Whole grain intake and glycaemic control in healthy subjects: A systematic review and meta-analysis of randomized controlled trials

Nutrients

Volumn 9, Issue 7, 2017, Pages

  Marventano, Stefano ^a   Vetrani, Claudia ^b   Vitale, Marilena ^b   Godos, Justyna ^c   Riccardi, Gabriele ^b   Grosso, Giuseppe ^c  

^a UNIVERSITY OF CATANIA   (Italy)

^b UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^c UNIVERSITY OF CATANIA   (Italy)

Author keywords

Glycemia; Healthy subjects; Insulin; Meta analysis; RTC; Whole grain

Indexed keywords

CARBOHYDRATE; GLUCOSE; INSULIN;

BIBLIOGRAPHIC DATABASE; DATA EXTRACTION; DIET RESTRICTION; FEEDING BEHAVIOR; FOOD INTAKE; GLYCEMIC CONTROL; HOMEOSTASIS MODEL ASSESSMENT; HUMAN; INSULIN SENSITIVITY; META ANALYSIS; OUTCOME ASSESSMENT; POSTPRANDIAL STATE; QUALITY CONTROL; RANDOMIZED CONTROLLED TRIAL (TOPIC); REFINED GRAIN; REVIEW; SENSITIVITY ANALYSIS; SYSTEMATIC REVIEW; WHOLE GRAIN; BLOOD; DIET; GLUCOSE BLOOD LEVEL; INSULIN RESISTANCE; METABOLISM;

BLOOD GLUCOSE; DIET; HUMANS; INSULIN; INSULIN RESISTANCE; POSTPRANDIAL PERIOD; RANDOMIZED CONTROLLED TRIALS AS TOPIC; WHOLE GRAINS;

EID: 85025818323     PISSN: None     EISSN: 20726643     Source Type: Journal    
DOI: 10.3390/nu9070769     Document Type: Review

References (69)

1. World Health Organization. World Health Statistics; World Health Organization: Geneva, Switzerland, 2009.
2. Slavin, J.L. Why wholegrains are protective: Biological mechanisms. Proc. Nutr. Soc. 2003, 62, 129–134. [CrossRef] [PubMed]
3. Seal, C.J.; Brownlee, I.A. Whole-grain foods and chronic disease: Evidence from epidemiological and intervention studies. Proc. Nutr. Soc. 2015, 74, 313–319. [CrossRef] [PubMed]
4. Costabile, A.; Klinder, A.; Fava, F.; Napolitano, A.; Fogliano, V.; Leonard, C.; Gibson, G.R.; Tuohy, K.M. Whole-grain wheat breakfast cereal has a prebiotic effect on the human gut microbiota: A double-blind, placebo-controlled, crossover study. Br. J. Nutr. 2008, 99, 110–120. [CrossRef] [PubMed]
5. Giacco, R.; Clemente, G.; Cipriano, D.; Luongo, D.; Viscovo, D.; Patti, L.; Di Marino, L.; Giacco, A.; Naviglio, D.; Bianchi, M.A.; et al. Effects of the regular consumption of wholemeal wheat foods on cardiovascular risk factors in healthy people. Nutr. Metab. Cardiovasc. Dis. NMCD 2010, 20, 186–194. [CrossRef] [PubMed]
6. Juntunen, K.S.; Laaksonen, D.E.; Poutanen, K.S.; Niskanen, L.K.; Mykkanen, H.M. High-fiber rye bread and insulin secretion and sensitivity in healthy postmenopausal women. Am. J. Clin. Nutr. 2003, 77, 385–391. [PubMed]
7. Kelly, S.A.; Summerbell, C.D.; Brynes, A.; Whittaker, V.; Frost, G. Wholegrain cereals for coronary heart disease. Cochrane Database Syst. Rev. 2007, 18, CD005051.
8. Aune, D.; Norat, T.; Romundstad, P.; Vatten, L.J. Whole grain and refined grain consumption and the risk of type 2 diabetes: A systematic review and dose-response meta-analysis of cohort studies. Eur. J. Epidemiol. 2013, 28, 845–858. [CrossRef] [PubMed]
9. Ye, E.Q.; Chacko, S.A.; Chou, E.L.; Kugizaki, M.; Liu, S. Greater whole-grain intake is associated with lower risk of type 2 diabetes, cardiovascular disease, and weight gain. J. Nutr. 2012, 142, 1304–1313. [CrossRef] [PubMed]
10. Aune, D.; Chan, D.S.; Lau, R.; Vieira, R.; Greenwood, D.C.; Kampman, E.; Norat, T. Dietary fibre, whole grains, and risk of colorectal cancer: Systematic review and dose-response meta-analysis of prospective studies. BMJ 2011, 343, d6617. [CrossRef] [PubMed]
11. Fardet, A. New hypotheses for the health-protective mechanisms of whole-grain cereals: What is beyond fibre? Nutr. Res. Rev. 2010, 23, 65–134. [CrossRef] [PubMed]
12. Nettleton, J.A.; McKeown, N.M.; Kanoni, S.; Lemaitre, R.N.; Hivert, M.F.; Ngwa, J.; van Rooij, F.J.; Sonestedt, E.; Wojczynski, M.K.; Ye, Z.; et al. 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. Diabetes Care 2010, 33, 2684–2691. [CrossRef] [PubMed]
13. Wells, G.A.; Shea, B.; O’Connell, D.; Peterson, J.; Welch, V.; Losos, M.; Tugwell, P. The Newcastle-Ottawa Scale (nos) for Assessing the Quality of Nonrandomised Studies in Meta-Analyses; Ottawa Health Research Institute: Ottawa, ON, Canada, 1999.
14. The Journal of the American Medical Association. Author Instructions: Systeme International (si) Conversion Factors for Selected Laboratory Components; The Journal of the American Medical Association: Berlin, Germany, 2001.
15. Higgins, J.P.T.; Green, S. Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0 (Updated March 2011); The Cochrane Collaboration: London, UK, 2011.
16. Higgins, J.P.; Thompson, S.G.; Deeks, J.J.; Altman, D.G. Measuring inconsistency in meta-analyses. BMJ 2003, 327, 557–560. [CrossRef] [PubMed]
17. Johansson, D.P.; Lee, I.; Riserus, U.; Langton, M.; Landberg, R. Effects of unfermented and fermented whole grain rye crisp breads served as part of a standardized breakfast, on appetite and postprandial glucose and insulin responses: A randomized cross-over trial. PLoS ONE 2015, 10, e0122241. [CrossRef] [PubMed]
18. Alminger, M.; Eklund-Jonsson, C. Whole-grain cereal products based on a high-fibre barley or oat genotype lower post-prandial glucose and insulin responses in healthy humans. Eur. J. Nutr. 2008, 47, 294–300. [CrossRef] [PubMed]
19. Hlebowicz, J.; Wickenberg, J.; Fahlstrom, R.; Bjorgell, O.; Almer, L.O.; Darwiche, G. 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. [CrossRef] [PubMed]
20. Nilsson, A.C.; Ostman, E.M.; Granfeldt, Y.; Bjorck, I.M. Effect of cereal test breakfasts differing in glycemic index and content of indigestible carbohydrates on daylong glucose tolerance in healthy subjects. Am. J. Clin. Nutr. 2008, 87, 645–654. [PubMed]
21. Rosen, L.A.; Silva, L.O.; Andersson, U.K.; Holm, C.; Ostman, E.M.; Bjorck, I.M. 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. [CrossRef] [PubMed]
22. Rosen, L.A.; Ostman, E.M.; Bjorck, I.M. 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. [CrossRef] [PubMed]
23. Andersson, A.; Tengblad, S.; Karlstrom, B.; Kamal-Eldin, A.; Landberg, R.; Basu, S.; Aman, P.; Vessby, B. Whole-grain foods do not affect insulin sensitivity or markers of lipid peroxidation and inflammation in healthy, moderately overweight subjects. J. Nutr. 2007, 137, 1401–1407. [PubMed]
24. Hlebowicz, J.; Jonsson, J.M.; Lindstedt, S.; Bjorgell, O.; Darwich, G.; Almer, L.O. Effect of commercial rye whole-meal bread on postprandial blood glucose and gastric emptying in healthy subjects. Nutr. J. 2009, 8, 26. [CrossRef] [PubMed]
25. Leinonen, K.; Liukkonen, K.; Poutanen, K.; Uusitupa, M.; Mykkanen, H. Rye bread decreases postprandial insulin response but does not alter glucose response in healthy finnish subjects. Eur. J. Clin. Nutr. 1999, 53, 262–267. [CrossRef] [PubMed]
26. Juntunen, K.S.; Niskanen, L.K.; Liukkonen, K.H.; Poutanen, K.S.; Holst, J.J.; Mykkanen, H.M. Postprandial glucose, insulin, and incretin responses to grain products in healthy subjects. Am. J. Clin. Nutr. 2002, 75, 254–262. [PubMed]
27. Juntunen, K.S.; Laaksonen, D.E.; Autio, K.; Niskanen, L.K.; Holst, J.J.; Savolainen, K.E.; Liukkonen, K.H.; Poutanen, K.S.; Mykkanen, H.M. Structural differences between rye and wheat breads but not total fiber content may explain the lower postprandial insulin response to rye bread. Am. J. Clin. Nutr. 2003, 78, 957–964. [PubMed]
28. Lappi, J.; Aura, A.M.; Katina, K.; Nordlund, E.; Kolehmainen, M.; Mykkanen, H.; Poutanen, K. Comparison of postprandial phenolic acid excretions and glucose responses after ingestion of breads with bioprocessed or native rye bran. Food Funct. 2013, 4, 972–981. [CrossRef] [PubMed]
29. Moazzami, A.A.; Shrestha, A.; Morrison, D.A.; Poutanen, K.; Mykkanen, H. Metabolomics reveals differences in postprandial responses to breads and fasting metabolic characteristics associated with postprandial insulin demand in postmenopausal women. J. Nutr. 2014, 144, 807–814. [CrossRef] [PubMed]
30. Mofidi, A.; Ferraro, Z.M.; Stewart, K.A.; Tulk, H.M.; Robinson, L.E.; Duncan, A.M.; Graham, T.E. The acute impact of ingestion of sourdough and whole-grain breads on blood glucose, insulin, and incretins in overweight and obese men. J. Nutr. Metab. 2012, 2012, 184710. [CrossRef] [PubMed]
31. Luhovyy, B.L.; Mollard, R.C.; Yurchenko, S.; Nunez, M.F.; Berengut, S.; Liu, T.T.; Smith, C.E.; Pelkman, C.L.; Anderson, G.H. The effects of whole grain high-amylose maize flour as a source of resistant starch on blood glucose, satiety, and food intake in young men. J. Food Sci. 2014, 79, H2550–H2556. [CrossRef] [PubMed]
32. MacKay, K.A.; Tucker, A.J.; Duncan, A.M.; Graham, T.E.; Robinson, L.E. Whole grain wheat sourdough bread does not affect plasminogen activator inhibitor-1 in adults with normal or impaired carbohydrate metabolism. Nutr. Metab. Cardiovasc. Dis. NMCD 2012, 22, 704–711. [CrossRef] [PubMed]
33. Najjar, A.M.; Parsons, P.M.; Duncan, A.M.; Robinson, L.E.; Yada, R.Y.; Graham, T.E. The acute impact of ingestion of breads of varying composition on blood glucose, insulin and incretins following first and second meals. Br. J. Nutr. 2009, 101, 391–398. [CrossRef] [PubMed]
34. Vuksan, V.; Jenkins, A.L.; Dias, A.G.; Lee, A.S.; Jovanovski, E.; Rogovik, A.L.; Hanna, A. 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. [CrossRef] [PubMed]
35. Brownlee, I.A.; Moore, C.; Chatfield, M.; Richardson, D.P.; Ashby, P.; Kuznesof, S.A.; Jebb, S.A.; Seal, C.J. 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. [CrossRef] [PubMed]
36. Ampatzoglou, A.; Atwal, K.K.; Maidens, C.M.; Williams, C.L.; Ross, A.B.; Thielecke, F.; Jonnalagadda, S.S.; Kennedy, O.B.; Yaqoob, P. Increased whole grain consumption does not affect blood biochemistry, body composition, or gut microbiology in healthy, low-habitual whole grain consumers. J. Nutr. 2015, 145, 215–221. [CrossRef] [PubMed]
37. Tighe, P.; Duthie, G.; Vaughan, N.; Brittenden, J.; Simpson, W.G.; Duthie, S.; Mutch, W.; Wahle, K.; Horgan, G.; Thies, F. Effect of increased consumption of whole-grain foods on blood pressure and other cardiovascular risk markers in healthy middle-aged persons: A randomized controlled trial. Am. J. Clin. Nutr. 2010, 92, 733–740. [CrossRef] [PubMed]
38. Ampatzoglou, A.; Williams, C.L.; Atwal, K.K.; Maidens, C.M.; Ross, A.B.; Thielecke, F.; Jonnalagadda, S.S.; Kennedy, O.B.; Yaqoob, P. Effects of increased wholegrain consumption on immune and inflammatory markers in healthy low habitual wholegrain consumers. Eur. J. Nutr. 2016, 55, 183–195. [CrossRef] [PubMed]
39. McIntosh, G.H.; Noakes, M.; Royle, P.J.; Foster, P.R. Whole-grain rye and wheat foods and markers of bowel health in overweight middle-aged men. Am. J. Clin. Nutr. 2003, 77, 967–974. [PubMed]
40. Keogh, J.; Atkinson, F.; Eisenhauer, B.; Inamdar, A.; Brand-Miller, J. Food intake, postprandial glucose, insulin and subjective satiety responses to three different bread-based test meals. Appetite 2011, 57, 707–710. [CrossRef] [PubMed]
41. Stefoska-Needham, A.; Beck, E.J.; Johnson, S.K.; Chu, J.; Tapsell, L.C. Flaked sorghum biscuits increase postprandial glp-1 and gip levels and extend subjective satiety in healthy subjects. Mol. Nutr. Food Res. 2016, 60, 1118–1128. [CrossRef] [PubMed]
42. Kristensen, M.; Toubro, S.; Jensen, M.G.; Ross, A.B.; Riboldi, G.; Petronio, M.; Bugel, S.; Tetens, I.; Astrup, A. Whole grain compared with refined wheat decreases the percentage of body fat following a 12-week, energy-restricted dietary intervention in postmenopausal women. J. Nutr. 2012, 142, 710–716. [CrossRef] [PubMed]
43. Bakhoj, S.; Flint, A.; Holst, J.J.; Tetens, I. Lower glucose-dependent insulinotropic polypeptide (gip) response but similar glucagon-like peptide 1 (glp-1), glycaemic, and insulinaemic response to ancient wheat compared to modern wheat depends on processing. Eur. J. Clin. Nutr. 2003, 57, 1254–1261. [CrossRef] [PubMed]
44. Kristensen, M.; Jensen, M.G.; Riboldi, G.; Petronio, M.; Bugel, S.; Toubro, S.; Tetens, I.; Astrup, A. 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. [CrossRef] [PubMed]
45. Vitaglione, P.; Mennella, I.; Ferracane, R.; Rivellese, A.A.; Giacco, R.; Ercolini, D.; Gibbons, S.M.; La Storia, A.; Gilbert, J.A.; Jonnalagadda, S.; et al. Whole-grain wheat consumption reduces inflammation in a randomized controlled trial on overweight and obese subjects with unhealthy dietary and lifestyle behaviors: Role of polyphenols bound to cereal dietary fiber. Am. J. Clin. Nutr. 2015, 101, 251–261. [CrossRef] [PubMed]
46. Casiraghi, M.C.; Garsetti, M.; Testolin, G.; Brighenti, F. Post-prandial responses to cereal products enriched with barley beta-glucan. J. Am. Coll. Nutr. 2006, 25, 313–320. [CrossRef] [PubMed]
47. Saltzman, E.; Das, S.K.; Lichtenstein, A.H.; Dallal, G.E.; Corrales, A.; Schaefer, E.J.; Greenberg, A.S.; Roberts, S.B. An oat-containing hypocaloric diet reduces systolic blood pressure and improves lipid profile beyond effects of weight loss in men and women. J. Nutr. 2001, 131, 1465–1470. [PubMed]
48. Pereira, M.A.; Jacobs, D.R., Jr.; Pins, J.J.; Raatz, S.K.; Gross, M.D.; Slavin, J.L.; Seaquist, E.R. Effect of whole grains on insulin sensitivity in overweight hyperinsulinemic adults. Am. J. Clin. Nutr. 2002, 75, 848–855. [PubMed]
49. Poquette, N.M.; Gu, X.; Lee, S.O. Grain sorghum muffin reduces glucose and insulin responses in men. Food Funct. 2014, 5, 894–899. [CrossRef] [PubMed]
50. Rave, K.; Roggen, K.; Dellweg, S.; Heise, T.; Tom Dieck, H. 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. [CrossRef] [PubMed]
51. Li, J.; Kaneko, T.; Qin, L.Q.; Wang, J.; Wang, Y. Effects of barley intake on glucose tolerance, lipid metabolism, and bowel function in women. Nutrition 2003, 19, 926–929. [CrossRef]
52. Zafar, T.A.; Al-Hassawi, F.; Al-Khulaifi, F.; Al-Rayyes, G.; Waslien, C.; Huffman, F.G. Organoleptic and glycemic properties of chickpea-wheat composite breads. J. Food Sci. Technol. 2015, 52, 2256–2263. [CrossRef] [PubMed]
53. Soong, Y.Y.; Quek, R.Y.; Henry, C.J. Glycemic potency of muffins made with wheat, rice, corn, oat and barley flours: A comparative study between in vivo and in vitro. Eur. J. Nutr. 2015, 54, 1281–1285. [CrossRef] [PubMed]
54. Gonzalez-Anton, C.; Rico, M.C.; Sanchez-Rodriguez, E.; Ruiz-Lopez, M.D.; Gil, A.; Mesa, M.D. Glycemic responses, appetite ratings and gastrointestinal hormone responses of most common breads consumed in spain. A randomized control trial in healthy humans. Nutrients 2015, 7, 4033–4053. [CrossRef] [PubMed]
55. Ross, A.B.; Bruce, S.J.; Blondel-Lubrano, A.; Oguey-Araymon, S.; Beaumont, M.; Bourgeois, A.; Nielsen-Moennoz, C.; Vigo, M.; Fay, L.B.; Kochhar, S.; 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, 1492–1502. [CrossRef] [PubMed]
56. Granfeldt, Y.; Wu, X.; Bjorck, I. Determination of glycaemic index; some methodological aspects related to the analysis of carbohydrate load and characteristics of the previous evening meal. Eur. J. Clin. Nutr. 2006, 60, 104–112. [CrossRef] [PubMed]
57. Ardisson Korat, A.V.; Willett, W.C.; Hu, F.B. Diet, lifestyle, and genetic risk factors for type 2 diabetes: A review from the nurses’ health study, nurses’ health study 2, and health professionals’ follow-up study. Curr. Nutr. Rep. 2014, 3, 345–354. [CrossRef] [PubMed]
58. Sahyoun, N.R.; Jacques, P.F.; Zhang, X.L.; Juan, W.; McKeown, N.N. Whole-grain intake is inversely associated with the metabolic syndrome and mortality in older adults. Am. J. Clin. Nutr. 2006, 83, 124–131. [PubMed]
59. Aune, D.; Keum, N.; Giovannucci, E.; Fadnes, L.T.; Boffetta, P.; Greenwood, D.C.; Tonstad, S.; Vatten, L.J.; Riboli, E.; Norat, T. Whole grain consumption and risk of cardiovascular disease, cancer, and all cause and cause specific mortality: Systematic review and dose-response meta-analysis of prospective studies. BMJ 2016, 353, i2716. [CrossRef] [PubMed]
60. Willett, W.; Manson, J.; Liu, S. Glycemic index, glycemic load, and risk of type 2 diabetes. Am. J. Clin. Nutr. 2002, 76, 274S–280S. [PubMed]
61. Lopez-Alarcon, M.; Perichart-Perera, O.; Flores-Huerta, S.; Inda-Icaza, P.; Rodriguez-Cruz, M.; Armenta-Alvarez, A.; Bram-Falcon, M.T.; Mayorga-Ochoa, M. Excessive refined carbohydrates and scarce micronutrients intakes increase inflammatory mediators and insulin resistance in prepubertal and pubertal obese children independently of obesity. Mediat. Inflamm. 2014, 2014, 849031. [CrossRef] [PubMed]
62. Liese, A.D.; Roach, A.K.; Sparks, K.C.; Marquart, L.; D’Agostino, R.B., Jr.; Mayer-Davis, E.J. Whole-grain intake and insulin sensitivity: The insulin resistance atherosclerosis study. Am. J. Clin. Nutr. 2003, 78, 965–971. [PubMed]
63. Meynier, A.; Goux, A.; Atkinson, F.; Brack, O.; Vinoy, S. Postprandial glycaemic response: How is it influenced by characteristics of cereal products? Br. J. Nutr. 2015, 113, 1931–1939. [CrossRef] [PubMed]
64. Steffen, L.M.; Jacobs, D.R., Jr.; Murtaugh, M.A.; Moran, A.; Steinberger, J.; Hong, C.P.; Sinaiko, A.R. Whole grain intake is associated with lower body mass and greater insulin sensitivity among adolescents. Am. J. Epidemiol. 2003, 158, 243–250. [CrossRef] [PubMed]
65. Canfora, E.E.; Jocken, J.W.; Blaak, E.E. Short-chain fatty acids in control of body weight and insulin sensitivity. Nat. Rev. Endocrinol. 2015, 11, 577–591. [CrossRef] [PubMed]
66. Robertson, R.P. Chronic oxidative stress as a central mechanism for glucose toxicity in pancreatic islet beta cells in diabetes. J. Biol. Chem. 2004, 8, 42351–42354. [CrossRef] [PubMed]
67. Ohnishi, M.; Matuo, T.; Tsuno, T.; Hosoda, A.; Nomura, E.; Taniguchi, H.; Sasaki, H.; Morishita, H. Antioxidant activity and hypoglycemic effect of ferulic acid in stz-induced diabetic mice and kk-ay mice. BioFactors 2004, 21, 315–319. [CrossRef] [PubMed]
68. Marventano, S.; Kolacz, P.; Castellano, S.; Galvano, F.; Buscemi, S.; Mistretta, A.; Grosso, G. A review of recent evidence in human studies of n-3 and n-6 pufa intake on cardiovascular disease, cancer, and depressive disorders: Does the ratio really matter? Int. J. Food Sci. Nutr. 2015, 66, 611–622. [CrossRef] [PubMed]
69. Food and Agriculture Organization of the United Nations (FAOSTAT). Cereal Production; Food and Agriculture Organization of the United Nations: Rome, Italy, 2016.