American Journal of Clinical Nutrition

Journal of the American Dietetic Association

The British Journal of Nutrition

The American Journal of Clinical Nutrition

Public Health Nutrition Journal of Nutrition

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Wholegrain vs. refined wheat bread and pasta. Effect on postprandial glycemia, appetite, and subsequent ad libitum energy intake in young healthy adults Intake of whole grains in Scandinavia is associated with healthy lifestyle, socio-economic and dietary factors Metabolomic analysis of plasma metabolites that may mediate effects of rye bread on satiety and weight maintenance in postmenopausal women Relation between changes in intakes of dietary fiber and grain products and changes in weight and development of obesity among middle-aged women Whole grain intake and its cross-sectional association with obesity, insulin resistance, inflammation, diabetes and subclinical CVD: The MESA Study Whole-grain ready-to-eat oat cereal, as part of a dietary program for weight loss, reduces low-density lipoprotein cholesterol in adults with overweight and obesity more than a dietary program including low-fiber control foods Whole and refined-grain intakes are related to inflammatory protein concentrations in human plasma Whole- and refined-grain intakes are differentially associated with abdominal visceral and subcutaneous adiposity in healthy adults: the Framingham Heart Study Whole-grain intake and cereal fiber are associated with lower abdominal adiposity in older adults Whole-grain intake is favorably associated with metabolic risk factors for type 2 diabetes and cardiovascular disease in the Framingham Offspring Study Consumption of whole-grain cereals during weight loss: effects on dietary quality, dietary fiber, magnesium, vitamin B-6, and obesity Changes in diet and lifestyle and long-term weight gain in women and men Supplementation of whole grain on body weight and lipid profile in obese females of various ethnic groups in Balochistan, Pakistan Interactions of dietary whole-grain intake with fasting glucose- and insulin-related genetic loci in individuals of European descent: a meta-analysis of 14 cohort studies Dietary patterns and changes in body mass index and waist circumference in adults Intake of whole grains, refined grains, and cereal fiber measured with 7-days diet records and associations with risk factors for chronic disease Including indigestible carbohydrates in the evening meal of healthy subjects improves glucose tolerance, lowers inflammatory markers, and increases satiety after a subsequent standardized breakfast Whole grain and fiber consumption are associated with lower body weight measures in US adults: National Health and Nutrition Examination Survey 1999-2004 Satiety from rice-based, wheat-based and rice-pulse combination preparations Improvement of insulin resistance after diet with a whole-grain based dietary product: Results of a randomized, controlled cross-over study in obese subjects with elevated fasting blood glucose Whole-grain intake is associated with body mass index in college students Endosperm and whole grain rye breads are characterized by low post-prandial insulin response and a beneficial blood glucose profile Effects of cereal breakfasts on postprandial glucose, appetite regulation and voluntary energy intake at a subsequent standardized lunch; focusing on rye products Postprandial Glycaemia, Insulinaemia and Satiety Responses in Healthy Subjects after Wholegrain Rye Bread Made From Different Rye Varieties. PART A Effects of a cereal rich in soluble fiber on body composition and dietary compliance during consumption of a hypocaloric diet Influence of whole grain barley, whole grain wheat, and refined rice-based foods on short-term satiety and energy intake Why whole grains are protective: Biological mechanisms Whole grain intake is associated with lower body mass and greater insulin sensitivity among adolescents



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measures are a reflection of healthier lifestyles and dietary patterns, with diets high in whole grains being more nutrientdense and less energy-dense.

Intervention Studies

Whole grains and adiposity: Little association among British adults Effect of barley incorporation in bread on its quality and glycemic responses in diabetics Whole-grain consumption, dietary fibre intake and body mass index in the Netherlands cohort study The effect of increasing consumption of pulses and wholegrains in obese people: a randomized controlled trial Reduction in postprandial glucose excursion and prolongation of satiety: possible explanation of the long-term effects of whole grain Salba (Salvia Hispanica L.) Efficacy of high-fiber diets in the management of type 2 diabetes mellitus Relationship between whole grain and fiber consumption and body weight measures among 6- to 18-year-olds Substituting white rice with brown rice for 16 wk does not substantially affect metabolic risk factors in middle-aged chinese men and women with diabetes or a high risk for diabetes Whole-grain intake is inversely associated with the metabolic syndrome and mortality in older adults Relationship between whole-grain intake, chronic disease risk indicators, and weight status among adolescents in the National Health and Nutrition Examination Survey, 1999-2004 Whole grain and body weight changes in apparently healthy adults: A systematic review and meta-analysis of randomized controlled studies A whole-grain cereal-rich diet increases plasma betaine, and tends to decrease total and LDL-cholesterol compared with a refined-grain diet in healthy subjects The role of whole grains in body weight regulation 63 64 65 66 67

References

TABLE 3. (continued)

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Of the 37 intervention studies, 21 were classified as short-term, acute response, satiety studies, 15 were classified as long-term, weight loss studies, and 1 was a combination study that included satiety and weight loss. Whereas 16 of the 21 satiety studies showed an effect of whole grain intake on subjective satiety measures (hunger, fullness, and overall satiety) over the course of a few hours, day, or several days, 5 studies did not demonstrate an effect of whole grain on subjective satiety (Table 2). However, very few of these studies demonstrated any impact of these subjective satiety effects of whole grains on energy intake either at the next meal or over the course of the day. Hence, further research is needed to better understand the satiety effects of whole grains and their impact on weight management. Ten of 15 weight loss studies showed an effect of whole grain consumption, in the context of hypocaloric diet, on body weight, and/or body composition. These intervention studies used a hypocaloric design to examine the impact of whole grain diets on metabolic risk factors. Five studies did not show an effect of whole grain consumption on anthropometric measures. The impact of whole grain diets on changes in body weight beyond the changes expected from calorie restriction can be considered as secondary outcomes. Compared with the hypocaloric diet, similar weight loss was observed with the whole grain diet intervention, but differences in body composition (abdominal body fat/waist circumference) were observed in a few of these studies with whole grain hypocaloric diet intervention. On the basis of intervention studies, including whole grain in weight loss regimens involving caloric restriction does not appear to lead to greater weight loss, although it does improve overall diet quality and has added beneficial effects on metabolic risk factors. There is some limited evidence to suggest that incorporating whole grains into the diet may play a role in altering body composition8 or metabolism irrespective of loss of body weight9; however, the magnitude of the effect is small and the long-term relevance to overall (metabolic) health is unclear (Table 3).

Limitations This review highlights several limitations in the existing literature, which are briefly summarized below:  In both epidemiology and intervention studies, there is no consistent definition of whole grain foods and no way to validate the actual amount of whole grain consumed.  Self-reported dietary intake assessment methods have their own limitations, which are further compounded by the lack of standard definition of whole grain foods and variability in the estimation of whole grain content of foods.  The epidemiological literature is predominantly from the United States, mainly among white, adult cohorts.  Although the statistical approaches used in epidemiological studies attempt to separate the independent effects of whole grains on body weight from other known lifestyle and dietary behaviors, residual confounding by unknown or poorly measured factors remains a problem.  Estimates of BMI or body weight measures in epidemiology studies are sometimes based on self-reported r

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measures by study participants, which may lead to misclassification.  Intervention studies exhibited considerable heterogeneity with regard to study duration, types, and amounts of whole grain foods included in each intervention, comparison groups, and sample sizes.

SUMMARY Epidemiological evidence suggests consistently that higher whole grain intake is associated with improvements in measures of body weight. The evidence from intervention studies is limited and less consistent; currently the majority of intervention studies do not support the concept that whole grain intake contributes to weight loss, independent of hypocaloric diets. Interestingly, improvements in body composition may shape up as a potential effect of whole grain consumption. Because of heterogeneity in study design clear conclusions are difficult to draw. Future studies need to use a consistent definition of whole grain food and protocols. Furthermore, single grain–based study protocols, the impact of processing and grain structure, food matrix, and food format needs to be taken into consideration. REFERENCES 1. Choumenkovitch SF, McKeown NM, Tovar A, et al. Whole grain consumption is inversely associated with BMI Z-score in rural school-aged children. Public Health Nutr. 2013;16:212–218. 2. Lutsey PL, Jacobs DR Jr, Kori S, et al. Whole grain intake and its cross-sectional association with obesity, insulin resistance, inflammation, diabetes and subclinical CVD: The MESA Study. Br J Nutr. 2007;98:397–405. 3. Steffen LM, Jacobs DR Jr, Murtaugh MA, et al. Whole grain intake is associated with lower body mass and greater insulin sensitivity among adolescents. Am J Epidemiol. 2003;158:243–250. 4. Ye EQ, Chacko SA, Chou EL, et al. Greater whole-grain intake is associated with lower risk of type 2 diabetes, cardiovascular disease, and weight gain. J Nutr. 2012; 142:1304–1313. 5. Harland JI, Garton LE. Whole-grain intake as a marker of healthy body weight and adiposity. Public Health Nutr. 2008;11:554–563. 6. Koh-Banerjee P, Franz M, Sampson L, et al. Changes in whole-grain, bran, and cereal fiber consumption in relation to 8-y weight gain among men. Am J Clin Nutr. 2004;80: 1237–1245. 7. McKeown NM, Yoshida M, Shea MK, et al. Whole-grain intake and cereal fiber are associated with lower abdominal adiposity in older adults. J Nutr. 2009;139:1950–1955. 8. Kristensen M, Jensen MG, Riboldi G, et al. Wholegrain vs. refined wheat bread and pasta. Effect on postprandial glycemia, appetite, and subsequent ad libitum energy intake in young healthy adults. Appetite. 2010;54:163–169. 9. Katcher HI, Legro RS, Kunselman AR, et al. The effects of a whole grain-enriched hypocaloric diet on cardiovascular disease risk factors in men and women with metabolic syndrome. Am J Clin Nutr. 2008;87:79–90. 10. Bazzano LA, Song Y, Bubes V, et al. Dietary intake of whole and refined grain breakfast cereals and weight gain in men. Obes Res. 2005;13:1952–1960. 11. Behall KM, Scholfield DJ, Hallfrisch J. Whole-grain diets reduce blood pressure in mildly hypercholesterolemic men and women. J Am Diet Assoc. 2006;106:1445–1449. 12. Berz JP, Singer MR, Guo X, et al. Use of a DASH food group score to predict excess weight gain in adolescent girls in the National Growth and Health Study. Arch Pediatr Adolesc Med. 2011;165:540–546. r

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13. Bodinham CL, Hitchen KL, Youngman PJ, et al. Short-term effects of whole-grain wheat on appetite and food intake in healthy adults: a pilot study. Br J Nutr. 2011;106:327–330. 14. Brownlee IA, Moore C, Chatfield M, et al. Markers of cardiovascular risk are not changed by increased whole-grain intake: the WHOLEheart study, a randomised, controlled dietary intervention. Br J Nutr. 2010;104:125–134. 15. Bryson E, Dore C, Garrow JS. Wholemeal bread and satiety. J Hum Nutr. 1980;34:113–116. 16. Burton-Freeman BM, Keim NL. Glycemic index, cholecystokinin, satiety and disinhibition: is there an unappreciated paradox for overweight women? Int J Obes (Lond). 2008;32: 1647–1654. 17. Cheng G, Karaolis-Danckert N, Libuda L, et al. Relation of dietary glycemic index, glycemic load, and fiber and wholegrain intakes during puberty to the concurrent development of percent body fat and body mass index. Am J Epidemiol. 2009;169:667–677. 18. Egeberg R, Frederiksen K, Olsen A, et al. Intake of wholegrain products is associated with dietary, lifestyle, anthropometric and socio-economic factors in Denmark. Public Health Nutr. 2009;12:1519–1530. 19. Esmaillzadeh A, Mirmiran P, Azizi F. Whole-grain consumption and the metabolic syndrome: a favorable association in Tehranian adults. Eur J Clin Nutr. 2005;59:353–362. 20. Esmaillzadeh A, Mirmiran P, Azizi F. Whole-grain intake and the prevalence of hypertriglyceridemic waist phenotype in Tehranian adults. Am J Clin Nutr. 2005;81:55–63. 21. Fordyce-Baum MK, Langer LM, Mantero-Atienza E, et al. Use of an expanded-whole-wheat product in the reduction of body weight and serum lipids in obese females. Am J Clin Nutr. 1989;50:30–36. 22. Gaesser GA. Carbohydrate quantity and quality in relation to body mass index. J Am Diet Assoc. 2007;107:1768–1780. 23. Good CK, Holschuh N, Albertson AM, et al. Whole grain consumption and body mass index in adult women: an analysis of NHANES 1999-2000 and the USDA pyramid servings database. J Am Coll Nutr. 2008;27:80–87. 24. Heinonen MV, Karhunen LJ, Chabot ED, et al. Plasma ghrelin levels after two high-carbohydrate meals producing different insulin responses in patients with metabolic syndrome. Regul Pept. 2007;138:118–125. 25. Hlebowicz J, Wickenberg J, Fahlstrom R, et al. Effect of commercial breakfast fibre cereals compared with corn flakes on postprandial blood glucose, gastric emptying and satiety in healthy subjects: a randomized blinded crossover trial. Nutr J. 2007;6:22. 26. Hlebowicz J, Darwiche G, Bjorgell O, et al. Effect of muesli with 4 g oat beta-glucan on postprandial blood glucose, gastric emptying and satiety in healthy subjects: a randomized crossover trial. J Am Coll Nutr. 2008;27:470–475. 27. Holt SH, Miller JB. Particle size, satiety and the glycaemic response. Eur J Clin Nutr. 1994;48:496–502. 28. Isaksson H, Rakha A, Andersson R, et al. Rye kernel breakfast increases satiety in the afternoon — an effect of food structure. Nutr J. 2011;10:31. 29. Isaksson H, Sundberg B, Aman P, et al. Whole grain rye porridge breakfast improves satiety compared to refined wheat bread breakfast. Food Nutr Res. 2008;52. 30. Jimenez-Cruz A, Manuel Loustaunau-Lopez V, BacardiGascon M. The use of low glycemic and high satiety index food dishes in Mexico: a low cost approach to prevent and control obesity and diabetes. Nutr Hosp. 2006;21:353–356. 31. Jonnalagadda SS, Harnack L, Liu RH, et al. Putting the whole grain puzzle together: health benefits associated with whole grains—summary of American Society for Nutrition 2010 Satellite Symposium. J Nutr. 2011;141:1011S–1022S. 32. Keogh J, Atkinson F, Eisenhauer B, et al. Food intake, postprandial glucose, insulin and subjective satiety responses to three different bread-based test meals. Appetite. 2011;57: 707–710.

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52. Nilsson AC, Ostman EM, Holst JJ, et al. Including indigestible carbohydrates in the evening meal of healthy subjects improves glucose tolerance, lowers inflammatory markers, and increases satiety after a subsequent standardized breakfast. J Nutr. 2008;138:732–739. 53. O’Neil CE, Zanovec M, Cho SS, et al. Whole grain and fiber consumption are associated with lower body weight measures in US adults: National Health and Nutrition Examination Survey 1999-2004. Nutr Res. 2010;30:815–822. 54. Pai S, Ghugre PS, Udipi SA. Satiety from rice-based, wheatbased and rice-pulse combination preparations. Appetite. 2005;44:263–271. 55. Rave K, Roggen K, Dellweg S, et al. Improvement of insulin resistance after diet with a whole-grain based dietary product: results of a randomized, controlled cross-over study in obese subjects with elevated fasting blood glucose. Br J Nutr. 2007;98:929–936. 56. Rose N, Hosig K, Davy B, et al. Whole-grain intake is associated with body mass index in college students. J Nutr Educ Behav. 2007;39:90–94. 57. Rosen LA, Silva LO, Andersson UK, et al. Endosperm and whole grain rye breads are characterized by low post-prandial insulin response and a beneficial blood glucose profile. Nutr J. 2009;8:42. 58. Rosen LA, Ostman EM, Bjorck IM. Effects of cereal breakfasts on postprandial glucose, appetite regulation and voluntary energy intake at a subsequent standardized lunch; focusing on rye products. Nutr J. 2011;10:7. 59. Rosen LA, Ostman EM, Shewry PR, et al. Postprandial glycemia, insulinemia, and satiety responses in healthy subjects after whole grain rye bread made from different rye varieties. 1. J Agric Food Chem. 2011;59:12139–12148. 60. Saltzman E, Moriguti JC, Das SK, et al. Effects of a cereal rich in soluble fiber on body composition and dietary compliance during consumption of a hypocaloric diet. J Am Coll Nutr. 2001;20:50–57. 61. Schroeder N, Gallaher DD, Arndt EA, et al. Influence of whole grain barley, whole grain wheat, and refined rice-based foods on short-term satiety and energy intake. Appetite. 2009;53:363–369. 62. Slavin J. Why whole grains are protective: biological mechanisms. Proc Nutr Soc. 2003;62:129–134. 63. Thane CW, Stephen AM, Jebb SA. Whole grains and adiposity: little association among British adults. Eur J Clin Nutr. 2009;63:229–237. 64. Urooj A, Vinutha SR, Puttaraj SK, et al. Effect of barley incorporation in bread on its quality and glycemic responses in diabetics. Int J Food Sci Nutr. 1998;49:265–270. 65. van de Vijver LP, van den Bosch LM, van den Brandt PA, et al. Whole-grain consumption, dietary fibre intake and body mass index in the Netherlands cohort study. Eur J Clin Nutr. 2009;63:31–38. 66. Venn BJ, Perry T, Green TJ, et al. The effect of increasing consumption of pulses and wholegrains in obese people: a randomized controlled trial. J Am Coll Nutr. 2010;29:365–372. 67. Vuksan V, Jenkins AL, Dias AG, et al. Reduction in postprandial glucose excursion and prolongation of satiety: possible explanation of the long-term effects of whole grain Salba (Salvia Hispanica L.). Eur J Clin Nutr. 2010;64:436–438. 68. Wolfram T, Ismail-Beigi F. Efficacy of high-fiber diets in the management of type 2 diabetes mellitus. Endocr Pract. 2011;17:132–142. 69. Zanovec M, O’Neil CE, Cho SS, et al. Relationship between whole grain and fiber consumption and body weight measures among 6- to 18-year-olds. J Pediatr. 2010;157:578–583. 70. Zhang G, Pan A, Zong G, et al. Substituting white rice with brown rice for 16 weeks does not substantially affect metabolic risk factors in middle-aged Chinese men and women with diabetes or a high risk for diabetes. J Nutr. 2011;141: 1685–1690. 71. Sahyoun NR, Jacques PF, Zhang XL, et al. Whole-grain intake is inversely associated with the metabolic syndrome r

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and mortality in older adults. Am J Clin Nutr. 2006;83: 124–131. 72. Hur IY, Reicks M. Relationship between whole-grain intake, chronic disease risk indicators, and weight status among adolescents in the National Health and Nutrition Examination Survey, 1999-2004. J Acad Nutr Diet. 2012;112:46–55. 73. Pol K, Christensen R, Bartels EM, et al. Whole grain and body weight changes in apparently healthy adults: a systematic

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review and meta-analysis of randomized controlled studies. Am J Clin Nutr. 2013;98:872–884. 74. Ross AB, Bruce SJ, Blondel-Lubrano A, et al. A whole-grain cereal-rich diet increases plasma betaine, and tends to decrease total and LDL-cholesterol compared with a refined-grain diet in healthy subjects. Br J Nutr. 2011;105:1–12. 75. Karl JP, Saltzman E. The role of whole grains in body weight regulation. Adv Nutr. 2012;3:697–707.

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Can whole grain help in weight management?

Evidence from epidemiological studies suggests that higher whole grain intake is associated with improvements in body weight measures. Evidence from r...
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