An 8-week diet high in cereal fiber and coffee but free of red meat does not improve beta-cell function in patients with type 2 diabetes mellitus: a randomized controlled trial

Yanislava Karusheva, Lejla Kunstein, Alessandra Bierwagen, Bettina Nowotny, Stefan Kabisch, Jan B Groener, Ann Kristin Fleitmann, Christian Herder, Giovanni Pacini, Klaus Strassburger, Hans-Ulrich Häring, Peter P Nawroth, Andreas F H Pfeiffer, Volker Burkart, Karsten Müssig, Michael Roden, Julia Szendroedi, Yanislava Karusheva, Lejla Kunstein, Alessandra Bierwagen, Bettina Nowotny, Stefan Kabisch, Jan B Groener, Ann Kristin Fleitmann, Christian Herder, Giovanni Pacini, Klaus Strassburger, Hans-Ulrich Häring, Peter P Nawroth, Andreas F H Pfeiffer, Volker Burkart, Karsten Müssig, Michael Roden, Julia Szendroedi

Abstract

Background: Higher dietary intake of fibers and coffee, but lower red meat intake is associated with reduced risk for type 2 diabetes in epidemiological studies. We hypothesized that a calorie-restricted diet, which is high in fiber and coffee, but free of red meat, improves beta-cell function in patients with T2D.

Methods: In a randomized parallel-group pilot trial, obese type 2 diabetes patients were randomly allocated to consume either a diet high in cereal fiber and coffee, but free of red meat (n = 17) (L-RISK) or a diet low in fiber, free of coffee but high in red meat (n = 20) (H-RISK) for 8 weeks. Insulin secretion was assessed from glucagon stimulation tests (GST) and mixed-meal tolerance tests (MMTT) before and after dietary intervention.

Results: Both diets resulted in comparable reduction of fasting concentrations of insulin (H-RISK -28% vs. L-RISK -32%, both p < 0.01), C-peptide (H-RISK -26% vs. L-RISK -30%, both p < 0.01) and blood glucose (H-RISK -6.8%, p < 0.05 vs. L-RISK -10%, p < 0.01). Gastric inhibitory peptide (GIP) secretion increased by 24% after 8 weeks in the L-RISK only (p < 0.01). However, GST and MMTT showed no differences in insulin secretion after intervention.

Conclusions: Calorie restriction independent of the intake of fiber, coffee or meat failed to improve beta-cell function, but improved GIP secretion in obese patients with type 2 diabetes.

Trial registration: Registration at Clinicaltrials.gov, Identifier number: NCT01409330, Registered 4 August 2011 - Retrospectively registered.

Keywords: Beta-cell function; Calorie restriction; Coffee; Dietary fiber; Red meat.

Conflict of interest statement

The study was performed according to the Declaration of Helsinki, approved by the ethics committee of the Medical Faculty of Heinrich Heine University Düsseldorf. All participants gave written informed consent before inclusion in the study.All authors have seen and approved the manuscript being submitted.The authors declare that they have no competing interests.Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Figures

Fig. 1
Fig. 1
Fasting concentrations of blood glucose (a), insulin (c), C-peptide (e), as well as mixed-meal-induced beta-cell function (means±SEM) from incremental areas under the respective concentration-time curves (iAUC; b, d, f) before and after dietary intervention in a subgroup of participants of the H-RISK group (n = 19) and L-RISK groups (n = 16). Glucagon-like peptide (GLP-1) (g) and gastric inhibitor peptide (GIP) (h) from incremental areas under the respective concentration-time curves
Fig. 2
Fig. 2
Glucagon-stimulated beta-cell function (means±SEM) from Δinsulin (a) and ΔC-peptide (b) before and after dietary intervention in a subgroup of participants of the H-RISK (n = 15) and L-RISK groups (n = 13)

References

    1. van Dam RM, Hu FB. Coffee consumption and risk of type 2 diabetes: a systematic review. JAMA. 2005;294:97–104. doi: 10.1001/jama.294.1.97.
    1. Lajous M, Tondeur L, Fagherazzi G, de Lauzon-Guillain B, Boutron-Ruaualt MC, Clavel-Chapelon F. Processed and unprocessed red meat consumption and incident type 2 diabetes among French women. Diabetes Care. 2012;35:128–130. doi: 10.2337/dc11-1518.
    1. Huxley R, Lee CM, Barzi F, Timmermeister L, Czernichow S, Perkovic V, Grobbee DE, Batty D, Woodward M. Coffee, decaffeinated coffee, and tea consumption in relation to incident type 2 diabetes mellitus: a systematic review with meta-analysis. Arch Intern Med. 2009;169:2053–2063. doi: 10.1001/archinternmed.2009.439.
    1. Post RE, Mainous AG, 3rd, King DE, Simpson KN. Dietary fiber for the treatment of type 2 diabetes mellitus: a meta-analysis. J Am Board Fam Med. 2012;25:16–23. doi: 10.3122/jabfm.2012.01.110148.
    1. Schulze MB, Hoffmann K, Boeing H, Linseisen J, Rohrmann S, Mohlig M, Pfeiffer AF, Spranger J, Thamer C, Haring HU, et al. An accurate risk score based on anthropometric, dietary, and lifestyle factors to predict the development of type 2 diabetes. Diabetes Care. 2007;30:510–515. doi: 10.2337/dc06-2089.
    1. Juntunen KS, Laaksonen DE, Poutanen KS, Niskanen LK, Mykkanen HM. High-fiber rye bread and insulin secretion and sensitivity in healthy postmenopausal women. Am J Clin Nutr. 2003;77:385–391. doi: 10.1093/ajcn/77.2.385.
    1. Weber KS, Buyken AE, Nowotny B, Strassburger K, Simon MC, Pacini G, Szendroedi J, Mussig K, Roden M. The impact of dietary factors on glycemic control, insulin sensitivity and secretion in the first years after diagnosis of diabetes. Exp Clin Endocrinol Diabetes. 2016;124:230–238. doi: 10.1055/s-0035-1569354.
    1. Loureiro LMR, Reis CEG, da Costa THM. Effects of coffee components on muscle glycogen recovery: a systematic review. Int J Sport Nutr Exerc Metab. 2018;28:284–93.
    1. Ghanim H, Batra M, Abuaysheh S, Green K, Makdissi A, Kuhadiya ND, Chaudhuri A, Dandona P. Antiinflammatory and ROS suppressive effects of the addition of fiber to a high-fat high-calorie meal. J Clin Endocrinol Metab. 2017;102:858–869.
    1. Jang Y, Lee JH, Kim OY, Park HY, Lee SY. Consumption of whole grain and legume powder reduces insulin demand, lipid peroxidation, and plasma homocysteine concentrations in patients with coronary artery disease: randomized controlled clinical trial. Arterioscler Thromb Vasc Biol. 2001;21:2065–2071. doi: 10.1161/hq1201.100258.
    1. Kim EK, Oh TJ, Kim LK, Cho YM. Improving effect of the acute Administration of dietary fiber-enriched cereals on blood glucose levels and gut hormone secretion. J Korean Med Sci. 2016;31:222–230. doi: 10.3346/jkms.2016.31.2.222.
    1. Krebs JD, Parry-Strong A, Weatherall M, Carroll RW, Downie M. A cross-over study of the acute effects of espresso coffee on glucose tolerance and insulin sensitivity in people with type 2 diabetes mellitus. Metabolism. 2012;61:1231–1237. doi: 10.1016/j.metabol.2012.01.021.
    1. Kempf K, Herder C, Erlund I, Kolb H, Martin S, Carstensen M, Koenig W, Sundvall J, Bidel S, Kuha S, Tuomilehto J. Effects of coffee consumption on subclinical inflammation and other risk factors for type 2 diabetes: a clinical trial. Am J Clin Nutr. 2010;91:950–957. doi: 10.3945/ajcn.2009.28548.
    1. Tang C, Koulajian K, Schuiki I, Zhang L, Desai T, Ivovic A, Wang P, Robson-Doucette C, Wheeler MB, Minassian B, et al. Glucose-induced beta cell dysfunction in vivo in rats: link between oxidative stress and endoplasmic reticulum stress. Diabetologia. 2012;55:1366–1379. doi: 10.1007/s00125-012-2474-8.
    1. Brun T, Li N, Jourdain AA, Gaudet P, Duhamel D, Meyer J, Bosco D, Maechler P. Diabetogenic milieus induce specific changes in mitochondrial transcriptome and differentiation of human pancreatic islets. Hum Mol Genet. 2015;24:5270–5284. doi: 10.1093/hmg/ddv247.
    1. Maedler K, Sergeev P, Ris F, Oberholzer J, Joller-Jemelka HI, Spinas GA, Kaiser N, Halban PA, Donath MY. Glucose-induced beta cell production of IL-1beta contributes to glucotoxicity in human pancreatic islets. J Clin Invest. 2017;127:1589. doi: 10.1172/JCI92172.
    1. Aune D, Ursin G, Veierod MB. Meat consumption and the risk of type 2 diabetes: a systematic review and meta-analysis of cohort studies. Diabetologia. 2009;52:2277–2287. doi: 10.1007/s00125-009-1481-x.
    1. de Mello VD, Zelmanovitz T, Perassolo MS, Azevedo MJ, Gross JL. Withdrawal of red meat from the usual diet reduces albuminuria and improves serum fatty acid profile in type 2 diabetes patients with macroalbuminuria. Am J Clin Nutr. 2006;83:1032–1038. doi: 10.1093/ajcn/83.5.1032.
    1. Pan A, Sun Q, Bernstein AM, Schulze MB, Manson JE, Willett WC, Hu FB. Red meat consumption and risk of type 2 diabetes: 3 cohorts of US adults and an updated meta-analysis. Am J Clin Nutr. 2011;94:1088–1096. doi: 10.3945/ajcn.111.018978.
    1. Krebs M, Brehm A, Krssak M, Anderwald C, Bernroider E, Nowotny P, Roth E, Chandramouli V, Landau BR, 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.
    1. Markova M, Pivovarova O, Hornemann S, Sucher S, Frahnow T, Wegner K, Machann J, Petzke KJ, Hierholzer J, Lichtinghagen R, et al. Isocaloric diets high in animal or plant protein reduce liver fat and inflammation in individuals with type 2 diabetes. Gastroenterology. 2017;152:571–585. doi: 10.1053/j.gastro.2016.10.007.
    1. van Nielen M, Feskens EJ, Rietman A, Siebelink E, Mensink M. Partly replacing meat protein with soy protein alters insulin resistance and blood lipids in postmenopausal women with abdominal obesity. J Nutr. 2014;144:1423–1429. doi: 10.3945/jn.114.193706.
    1. Nowotny B, Zahiragic L, Bierwagen A, Kabisch S, Groener JB, Nowotny PJ, Fleitmann AK, Herder C, Pacini G, Erlund I, et al. Low-energy diets differing in fibre, red meat and coffee intake equally improve insulin sensitivity in type 2 diabetes: a randomised feasibility trial. Diabetologia. 2015;58:255–264. doi: 10.1007/s00125-014-3457-8.
    1. Ziegler D, Strom A, Nowotny B, Zahiragic L, Nowotny PJ, Carstensen-Kirberg M, Herder C, Roden M. Effect of low-energy diets differing in fiber, red meat, and coffee intake on cardiac autonomic function in obese individuals with type 2 diabetes. Diabetes Care. 2015;38:1750–1757. doi: 10.2337/dc15-0466.
    1. Carlessi R, Keane KN, Mamotte C, Newsholme P. Nutrient regulation of beta-cell function: what do islet cell/animal studies tell us? Eur J Clin Nutr. 2017;71:890–895. doi: 10.1038/ejcn.2017.49.
    1. Szendroedi J, Saxena A, Weber KS, Strassburger K, Herder C, Burkart V, Nowotny B, Icks A, Kuss O, Ziegler D, et al. Cohort profile: the German diabetes study (GDS) Cardiovasc Diabetol. 2016;15:59. doi: 10.1186/s12933-016-0374-9.
    1. Tura A, Kautzky-Willer A, Pacini G. Insulinogenic indices from insulin and C-peptide: comparison of beta-cell function from OGTT and IVGTT. Diabetes Res Clin Pract. 2006;72:298–301. doi: 10.1016/j.diabres.2005.10.005.
    1. Greenbaum CJ, Mandrup-Poulsen T, McGee PF, Battelino T, Haastert B, Ludvigsson J, Pozzilli P, Lachin JM, Kolb H. Mixed-meal tolerance test versus glucagon stimulation test for the assessment of beta-cell function in therapeutic trials in type 1 diabetes. Diabetes Care. 2008;31:1966–1971. doi: 10.2337/dc07-2451.
    1. Nowotny B, Zahiragic L, Krog D, Nowotny PJ, Herder C, Carstensen M, Yoshimura T, Szendroedi J, Phielix E, Schadewaldt P, et al. Mechanisms underlying the onset of oral lipid-induced skeletal muscle insulin resistance in humans. Diabetes. 2013;62:2240–2248. doi: 10.2337/db12-1179.
    1. Dominguez LJ, Bes-Rastrollo M, Basterra-Gortari FJ, Gea A, Barbagallo M, Martinez-Gonzalez MA. Association of a dietary score with incident type 2 diabetes: the dietary-based diabetes-risk score (DDS) PLoS One. 2015;10:e0141760. doi: 10.1371/journal.pone.0141760.
    1. Ye EQ, Chacko SA, Chou EL, 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. doi: 10.3945/jn.111.155325.
    1. Lean ME, Leslie WS, Barnes AC, Brosnahan N, Thom G, McCombie L, Peters C, Zhyzhneuskaya S, Al-Mrabeh A, Hollingsworth KG, et al. Primary care-led weight management for remission of type 2 diabetes (DiRECT): an open-label, cluster-randomised trial. Lancet. 2018;391:541–551. doi: 10.1016/S0140-6736(17)33102-1.
    1. Sjostrom L, Peltonen M, Jacobson P, Ahlin S, Andersson-Assarsson J, Anveden A, Bouchard C, Carlsson B, Karason K, Lonroth H, et al. Association of bariatric surgery with long-term remission of type 2 diabetes and with microvascular and macrovascular complications. JAMA. 2014;311:2297–2304. doi: 10.1001/jama.2014.5988.
    1. Yamakado M, Nagao K, Imaizumi A, Tani M, Toda A, Tanaka T, Jinzu H, Miyano H, Yamamoto H, Daimon T, et al. Plasma free amino acid profiles predict four-year risk of developing diabetes, metabolic syndrome, dyslipidemia, and hypertension in Japanese population. Sci Rep. 2015;5:11918. doi: 10.1038/srep11918.
    1. Cho SS, Qi L, Fahey GC, Jr, Klurfeld DM. Consumption of cereal fiber, mixtures of whole grains and bran, and whole grains and risk reduction in type 2 diabetes, obesity, and cardiovascular disease. Am J Clin Nutr. 2013;98:594–619. doi: 10.3945/ajcn.113.067629.
    1. Pham NM, Nanri A, Kochi T, Kuwahara K, Tsuruoka H, Kurotani K, Akter S, Kabe I, Sato M, Hayabuchi H, Mizoue T. Coffee and green tea consumption is associated with insulin resistance in Japanese adults. Metabolism. 2014;63:400–408. doi: 10.1016/j.metabol.2013.11.008.
    1. Arnlov J, Vessby B, Riserus U. Coffee consumption and insulin sensitivity. JAMA. 2004;291:1199–1201. doi: 10.1001/jama.291.10.1199-b.
    1. Dandona P, Ghanim H, Abuaysheh S, Green K, Batra M, Dhindsa S, Makdissi A, Patel R, Chaudhuri A. Decreased insulin secretion and incretin concentrations and increased glucagon concentrations after a high-fat meal when compared with a high-fruit and -fiber meal. Am J Physiol Endocrinol Metab. 2015;308:E185–E191. doi: 10.1152/ajpendo.00275.2014.
    1. Tilg H, Moschen AR, Roden M. NAFLD and diabetes mellitus. Nat Rev Gastroenterol Hepatol. 2017;14:32–42. doi: 10.1038/nrgastro.2016.147.
    1. Keijzers GB, De Galan BE, Tack CJ, Smits P. Caffeine can decrease insulin sensitivity in humans. Diabetes Care. 2002;25:364–369. doi: 10.2337/diacare.25.2.364.

Source: PubMed

3
Abonneren