Impact of Short Term Consumption of Diets High in Either Non-Starch Polysaccharides or Resistant Starch in Comparison with Moderate Weight Loss on Indices of Insulin Sensitivity in Subjects with Metabolic Syndrome
This study investigated if additional non-starch polysaccharide (NSP) or resistant starch (RS), above that currently recommended, leads to better improvement in insulin sensitivity (IS) than observed with modest weight loss (WL). Obese male volunteers ( n = 14) were given an energy-maintenance (M) diet containing 27 g NSP and 5 g RS daily for one week. They then received, in a cross-over design, energy-maintenance intakes of either an NSP-enriched diet (42 g NSP, 2.5 g RS) or an RS-enriched diet (16 g NSP, 25 g RS), each for three weeks. Finally, a high protein (30% calories) WL diet was provided at 8 MJ/day for three weeks. During each dietary intervention, endogenous glucose production (EGP) and IS were assessed. Fasting glycaemia was unaltered by diet, but plasma insulin and C-peptide both decreased with the WL diet ( p < 0.001), as did EGP (？11%, p = 0.006). Homeostatis model assessment of insulin resistance improved following both WL ( p < 0.001) and RS ( p < 0.05) diets. Peripheral tissue IS improved only with WL (57%–83%, p < 0.005). Inclusion of additional RS or NSP above amounts currently recommended resulted in little or no improvement in glycaemic control, whereas moderate WL (approximately 3 kg fat) improved IS.
References
[1]
Willett, W.C.; Dietz, W.H.; Colditz, G.A. Guidelines for healthy weight. N. Engl. J. Med. 1999, 341, 427–434, doi:10.1056/NEJM199908053410607.
Counterweight Project Team. Influence of body mass index on prescribing costs and potential cost savings of a weight management programme in primary care. J. Health Serv. Res. Policy 2008, 13, 158–166, doi:10.1258/jhsrp.2008.007140.
[4]
Nuttall, F.Q.; Gannon, M.C.; Saeed, A.; Jordan, K.; Hoover, H. The metabolic response of subjects with type 2 diabetes to a high-protein, weight-maintenance diet. J. Clin. Endocrinol. Metab. 2003, 88, 3577–3583, doi:10.1210/jc.2003-030419.
[5]
Sullivan, V.K. Prevention and treatment of the metabolic syndrome with lifestyle intervention: Where do we start? J. Am. Diet. Assoc. 2006, 106, 668–671, doi:10.1016/j.jada.2006.03.027.
[6]
Fappa, E.; Yannakoulia, M.; Pitsavos, C.; Skoumas, I.; Valourdou, S.; Stefanadis, C. Lifestyle intervention in the management of metabolic syndrome: Could we improve adherence issues? Nutrition 2008, 24, 286–291, doi:10.1016/j.nut.2007.11.008.
[7]
Muscelli, E.; Camastra, S.; Catalano, C.; Galvan, A.Q.; Ciociaro, D.; Baldi, S.; Ferrannini, E. Metabolic and cardiovascular assessment in moderate obesity: Effect of weight loss. J. Clin. Endocrinol. Metab. 1997, 82, 2937–2943, doi:10.1210/jc.82.9.2937.
[8]
Goodpaster, B.H.; Kelley, D.E.; Wing, R.R.; Meier, A.; Thaete, F.L. Effects of weight loss on regional fat distribution and insulin sensitivity in obesity. Diabetes 1999, 48, 839–847, doi:10.2337/diabetes.48.4.839.
[9]
Skov, A.R.; Toubro, S.; Ronn, B.; Holm, L.; Astrup, A. Randomized trial on protein vs. carbohydrate in ad libitum fat reduced diet for the treatment of obesity. Int. J. Obes. Relat. Metab. Disord. 1999, 23, 528–536.
[10]
Weigle, D.S.; Breen, P.A.; Matthys, C.C.; Callahan, H.S.; Meeuws, K.E.; Burden, V.R.; Purnell, J.Q. A high-protein diet induces sustained reductions in appetite, ad libitum caloric intake, and body weight despite compensatory changes in diurnal plasma leptin and ghrelin concentrations. Am. J. Clin. Nutr. 2005, 82, 41–48.
[11]
Johnstone, A.M.; Horgan, G.W.; Murison, S.D.; Bremner, D.M.; Lobley, G.E. Effects of a high-protein ketogenic diet on hunger, appetite, and weight loss in obese men feeding ad libitum. Am. J. Clin. Nutr. 2008, 87, 44–55.
[12]
Wolever, T.M.; Gibbs, A.L.; Mehling, C.; Chiasson, J.L.; Connelly, P.W.; Josse, R.G.; Leiter, L.A.; Maheux, P.; Rabasa-Lhoret, R.; Rodger, N.W.; Ryan, E.A. The Canadian Trial of Carbohydrates in Diabetes (CCD), a 1-y controlled trial of low-glycemic-index dietary carbohydrate in type 2 diabetes: No effect on glycated hemoglobin but reduction in C-reactive protein. Am. J. Clin. Nutr. 2008, 87, 114–125.
[13]
Robertson, M.D. Metabolic cross talk between the colon and the periphery: Implications for insulin sensitivity. Proc. Nutr. Soc. 2007, 66, 351–361, doi:10.1017/S0029665107005617.
[14]
Wursch, P.; Pi-Sunyer, F.X. The role of viscous soluble fiber in the metabolic control of diabetes. A review with special emphasis on cereals rich in beta-glucan. Diabetes Care 1997, 1774–1780.
[15]
Morita, T.; Kasaoka, S.; Hase, K.; Kiriyama, S. Psyllium shifts the fermentation site of high-amylose cornstarch toward the distal colon and increases fecal butyrate concentration in rats. J. Nutr. 1999, 129, 2081–2087.
[16]
Giacco, R.; Parillo, M.; Rivellese, A.A.; Lasorella, G.; Giacco, A.; D’Episcopo, L.; Riccardi, G. Long-term dietary treatment with increased amounts of fiber-rich low-glycemic index natural foods improves blood glucose control and reduces the number of hypoglycemic events in type 1 diabetic patients. Diabetes Care 2000, 23, 1461–1466, doi:10.2337/diacare.23.10.1461.
Robertson, M.D.; Bickerton, A.S.; Dennis, A.L.; Vidal, H.; Frayn, K.N. Insulin-sensitizing effects of dietary resistant starch and effects on skeletal muscle and adipose tissue metabolism. Am. J. Clin. Nutr. 2005, 82, 559–567.
[19]
Krebs, M.; Brehm, A.; Krssak, M.; Anderwald, C.; Bernroider, E.; Nowotny, P.; Roth, E.; Chandramouli, V.; Landau, B.R.; Waldhausl, W.; Roden, M. Direct and indirect effects of amino acids on hepatic glucose metabolism in humans. Diabetologia 2003, 46, 917–925, doi:10.1007/s00125-003-1129-1.
[20]
Chevalier, S.; Burgess, S.C.; Malloy, C.R.; Gougeon, R.; Marliss, E.B.; Morais, J.A. The greater contribution of gluconeogenesis to glucose production in obesity is related to increased whole-body protein catabolism. Diabetes 2006, 55, 675–681, doi:10.2337/diabetes.55.03.06.db05-1117.
[21]
Veldhorst, M.A.; Westerterp-Plantenga, M.S.; Westerterp, K.R. Gluconeogenesis and energy expenditure after a high-protein, carbohydrate-free diet. Am. J. Clin. Nutr. 2009, 90, 519–526, doi:10.3945/ajcn.2009.27834.
[22]
Schutz, Y. Protein turnover, ureagenesis and gluconeogenesis. Int. J. Vitam. Nutr Res. 2011, 81, 101–107, doi:10.1024/0300-9831/a000064.
[23]
Walker, A.W.; Ince, J.; Duncan, S.H.; Webster, L.M.; Holtrop, G.; Ze, X.; Brown, D.; Stares, M.D.; Scott, P.; Bergerat, A.; et al. Dominant and diet-responsive groups of bacteria within the human colonic microbiota. ISME. J. 2011, 5, 220–230, doi:10.1038/ismej.2010.118.
[24]
McIntosh, F.M.; Maison, N.; Holtrop, G.; Young, P.; Stevens, V.J.; Ince, J.; Johnstone, A.M.; Lobley, G.E.; Flint, H.J.; Louis, P. Phylogenetic distribution of genes encoding beta-glucuronidase activity in human colonic bacteria and the impact of diet on faecal glycosidase activities. Environ. Microbiol. 2012, 14, 1876–1887, doi:10.1111/j.1462-2920.2012.02711.x.
[25]
O’Sullivan, K.R.; Cho, S.S. Fibre recommendations throughout the world. Int. J. Food Sci. Nutr. 1998, 49, S13–S21.
[26]
Johnstone, A.M.; Lobley, G.E.; Horgan, G.W.; Bremner, D.M.; Fyfe, C.L.; Morrice, P.C.; Duthie, G.G. Effects of a high-protein, low-carbohydrate v. high-protein, moderate-carbohydrate weight-loss diet on antioxidant status, endothelial markers and plasma indices of the cardiometabolic profile. Br. J. Nutr. 2011, 106, 282–291, doi:10.1017/S0007114511000092.
[27]
Calder, A.G.; Smith, A. Stable isotope ratio analysis of leucine and ketoisocaproic acid in blood plasma by gas chromatography/mass spectrometry. Use of tertiary butyldimethylsilyl derivatives. Rapid Commum. Mass Spectrom. 1988, 2, 14–16, doi:10.1002/rcm.1290020105.
[28]
Calder, A.G.; Garden, K.E.; Anderson, S.E.; Lobley, G.E. Quantitation of blood and plasma amino acids using isotope dilution electron impact gas chromatography/mass spectrometry with U-(13)C amino acids as internal standards. Rapid Commum. Mass Spectrom. 1999, 13, 2080–2083.
[29]
Wilson, F.A.; van den Borne, J.J.; Calder, A.G.; O'Kennedy, N.; Holtrop, G.; Rees, W.D.; Lobley, G.E. Tissue methionine cycle activity and homocysteine metabolism in female rats: Impact of dietary methionine and folate plus choline. Am. J. Physiol Endocrinol. Metab. 2009, 296, E702–E713, doi:10.1152/ajpendo.90670.2008.
[30]
Patterson, B.W.; Carraro, F.; Wolfe, R.R. Measurement of 15N enrichment in multiple amino acids and urea in a single analysis by gas chromatography/mass spectrometry. Biol. Mass Spectrom. 1993, 22, 518–523, doi:10.1002/bms.1200220905.
[31]
Levy, J.C.; Matthews, D.R.; Hermans, M.P. Correct homeostasis model assessment (HOMA) evaluation uses the computer program. Diabetes Care 1998, 21, 2191–2192, doi:10.2337/diacare.21.12.2191.
[32]
The Oxford Centre for Diabetes. Endocrinology & Metabolism, Diabetes Trial Unit. HOMA Calculator. Available online: http://www.dtu.ox.ac.uk/homacalculator/index.php (accessed on 16 July 2012).
[33]
Matsuda, M.; Defronzo, R.A. Insulin sensitivity indices obtained from oral glucose tolerance testing: comparison with the euglycemic insulin clamp. Diabetes Care 1999, 22, 1462–1470, doi:10.2337/diacare.22.9.1462.
[34]
Wolever, T.M.; Jenkins, D.J.; Jenkins, A.L.; Josse, R.G. The glycemic index: Methodology and clinical implications. Am. J. Clin. Nutr. 1991, 54, 846–854.
[35]
Basu, R.; Di Camillo, B.; Toffolo, G.; Basu, A.; Shah, P.; Vella, A.; Rizza, R.; Cobelli, C. Use of a novel triple-tracer approach to assess postprandial glucose metabolism. Am. J. Physiol Endocrinol. Metab. 2003, 284, E55–E69.
[36]
Bluck, L.J.; Clapperton, A.T.; Coward, W.A. 13C- and 2H-labelled glucose compared for minimal model estimates of glucose metabolism in man. Clin. Sci. (Lond.) 2005, 109, 513–521, doi:10.1042/CS20050155.
[37]
Vicini, P.; Zachwieja, J.J.; Yarasheski, K.E.; Bier, D.M.; Caumo, A.; Cobelli, C. Glucose production during an IVGTT by deconvolution: validation with the tracer-to-tracee clamp technique. Am. J. Physiol. 1999, 276, E285–E294.
[38]
Shipley, R.A.; Clark, R.E. Tracer Methods for in Vivo Kinetics. Theory and Applications; Academic Press: London, UK, 1972.
[39]
Ferrannini, E.; Smith, J.D.; Cobelli, C.; Toffolo, G.; Pilo, A.; Defronzo, R.A. Effect of insulin on the distribution and disposition of glucose in man. J. Clin. Invest. 1985, 76, 357–364, doi:10.1172/JCI111969.
[40]
Toffolo, G.; Basu, R.; Dalla, M.C.; Rizza, R.; Cobelli, C. Assessment of postprandial glucose metabolism: Conventional dual- vs. triple-tracer method. Am. J. Physiol Endocrinol. Metab. 2006, 291, E800–E806, doi:10.1152/ajpendo.00461.2005.
[41]
Vicini, P.; Caumo, A.; Cobelli, C. The hot IVGTT two-compartment minimal model: Indexes of glucose effectiveness and insulin sensitivity. Am. J. Physiol. 1997, 273, E1024–E1032.
[42]
The R Project for Statistical Computing. Available online: http://www.r-project.org/ (accessed on 6 November 2012).
[43]
Statistical Libraries. GLIM4 Macro Libraries. Available online: http://www.commanster.eu/rcode.html (accessed on 6 November 2012).
[44]
Anderson, J.W.; Baird, P.; Davis, R.H., Jr.; Ferreri, S.; Knudtson, M.; Koraym, A.; Waters, V.; Williams, C.L. Health benefits of dietary fiber. Nutr. Rev. 2009, 67, 188–205, doi:10.1111/j.1753-4887.2009.00189.x.
[45]
Felig, P. Amino acid metabolism in man. Annu. Rev. Biochem. 1975, 44, 933–955, doi:10.1146/annurev.bi.44.070175.004441.
[46]
Basu, R.; Schwenk, W.F.; Rizza, R.A. Both fasting glucose production and disappearance are abnormal in people with “mild” and “severe” type 2 diabetes. Am. J. Physiol Endocrinol. Metab. 2004, 28, E55–E62, doi:10.1152/ajpendo.00549.2003.
[47]
Gastaldelli, A.; Toschi, E.; Pettiti, M.; Frascerra, S.; Quinones-Galvan, A.; Sironi, A.M.; Natali, A.; Ferrannini, E. Effect of physiological hyperinsulinemia on gluconeogenesis in nondiabetic subjects and in type 2 diabetic patients. Diabetes 2001, 50, 1807–1812, doi:10.2337/diabetes.50.8.1807.
[48]
Boden, G.; Cheung, P.; Stein, T.P.; Kresge, K.; Mozzoli, M. FFA cause hepatic insulin resistance by inhibiting insulin suppression of glycogenolysis. Am. J. Physiol. Endocrinol. Metab. 2002, 283, E12–E19.
[49]
Robertson, M.D.; Wright, J.W.; Loizon, E.; Debard, C.; Vidal, H.; Shojaee-Moradie, F.; Russell-Jones, D.; Umpleby, A.M. Insulin-sensitizing effects on muscle and adipose tissue after dietary fiber intake in men and women with metabolic syndrome. J. Clin. Endocrinol. Metab. 2012, 97, 3326–3332, doi:10.1210/jc.2012-1513.
[50]
Weickert, M.O.; Roden, M.; Isken, F.; Hoffmann, D.; Nowotny, P.; Osterhoff, M.; Blaut, M.; Alpert, C.; Gogebakan, O.; Bumke-Vogt, C.; et al. Effects of supplemented isoenergetic diets differing in cereal fiber and protein content on insulin sensitivity in overweight humans. Am. J. Clin. Nutr. 2011, 94, 459–471, doi:10.3945/ajcn.110.004374.
[51]
Viljanen, A.P.; Iozzo, P.; Borra, R.; Kankaanpaa, M.; Karmi, A.; Lautamaki, R.; Jarvisalo, M.; Parkkola, R.; Ronnemaa, T.; Guiducci, L.; et al. Effect of weight loss on liver free fatty acid uptake and hepatic insulin resistance. J. Clin. Endocrinol. Metab. 2009, 94, 50–55.
[52]
Wahren, J.; Efendic, S.; Luft, R.; Hagenfeldt, L.; Bjorkman, O.; Felig, P. Influence of somatostatin on splanchnic glucose metabolism in postabsorptive and 60-hour fasted humans. J. Clin. Invest. 1977, 59, 299–307, doi:10.1172/JCI108641.
[53]
Laffel, L. Ketone bodies: A review of physiology, pathophysiology and application of monitoring to diabetes. Diabetes Metab Res. Rev. 1999, 15, 412–426, doi:10.1002/(SICI)1520-7560(199911/12)15:6<412::AID-DMRR72>3.0.CO;2-8.
[54]
Hollenbeck, C.B.; Coulston, A.M.; Reaven, G.M. To what extent does increased dietary fiber improve glucose and lipid metabolism in patients with noninsulin-dependent diabetes mellitus (NIDDM)? Am. J. Clin. Nutr. 1986, 43, 16–24.
[55]
Gatenby, S.J.; Ellis, P.R.; Morgan, L.M.; Judd, P.A. Effect of partially depolymerized guar gum on acute metabolic variables in patients with non-insulin-dependent diabetes. Diabet. Med. 1996, 13, 358–364.
[56]
Nuttall, F.Q.; Mooradian, A.D.; Gannon, M.C.; Billington, C.; Krezowski, P. Effect of protein ingestion on the glucose and insulin response to a standardized oral glucose load. Diabetes Care 1984, 7, 465–470.
[57]
Kelley, D.E.; Wing, R.; Buonocore, C.; Sturis, J.; Polonsky, K.; Fitzsimmons, M. Relative effects of calorie restriction and weight loss in noninsulin-dependent diabetes mellitus. J. Clin. Endocrinol. Metab. 1993, 77, 1287–1293, doi:10.1210/jc.77.5.1287.
[58]
McLaughlin, T.; Carter, S.; Lamendola, C.; Abbasi, F.; Yee, G.; Schaaf, P.; Basina, M.; Reaven, G. Effects of moderate variations in macronutrient composition on weight loss and reduction in cardiovascular disease risk in obese, insulin-resistant adults. Am. J. Clin. Nutr. 2006, 8, 813–821.
[59]
Matthews, D.R.; Hosker, J.P.; Rudenski, A.S.; Naylor, B.A.; Treacher, D.F.; Turner, R.C. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 1985, 28, 412–419, doi:10.1007/BF00280883.
[60]
Faber, O.K.; Hagen, C.; Binder, C.; Markussen, J.; Naithani, V.K.; Blix, P.M.; Kuzuya, H.; Horwitz, D.L.; Rubenstein, A.H.; Rossing, N. Kinetics of human connecting peptide in normal and diabetic subjects. J. Clin. Invest. 1978, 62, 197–203, doi:10.1172/JCI109106.
[61]
McLaughlin, T.; Schweitzer, P.; Carter, S.; Yen, C.G.; Lamendola, C.; Abbasi, F.; Reaven, G. Persistence of improvement in insulin sensitivity following a dietary weight loss programme. Diabetes Obes. Metab. 2008, 10, 1186–1194.
[62]
Niskanen, L.; Uusitupa, M.; Sarlund, H.; Siitonen, O.; Paljarvi, L.; Laakso, M. The effects of weight loss on insulin sensitivity, skeletal muscle composition and capillary density in obese non-diabetic subjects. Int. J. Obes. Relat. Metab. Disord. 1996, 20, 154–160.
[63]
Wolever, T.M.; Mehling, C.; Chiasson, J.L.; Josse, R.G.; Leiter, L.A.; Maheux, P.; Rabasa-Lhoret, R.; Rodger, N.W.; Ryan, E.A. Low glycaemic index diet and disposition index in type 2 diabetes (the Canadian trial of carbohydrates in diabetes): A randomised controlled trial. Diabetologia 2008, 51, 1607–1615, doi:10.1007/s00125-008-1093-x.
[64]
Anderson, G.H.; Cho, C.E.; Akhavan, T.; Mollard, R.C.; Luhovyy, B.L.; Finocchiaro, E.T. Relation between estimates of cornstarch digestibility by the Englyst in vitro method and glycemic response, subjective appetite, and short-term food intake in young men. Am. J. Clin. Nutr. 2010, 9, 932–939.
[65]
Robertson, M.D. Dietary-resistant starch and glucose metabolism. Curr. Opin. Clin. Nutr. Metab. Care 2012, 15, 362–367, doi:10.1097/MCO.0b013e3283536931.
[66]
Dixon, L.B.; Subar, A.F.; Peters, U.; Weissfeld, J.L.; Bresalier, R.S.; Risch, A.; Schatzkin, A.; Hayes, R.B. Adherence to the USDA Food Guide, DASH Eating Plan, and Mediterranean dietary pattern reduces risk of colorectal adenoma. J. Nutr. 2007, 137, 2443–2450.
Maki, K.C.; Pelkman, C.L.; Finocchiaro, E.T.; Kelley, K.M.; Lawless, A.L.; Schild, A.L.; Rains, T.M. Resistant starch from high-amylose maize increases insulin sensitivity in overweight and obese men. J. Nutr. 2012, 142, 717–723, doi:10.3945/jn.111.152975.
[71]
Todesco, T.; Rao, A.V.; Bosello, O.; Jenkins, D.J. Propionate lowers blood glucose and alters lipid metabolism in healthy subjects. Am. J. Clin. Nutr. 1991, 54, 860–865.
[72]
Clark, M.J.; Robien, K.; Slavin, J.L. Effect of prebiotics on biomarkers of colorectal cancer in humans: A systematic review. Nutr. Rev. 2012, 70, 436–443, doi:10.1111/j.1753-4887.2012.00495.x.
[73]
Sims, E.A. Are there persons who are obese, but metabolically healthy? Metabolism 2001, 50, 1499–1504, doi:10.1053/meta.2001.27213.
[74]
Brochu, M.; Tchernof, A.; Dionne, I.J.; Sites, C.K.; Eltabbakh, G.H.; Sims, E.A.; Poehlman, E.T. What are the physical characteristics associated with a normal metabolic profile despite a high level of obesity in postmenopausal women? J. Clin. Endocrinol. Metab. 2001, 86, 1020–1025, doi:10.1210/jc.86.3.1020.
[75]
Karelis, A.D.; Faraj, M.; Bastard, J.P.; St Pierre, D.H.; Brochu, M.; Prud’homme, D.; Rabasa-Lhoret, R. The metabolically healthy but obese individual presents a favorable inflammation profile. J. Clin. Endocrinol. Metab. 2005, 90, 4145–4150, doi:10.1210/jc.2005-0482.
[76]
Topping, D.L.; Clifton, P.M. Short-chain fatty acids and human colonic function: roles of resistant starch and nonstarch polysaccharides. Physiol Rev. 2001, 81, 1031–1064.
