Skip to main content
SpringerLink
Log in

Consumption of a high β-glucan barley flour improves glucose control and fatty liver and increases muscle acylcarnitines in the Zucker diabetic fatty rat

  • Original Contribution
  • Published:
European Journal of Nutrition Aims and scope Submit manuscript

Abstract

Purpose

The soluble fiber β-glucan, a natural component of barley, has been shown to lower the postprandial glucose response and is thought to improve insulin resistance.

Methods

This study examined the effect of chronic consumption of the high β-glucan barley flour on glucose control, liver lipids and markers of muscle fatty acid oxidation in the Zucker diabetic fatty (ZDF) rat. Two groups of ZDF rats were fed diets containing either 6 % β-glucan in the form of barley flour or cellulose as a control for 6 weeks. A group of Zucker lean rats served as a negative control.

Results

The barley flour group had an increased small intestinal contents viscosity compared to the obese control group. After 6 weeks, the barley flour group had reduced glycated hemoglobin, lower relative kidney weights and a reduced area under the curve during a glucose tolerance test, indicating improved glucose control. Fasting plasma adiponectin levels increased in the barley flour group and were not different than the lean control group. ZDF rats on the barley flour diet had lower relative epididymal fat pad weights than the obese control and a greater food efficiency ratio. The barley flour group also had reduced liver weights and a decreased concentration of liver lipids. The barley flour group had significantly higher concentrations of muscle acylcarnitines, a metabolite generated during fatty acid oxidation.

Conclusion

These results show that chronic consumption of β-glucans can improve glucose control and decrease fatty liver in a model of diabetes with obesity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Shaw JE, Sicree RA, Zimmet PZ (2010) Global estimates of the prevalence of diabetes for 2010 and 2030. Diabetes Res Clin Pract 87(1):4–14. doi:10.1016/j.diabres.2009.10.007

    Article  CAS  Google Scholar 

  2. Wang YC, McPherson K, Marsh T, Gortmaker SL, Brown M (2011) Health and economic burden of the projected obesity trends in the USA and the UK. Lancet 378(9793):815–825. doi:10.1016/S0140-6736(11)60814-3

    Article  Google Scholar 

  3. Ratziu V, Bellentani S, Cortez-Pinto H, Day C, Marchesini G (2010) A position statement on NAFLD/NASH based on the EASL 2009 special conference. J Hepatol 53(2):372–384. doi:10.1016/j.jhep.2010.04.008

    Article  Google Scholar 

  4. Cheung O, Sanyal AJ (2009) Recent advances in nonalcoholic fatty liver disease. Curr Opin Gastroenterol 25(3):230–237

    Article  Google Scholar 

  5. Koves TR, Ussher JR, Noland RC, Slentz D, Mosedale M, Ilkayeva O, Bain J, Stevens R, Dyck JR, Newgard CB, Lopaschuk GD, Muoio DM (2008) Mitochondrial overload and incomplete fatty acid oxidation contribute to skeletal muscle insulin resistance. Cell Metab 7(1):45–56. doi:10.1016/j.cmet.2007.10.013

    Article  CAS  Google Scholar 

  6. Adams SH, Hoppel CL, Lok KH, Zhao L, Wong SW, Minkler PE, Hwang DH, Newman JW, Garvey WT (2009) Plasma acylcarnitine profiles suggest incomplete long-chain fatty acid beta-oxidation and altered tricarboxylic acid cycle activity in type 2 diabetic African-American women. J Nutr 139(6):1073–1081. doi:10.3945/jn.108.103754

    Article  CAS  Google Scholar 

  7. Post RE, Mainous AG 3rd, King DE, Simpson KN (2012) Dietary fiber for the treatment of type 2 diabetes mellitus: a meta-analysis. J Am Board Fam Med JABFM 25(1):16–23. doi:10.3122/jabfm.2012.01.110148

    Article  Google Scholar 

  8. Ye EQ, Chacko SA, Chou EL, Kugizaki M, Liu S (2012) Greater whole-grain intake is associated with lower risk of type 2 diabetes, cardiovascular disease, and weight gain. J Nutr 142(7):1304–1313. doi:10.3945/jn.111.155325

    Article  CAS  Google Scholar 

  9. Grunberger G, Jen KL, Artiss JD (2007) The benefits of early intervention in obese diabetic patients with FBCx: a new dietary fibre. Diabetes/Metabolism Res Rev 23(1):56–62

    Article  CAS  Google Scholar 

  10. Galisteo M, Sanchez M, Vera R, Gonzalez M, Anguera A, Duarte J, Zarzuelo A (2005) A diet supplemented with husks of Plantago ovata reduces the development of endothelial dysfunction, hypertension, and obesity by affecting adiponectin and TNF-alpha in obese Zucker rats. J Nutr 135(10):2399–2404

    CAS  Google Scholar 

  11. Targher G, Bertolini L, Scala L, Poli F, Zenari L, Falezza G (2004) Decreased plasma adiponectin concentrations are closely associated with nonalcoholic hepatic steatosis in obese individuals. Clin Endocrinol 61(6):700–703. doi:10.1111/j.1365-2265.2004.02151.x

    Article  CAS  Google Scholar 

  12. Dikeman CL, Fahey GC (2006) Viscosity as related to dietary fiber: a review. Crit Rev Food Sci Nutr 46(8):649–663. doi:10.1080/10408390500511862

    Article  CAS  Google Scholar 

  13. Brown AJ, Goldsworthy SM, Barnes AA, Eilert MM, Tcheang L, Daniels D, Muir AI, Wigglesworth MJ, Kinghorn I, Fraser NJ, Pike NB, Strum JC, Steplewski KM, Murdock PR, Holder JC, Marshall FH, Szekeres PG, Wilson S, Ignar DM, Foord SM, Wise A, Dowell SJ (2003) The orphan G protein-coupled receptors GPR41 and GPR43 are activated by propionate and other short chain carboxylic acids. J Biol Chem 278(13):11312–11319. doi:10.1074/jbc.M211609200

    Article  CAS  Google Scholar 

  14. Ge H, Li X, Weiszmann J, Wang P, Baribault H, Chen JL, Tian H, Li Y (2008) Activation of G protein-coupled receptor 43 in adipocytes leads to inhibition of lipolysis and suppression of plasma free fatty acids. Endocrinology 149(9):4519–4526. doi:10.1210/en.2008-0059

    Article  CAS  Google Scholar 

  15. Reaven GM, Hollenbeck C, Jeng C-Y, Wu MS, Chen Y-DI (1988) Measurement of plasma glucose, free fatty acid, lactate, and insulin for 24 h in patients with NIDDM. Diabetes 37(8):1020–1024. doi:10.2337/diab.37.8.1020

    Article  CAS  Google Scholar 

  16. Staehr P, Hother-Nielsen O, Landau BR, Chandramouli V, Holst JJ, Beck-Nielsen H (2003) Effects of free fatty acids per se on glucose production, gluconeogenesis, and glycogenolysis. Diabetes 52(2):260–267

    Article  CAS  Google Scholar 

  17. Choi JS, Kim H, Jung MH, Hong S, Song J (2010) Consumption of barley beta-glucan ameliorates fatty liver and insulin resistance in mice fed a high-fat diet. Mol Nutr Food Res 54(7):1004–1013. doi:10.1002/mnfr.200900127

    Article  CAS  Google Scholar 

  18. Biorklund M, van Rees A, Mensink RP, Onning G (2005) Changes in serum lipids and postprandial glucose and insulin concentrations after consumption of beverages with beta-glucans from oats or barley: a randomised dose-controlled trial. Eur J Clin Nutr 59(11):1272–1281. doi:10.1038/sj.ejcn.1602240

    Article  CAS  Google Scholar 

  19. Keogh GF, Cooper GJ, Mulvey TB, McArdle BH, Coles GD, Monro JA, Poppitt SD (2003) Randomized controlled crossover study of the effect of a highly beta-glucan-enriched barley on cardiovascular disease risk factors in mildly hypercholesterolemic men. Am J Clin Nutr 78(4):711–718

    CAS  Google Scholar 

  20. Liatis S, Tsapogas P, Chala E, Dimosthenopoulos C, Kyriakopoulos K, Kapantais E, Katsilambros N (2009) The consumption of bread enriched with betaglucan reduces LDL-cholesterol and improves insulin resistance in patients with type 2 diabetes. Diabetes Metabolism 35(2):115–120. doi:10.1016/j.diabet.2008.09.004

    Article  CAS  Google Scholar 

  21. Kabir M, Oppert JM, Vidal H, Bruzzo F, Fiquet C, Wursch P, Slama G, Rizkalla SW (2002) Four-week low-glycemic index breakfast with a modest amount of soluble fibers in type 2 diabetic men. Metabolism Clin Exp 51(7):819–826

    Article  CAS  Google Scholar 

  22. Clark JB, Palmer CJ, Shaw WN (1983) The diabetic Zucker fatty rat. Proc Soc Exp Biol Med Soc Exp Biol Med 173(1):68–75

    Article  CAS  Google Scholar 

  23. Morin LG, Prox J (1973) Single glucose oxidase–peroxidase reagent for two-minute determination of serum glucose. Clin Chem 19(9):959–962

    CAS  Google Scholar 

  24. Lee HS, Shoeman DW, Csallany AS (1992) Urinary response to in vivo lipid peroxidation induced by vitamin E deficiency. Lipids 27(2):124–128

    Article  CAS  Google Scholar 

  25. Folch J, Lees M, Sloane Stanley GH (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226(1):497–509

    CAS  Google Scholar 

  26. Gallaher DD, Hassel CA, Lee KJ, Gallaher CM (1993) Viscosity and fermentability as attributes of dietary fiber responsible for the hypocholesterolemic effect in hamsters. J Nutr 123(2):244–252

    CAS  Google Scholar 

  27. Yang S, Minkler P, Hoppel C (2007) cis-3,4-Methylene-heptanoylcarnitine: characterization and verification of the C8:1 acylcarnitine in human urine. J Chromatogr B Analyt Technol Biomed Life Sci 857(2):251–258. doi:10.1016/j.jchromb.2007.07.027

    Article  CAS  Google Scholar 

  28. Rabe K, Lehrke M, Parhofer KG, Broedl UC (2008) Adipokines and insulin resistance. Mol Med 14(11–12):741–751. doi:10.2119/2008-00058.Rabe

    CAS  Google Scholar 

  29. Tishinsky JM, Robinson LE, Dyck DJ (2012) Insulin-sensitizing properties of adiponectin. Biochimie 94(10):2131–2136. doi:10.1016/j.biochi.2012.01.017

    Google Scholar 

  30. Verbeke K, Ferchaud-Roucher V, Preston T, Small AC, Henckaerts L, Krempf M, Wang H, Vonk RJ, Priebe MG (2010) Influence of the type of indigestible carbohydrate on plasma and urine short-chain fatty acid profiles in healthy human volunteers. Eur J Clin Nutr 64(7):678–684. doi:10.1038/ejcn.2010.92

    Article  CAS  Google Scholar 

  31. Koves TR, Ussher JR, Noland RC, Slentz D, Mosedale M, Ilkayeva O, Bain J, Stevens R, Dyck JR, Newgard CB, Lopaschuk GD, Muoio DM (2008) Mitochondrial overload and incomplete fatty acid oxidation contribute to skeletal muscle insulin resistance. Cell Metab 7(1):45–56. doi:10.1016/j.cmet.2007.10.013

    Article  CAS  Google Scholar 

  32. Gerhart-Hines Z, Rodgers JT, Bare O, Lerin C, Kim S-H, Mostoslavsky R, Alt FW, Wu Z, Puigserver P (2007) Metabolic control of muscle mitochondrial function and fatty acid oxidation through SIRT1/PGC-1a. EMBO J 26:1913–1923. doi:10.1038/

    Article  CAS  Google Scholar 

  33. Marciani L, Gowland PA, Spiller RC, Manoj P, Moore RJ, Young P, Fillery-Travis AJ (2001) Effect of meal viscosity and nutrients on satiety, intragastric dilution, and emptying assessed by MRI. Am J Physiol Gastrointest Liver Physiol 280(6):G1227–G1233

    CAS  Google Scholar 

  34. Schneeman BO, Gallaher D (1985) Effects of dietary fiber on digestive enzyme activity and bile acids in the small intestine. Proc Soc Exp Biol Med Soc Exp Biol Med 180(3):409–414

    Article  CAS  Google Scholar 

  35. McDonald MHDaA (1998) Fiber: forms and functions. Nutr Res 18(4):617–624

    Article  Google Scholar 

  36. Yokoyama WH, Shao Q (2006) Soluble fibers prevent insulin resistance in hamsters fed high saturated fat diets. Cereal Food World 51(1):16–18. doi:10.1094/Cfw-51-0016

    CAS  Google Scholar 

  37. Leonard BL, Watson RN, Loomes KM, Phillips AR, Cooper GJ (2005) Insulin resistance in the Zucker diabetic fatty rat: a metabolic characterisation of obese and lean phenotypes. Acta Diabetol 42(4):162–170. doi:10.1007/s00592-005-0197-8

    Article  CAS  Google Scholar 

  38. Youn M, Csallany AS, Gallaher DD (2012) Whole grain consumption has a modest effect on the development of diabetes in the Goto-Kakisaki rat. Br J Nutr 107(2):192–201. doi:10.1017/S0007114511002741

    Article  CAS  Google Scholar 

  39. Islam A, Civitarese AE, Hesslink RL, Gallaher DD (2012) Viscous dietary fiber reduces adiposity and plasma leptin and increases muscle expression of fat oxidation genes in rats. Obesity (Silver Spring) 20(2):349–355. doi:10.1038/oby.2011.341

  40. Suzuki T, Hara H (2004) Ingestion of guar gum hydrolysate, a soluble and fermentable nondigestible saccharide, improves glucose intolerance and prevents hypertriglyceridemia in rats fed fructose. J Nutr 134(8):1942–1947

    CAS  Google Scholar 

  41. Groop PH, Aro A, Stenman S, Groop L (1993) Long-term effects of guar gum in subjects with non-insulin-dependent diabetes mellitus. Am J Clin Nutr 58(4):513–518

    CAS  Google Scholar 

  42. Isken F, Klaus S, Osterhoff M, Pfeiffer AF, Weickert MO (2010) Effects of long-term soluble vs. insoluble dietary fiber intake on high-fat diet-induced obesity in C57BL/6 J mice. J Nutr Biochem 21(4):278–284. doi:10.1016/j.jnutbio.2008.12.012

    Article  CAS  Google Scholar 

  43. Track NS, Cawkwell ME, Chin BC, Chiu SS, Haberer SA, Honey CR (1985) Guar gum consumption in adolescent and adult rats: short- and long-term metabolic effects. Can J Physiol Pharmacol 63(9):1113–1121

    Article  CAS  Google Scholar 

  44. Meyer KA, Kushi LH, Jacobs DR Jr, Slavin J, Sellers TA, Folsom AR (2000) Carbohydrates, dietary fiber, and incident type 2 diabetes in older women. Am J Clin Nutr 71(4):921–930

    CAS  Google Scholar 

  45. Seyer-Hansen K (1977) Renal hypertrophy in experimental diabetes: relation to severity of diabetes. Diabetologia 13(2):141–143

    Article  CAS  Google Scholar 

  46. Gallaher DD, Olson JM, Larntz K (1992) Dietary guar gum halts further renal enlargement in rats with established diabetes. J Nutr 122(12):2391–2397

    CAS  Google Scholar 

  47. Giacco F, Brownlee M (2010) Oxidative stress and diabetic complications. Circ Res 107(9):1058–1070. doi:10.1161/CIRCRESAHA.110.223545

    Article  CAS  Google Scholar 

  48. Rains JL, Jain SK (2011) Oxidative stress, insulin signaling, and diabetes. Free Radic Biol Med 50(5):567–575. doi:10.1016/j.freeradbiomed.2010.12.006

    Article  CAS  Google Scholar 

  49. Hara K, Horikoshi M, Yamauchi T, Yago H, Miyazaki O, Ebinuma H, Imai Y, Nagai R, Kadowaki T (2006) Measurement of the high-molecular weight form of adiponectin in plasma is useful for the prediction of insulin resistance and metabolic syndrome. Diabetes Care 29(6):1357–1362. doi:10.2337/dc05-1801

    Article  CAS  Google Scholar 

  50. Cnop M, Havel PJ, Utzschneider KM, Carr DB, Sinha MK, Boyko EJ, Retzlaff BM, Knopp RH, Brunzell JD, Kahn SE (2003) Relationship of adiponectin to body fat distribution, insulin sensitivity and plasma lipoproteins: evidence for independent roles of age and sex. Diabetologia 46(4):459–469. doi:10.1007/s00125-003-1074-z

    CAS  Google Scholar 

  51. Hong YH, Nishimura Y, Hishikawa D, Tsuzuki H, Miyahara H, Gotoh C, Choi KC, Feng DD, Chen C, Lee HG, Katoh K, Roh SG, Sasaki S (2005) Acetate and propionate short chain fatty acids stimulate adipogenesis via GPCR43. Endocrinology 146(12):5092–5099. doi:10.1210/en.2005-0545

    Article  CAS  Google Scholar 

  52. Banz WJ, Iqbal MJ, Bollaert M, Chickris N, James B, Higginbotham DA, Peterson R, Murphy L (2007) Ginseng modifies the diabetic phenotype and genes associated with diabetes in the male ZDF rat. Phytomed Int J Phytother Phytopharmacol 14(10):681–689. doi:10.1016/j.phymed.2007.06.003

    Article  CAS  Google Scholar 

  53. Angulo P (2002) Nonalcoholic fatty liver disease. New Engl J Med 346(16):1221–1231. doi:10.1056/NEJMra011775

    Article  CAS  Google Scholar 

  54. Hung SC, Anderson WH, Albers DR, Langhorst ML, Young SA (2011) Effect of hydroxypropyl methylcellulose on obesity and glucose metabolism in a diet-induced obesity mouse model. J Diabetes 3(2):158–167. doi:10.1111/j.1753-0407.2011.00118.x

    Article  CAS  Google Scholar 

  55. Anastasovska J, Arora T, Sanchez Canon GJ, Parkinson JR, Touhy K, Gibson GR, Nadkarni NA, So PW, Goldstone AP, Thomas EL, Hankir MK, Van Loo J, Modi N, Bell JD, Frost G (2012) Fermentable carbohydrate alters hypothalamic neuronal activity and protects against the obesogenic environment. Obesity (Silver Spring) 20(5):1016–1023. doi:10.1038/oby.2012.6

    Article  CAS  Google Scholar 

  56. AbuMweis SS, Jew S, Ames NP (2010) Beta-glucan from barley and its lipid-lowering capacity: a meta-analysis of randomized, controlled trials. Eur J Clin Nutr 64(12):1472–1480. doi:10.1038/ejcn.2010.178

    Article  CAS  Google Scholar 

  57. Puri P, Baillie RA, Wiest MM, Mirshahi F, Choudhury J, Cheung O, Sargeant C, Contos MJ, Sanyal AJ (2007) A lipidomic analysis of nonalcoholic fatty liver disease. Hepatology 46(4):1081–1090. doi:10.1002/hep.21763

    Article  CAS  Google Scholar 

  58. Van Rooyen DM, Larter CZ, Haigh WG, Yeh MM, Ioannou G, Kuver R, Lee SP, Teoh NC, Farrell GC (2011) Hepatic free cholesterol accumulates in obese, diabetic mice and causes nonalcoholic steatohepatitis. Gastroenterology 141(4):1393–1403, 1403 e1391–1395. doi:10.1053/j.gastro.2011.06.040

    Google Scholar 

  59. Yao PM, Tabas I (2001) Free cholesterol loading of macrophages is associated with widespread mitochondrial dysfunction and activation of the mitochondrial apoptosis pathway. J Biol Chem 276(45):42468–42476. doi:10.1074/jbc.M101419200

    Article  CAS  Google Scholar 

  60. Farrell GC, van Rooyen D (2012) Liver cholesterol: is it playing possum in NASH? Am J Physiol Gastrointest Liver Physiol 303(1):G9–G11. doi:10.1152/ajpgi.00008.2012

    Article  CAS  Google Scholar 

  61. Watt MJ, Hoy AJ (2012) Lipid metabolism in skeletal muscle: generation of adaptive and maladaptive intracellular signals for cellular function. Am J Physiol Endocrinol Metab 302(11):E1315–E1328. doi:10.1152/ajpendo.00561.2011

    Article  CAS  Google Scholar 

  62. McGarry JD, Brown NF (1997) The mitochondrial carnitine palmitoyltransferase system. From concept to molecular analysis. Eur J Biochem 244(1):1–14

    Article  CAS  Google Scholar 

  63. Ramos-Roman MA, Sweetman L, Valdez MJ, Parks EJ (2012) Postprandial changes in plasma acylcarnitine concentrations as markers of fatty acid flux in overweight and obesity. Metabolism Clin Exp 61(2):202–212. doi:10.1016/j.metabol.2011.06.008

    Article  CAS  Google Scholar 

  64. Bridges SR, Anderson JW, Deakins DA, Dillon DW, Wood CL (1992) Oat bran increases serum acetate of hypercholesterolemic men. Am J Clin Nutr 56(2):455–459

    CAS  Google Scholar 

  65. Bian F, Kasumov T, Jobbins KA, Minkler PE, Anderson VE, Kerner J, Hoppel CL, Brunengraber H (2006) Competition between acetate and oleate for the formation of malonyl-CoA and mitochondrial acetyl-CoA in the perfused rat heart. J Mol Cell Cardiol 41(5):868–875. doi:10.1016/j.yjmcc.2006.08.011

    Article  CAS  Google Scholar 

  66. O’Donnell JM, Alpert NM, White LT, Lewandowski ED (2002) Coupling of mitochondrial fatty acid uptake to oxidative flux in the intact heart. Biophys J 82(1 Pt 1):11–18. doi:10.1016/S0006-3495(02)75369-1

    Article  Google Scholar 

Download references

Acknowledgments

We thank Nghia Le for liver extraction and lipid and cholesterol analysis and Ana Carla Gilberto dos Santos for urinary TBARS analysis. Supported by the University of Minnesota College of Human Ecology Legacy Funds and the Minnesota Agriculture Experiment Station.

Conflict of interest

The authors have declared no conflict of interest.

Author information

Authors and Affiliations

  1. Department of Food Science and Nutrition, University of Minnesota-Twin Cities, 1334 Eckles Avenue, St. Paul, MN, 55108-1038, USA

    David A. Brockman, Xiaoli Chen & Daniel D. Gallaher

Authors
  1. David A. Brockman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiaoli Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Daniel D. Gallaher
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Daniel D. Gallaher.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Brockman, D.A., Chen, X. & Gallaher, D.D. Consumption of a high β-glucan barley flour improves glucose control and fatty liver and increases muscle acylcarnitines in the Zucker diabetic fatty rat. Eur J Nutr 52, 1743–1753 (2013). https://doi.org/10.1007/s00394-012-0478-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00394-012-0478-2

Keywords

Search

Navigation