A Plant-Based Dietary Intervention Improves Beta-Cell Function and Insulin Resistance in Overweight Adults: A 16-Week Randomized Clinical Trial

Hana Kahleova, Andrea Tura, Martin Hill, Richard Holubkov, Neal D Barnard, Hana Kahleova, Andrea Tura, Martin Hill, Richard Holubkov, Neal D Barnard

Abstract

The aim of this study was to test the effect of a plant-based dietary intervention on beta-cell function in overweight adults with no history of diabetes. Participants (n = 75) were randomized to follow a low-fat plant-based diet (n = 38) or to make no diet changes (n = 37) for 16 weeks. At baseline and 16 weeks, beta-cell function was quantified with a mathematical model. Using a standard meal test, insulin secretory rate was calculated by C-peptide deconvolution. The Homeostasis Model Assessment (HOMA-IR) index was used to assess insulin resistance while fasting. A marked increase in meal-stimulated insulin secretion was observed in the intervention group compared with controls (interaction between group and time, Gxt, p < 0.001). HOMA-IR index fell significantly (p < 0.001) in the intervention group (treatment effect -1.0 (95% CI, -1.2 to -0.8); Gxt, p = 0.004). Changes in HOMA-IR correlated positively with changes in body mass index (BMI) and visceral fat volume (r = 0.34; p = 0.009 and r = 0.42; p = 0.001, respectively). The latter remained significant after adjustment for changes in BMI (r = 0.41; p = 0.002). Changes in glucose-induced insulin secretion correlated negatively with BMI changes (r = -0.25; p = 0.04), but not with changes in visceral fat. Beta-cell function and insulin sensitivity were significantly improved through a low-fat plant-based diet in overweight adults.

Keywords: beta-cell function; diabetes; diet; nutrition; vegan.

Conflict of interest statement

Hana Kahleova works as the Director of Clinical Research at the Physicians Committee for Responsible Medicine, a nonprofit organization encouraging the use of low-fat, plant-based diets and discouraging the use of animal-derived, fatty, and sugary foods. Barnard has received research funding from the National Institute of Diabetes and Digestive and Kidney Diseases (NIH), the National Science Foundation, and the Diabetes Action Research and Education Foundation. He serves without financial compensation as president of the Physicians Committee for Responsible Medicine and Barnard Medical Center, nonprofit organizations providing education, research, and medical care related to nutrition. He writes books and gives lectures related to nutrition and health, and has received royalties and honoraria from these sources. Andrea Tura, Martin Hill and Richard Holubkov declare no conflict of interest.

Figures

Figure 1
Figure 1
Enrollment of the participants and completion of the study.
Figure 2
Figure 2
Dose-response insulin secretion in response to different plasma glucose levels. Triangles with the blue line represent the control group (empty triangles and a dashed line at baseline, and full triangles with a full line at 16 weeks), while squares with the red line show data from the intervention group (empty squares with a dashed line at baseline, and full squares with a full line at 16 weeks). Data are given as means with 95% CIs.

References

    1. Ferrannini E., Gastaldelli A., Miyazaki Y., Matsuda M., Pettiti M., Natali A., Mari A., DeFronzo R.A. Predominant role of reduced beta-cell sensitivity to glucose over insulin resistance in impaired glucose tolerance. Diabetologia. 2003;46:1211–1219. doi: 10.1007/s00125-003-1169-6.
    1. Butler A.E., Janson J., Bonner-Weir S., Ritzel R., Rizza R.A., Butler P.C. Beta-cell deficit and increased beta-cell apoptosis in humans with type 2 diabetes. Diabetes. 2003;52:102–110. doi: 10.2337/diabetes.52.1.102.
    1. Gastaldelli A., Ferrannini E., Miyazaki Y., Matsuda M., DeFronzo R.A. Beta-cell dysfunction and glucose intolerance: Results from the San Antonio metabolism (SAM) study. Diabetologia. 2004;47:31–39. doi: 10.1007/s00125-003-1263-9.
    1. Solomon T.P.J., Haus J.M., Kelly K.R., Rocco M., Kashyap S.R., Kirwan J.P. Improved Pancreatic Beta-Cell Function In Type 2 Diabetics Following Lifestyle-Induced Weight Loss Is Related To Glucose-Dependent Insulinotropic Polypeptide. Diabetes Care. 2010 doi: 10.2337/dc09-2021.
    1. Tonstad S., Butler T., Yan R., Fraser G.E. Type of Vegetarian Diet, Body Weight, and Prevalence of Type 2 Diabetes. Diabetes Care. 2009;32:791–796. doi: 10.2337/dc08-1886.
    1. Snowdon D.A., Phillips R.L. Does a vegetarian diet reduce the occurrence of diabetes? Am. J. Public Health. 1985;75:507–512. doi: 10.2105/AJPH.75.5.507.
    1. Cersosimo E., Solis-Herrera C., Trautmann M.E., Malloy J., Triplitt C.L. Assessment of pancreatic β-cell function: Review of methods and clinical applications. Curr. Diabetes Rev. 2014;10:2–42. doi: 10.2174/1573399810666140214093600.
    1. Pacini G., Mari A. Methods for clinical assessment of insulin sensitivity and beta-cell function. Best Pract. Res. Clin. Endocrinol. Metab. 2003;17:305–322. doi: 10.1016/S1521-690X(03)00042-3.
    1. Vang A., Singh P.N., Lee J.W., Haddad E.H., Brinegar C.H. Meats, processed meats, obesity, weight gain and occurrence of diabetes among adults: Findings from Adventist Health Studies. Ann. Nutr. Metab. 2008;52:96–104. doi: 10.1159/000121365.
    1. Barnard N.D., Cohen J., Jenkins D.J.A., Turner-McGrievy G., Gloede L., Jaster B., Seidl K., Green A.A., Talpers S. A low-fat vegan diet improves glycemic control and cardiovascular risk factors in a randomized clinical trial in individuals with type 2 diabetes. Diabetes Care. 2006;29:1777–1783. doi: 10.2337/dc06-0606.
    1. Barnard N.D., Gloede L., Cohen J., Jenkins D.J.A., Turner-McGrievy G., Green A.A., Ferdowsian H. A low-fat vegan diet elicits greater macronutrient changes, but is comparable in adherence and acceptability, compared with a more conventional diabetes diet among individuals with type 2 diabetes. J. Am. Diet. Assoc. 2009;109:263–272. doi: 10.1016/j.jada.2008.10.049.
    1. Schakel S.F., Sievert Y.A., Buzzard I.M. Sources of data for developing and maintaining a nutrient database. J. Am. Diet. Assoc. 1988;88:1268–1271.
    1. Hagströmer M., Oja P., Sjöström M. The International Physical Activity Questionnaire (IPAQ): A study of concurrent and construct validity. Public Health Nutr. 2006;9:755–762. doi: 10.1079/PHN2005898.
    1. Van Cauter E., Mestrez F., Sturis J., Polonsky K.S. Estimation of insulin secretion rates from C-peptide levels. Comparison of individual and standard kinetic parameters for C-peptide clearance. Diabetes. 1992;41:368–377. doi: 10.2337/diabetes.41.3.368.
    1. Mari A., Tura A., Gastaldelli A., Ferrannini E. Assessing insulin secretion by modeling in multiple-meal tests: Role of potentiation. Diabetes. 2002;51:S221–S226. doi: 10.2337/diabetes.51.2007.S221.
    1. Mari A., Schmitz O., Gastaldelli A., Oestergaard T., Nyholm B., Ferrannini E. Meal and oral glucose tests for assessment of beta-cell function: Modeling analysis in normal subjects. Am. J. Physiol. Endocrinol. Metab. 2002;283:E1159–E1166. doi: 10.1152/ajpendo.00093.2002.
    1. 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.
    1. Abdul-Ghani M.A., Matsuda M., Balas B., DeFronzo R.A. Muscle and liver insulin resistance indexes derived from the oral glucose tolerance test. Diabetes Care. 2007;30:89–94. doi: 10.2337/dc06-1519.
    1. Gupta S.K. Intention-to-treat concept: A review. Perspect. Clin. Res. 2011;2:109–112. doi: 10.4103/2229-3485.83221.
    1. Kahleova H., Mari A., Nofrate V., Matoulek M., Kazdova L., Hill M., Pelikanova T. Improvement in β-cell function after diet-induced weight loss is associated with decrease in pancreatic polypeptide in subjects with type 2 diabetes. J. Diabetes Complicat. 2012;26:442–449. doi: 10.1016/j.jdiacomp.2012.05.003.
    1. Gerst F., Wagner R., Kaiser G., Panse M., Heni M., Machann J., Bongers M.N., Sartorius T., Sipos B., Fend F., et al. Metabolic crosstalk between fatty pancreas and fatty liver: Effects on local inflammation and insulin secretion. Diabetologia. 2017;60:2240–2251. doi: 10.1007/s00125-017-4385-1.
    1. Tuomilehto J., Lindström J., Eriksson J.G., Valle T.T., Hämäläinen H., Ilanne-Parikka P., Keinänen-Kiukaanniemi S., Laakso M., Louheranta A., Rastas M., et al. Finnish Diabetes Prevention Study Group Prevention of type 2 diabetes mellitus by changes in lifestyle among subjects with impaired glucose tolerance. N. Engl. J. Med. 2001;344:1343–1350. doi: 10.1056/NEJM200105033441801.
    1. De Mello V.D.F., Lindström J., Eriksson J., Ilanne-Parikka P., Keinänen-Kiukaanniemi S., Sundvall J., Laakso M., Tuomilehto J., Uusitupa M. Insulin secretion and its determinants in the progression of impaired glucose tolerance to type 2 diabetes in impaired glucose-tolerant individuals: The Finnish Diabetes Prevention Study. Diabetes Care. 2012;35:211–217. doi: 10.2337/dc11-1272.
    1. Moore W.J., McGrievy M.E., Turner-McGrievy G.M. Dietary adherence and acceptability of five different diets, including vegan and vegetarian diets, for weight loss: The New DIETs study. Eat. Behav. 2015;19:33–38. doi: 10.1016/j.eatbeh.2015.06.011.
    1. Barnard N.D., Levin S.M., Yokoyama Y. A systematic review and meta-analysis of changes in body weight in clinical trials of vegetarian diets. J. Acad. Nutr. Diet. 2015;115:954–969. doi: 10.1016/j.jand.2014.11.016.
    1. Huang R.-Y., Huang C.-C., Hu F.B., Chavarro J.E. Vegetarian Diets and Weight Reduction: A Meta-Analysis of Randomized Controlled Trials. J. Gen. Intern. Med. 2016;31:109–116. doi: 10.1007/s11606-015-3390-7.
    1. Yokoyama Y., Levin S.M., Barnard N.D. Association between plant-based diets and plasma lipids: A systematic review and meta-analysis. Nutr. Rev. 2017;75:683–698. doi: 10.1093/nutrit/nux030.
    1. Kahleova H., Levin S., Barnard N. Cardio-Metabolic Benefits of Plant-Based Diets. Nutrients. 2017;9:848. doi: 10.3390/nu9080848.
    1. Page K.A., Reisman T. Interventions to Preserve Beta-Cell Function in the Management and Prevention of Type 2 Diabetes. Curr. Diabetes Rep. 2013;13:252–260. doi: 10.1007/s11892-013-0363-2.
    1. Ismail-Beigi F. Clinical practice. Glycemic management of type 2 diabetes mellitus. N. Engl. J. Med. 2012;366:1319–1327. doi: 10.1056/NEJMcp1013127.
    1. Kahleova H., Matoulek M., Malinska H., Oliyarnik O., Kazdova L., Neskudla T., Skoch A., Hajek M., Hill M., Kahle M., et al. Vegetarian diet improves insulin resistance and oxidative stress markers more than conventional diet in subjects with Type 2 diabetes. Diabet. Med. 2011;28:549–559. doi: 10.1111/j.1464-5491.2010.03209.x.
    1. Kahleova H., Klementova M., Herynek V., Skoch A., Herynek S., Hill M., Mari A., Pelikanova T. The Effect of a Vegetarian vs Conventional Hypocaloric Diabetic Diet on Thigh Adipose Tissue Distribution in Subjects with Type 2 Diabetes: A Randomized Study. J. Am. Coll. Nutr. 2017;36:364–369. doi: 10.1080/07315724.2017.1302367.
    1. Shulman G.I. Ectopic Fat in Insulin Resistance, Dyslipidemia, and Cardiometabolic Disease. [(accessed on 24 October 2017)]; Available online: .
    1. Wajchenberg B.L. β-cell failure in diabetes and preservation by clinical treatment. Endocr. Rev. 2007;28:187–218. doi: 10.1210/10.1210/er.2006-0038.
    1. Vilsbøll T., Holst J.J. Incretins, insulin secretion and Type 2 diabetes mellitus. Diabetologia. 2004;47:357–366. doi: 10.1007/s00125-004-1342-6.
    1. Belinova L., Kahleova H., Malinska H., Topolcan O., Vrzalova J., Oliyarnyk O., Kazdova L., Hill M., Pelikanova T. Differential acute postprandial effects of processed meat and isocaloric vegan meals on the gastrointestinal hormone response in subjects suffering from type 2 diabetes and healthy controls: A randomized crossover study. PLoS ONE. 2014;9:e107561. doi: 10.1371/journal.pone.0107561.
    1. Haghighatdoost F., Bellissimo N., Totosy de Zepetnek J.O., Rouhani M.H. Association of vegetarian diet with inflammatory biomarkers: A systematic review and meta-analysis of observational studies. Public Health Nutr. 2017;20:2713–2721. doi: 10.1017/S1368980017001768.
    1. Gower B.A., Goree L.L., Chandler-Laney P.C., Ellis A.C., Casazza K., Granger W.M. A higher-carbohydrate, lower-fat diet reduces fasting glucose concentration and improves β-cell function in individuals with impaired fasting glucose. Metab. Clin. Exp. 2012;61:358–365. doi: 10.1016/j.metabol.2011.07.011.
    1. Carrasco-Pozo C., Tan K.N., Reyes-Farias M., De La Jara N., Ngo S.T., Garcia-Diaz D.F., Llanos P., Cires M.J., Borges K. The deleterious effect of cholesterol and protection by quercetin on mitochondrial bioenergetics of pancreatic β-cells, glycemic control and inflammation: In vitro and in vivo studies. Redox Biol. 2016;9:229–243. doi: 10.1016/j.redox.2016.08.007.
    1. Xiao J.B., Högger P. Dietary polyphenols and type 2 diabetes: Current insights and future perspectives. Curr. Med. Chem. 2015;22:23–38. doi: 10.2174/0929867321666140706130807.
    1. Yuan C., Spiegelman D., Rimm E.B., Rosner B.A., Stampfer M.J., Barnett J.B., Chavarro J.E., Rood J.C., Harnack L.J., Sampson L.K., et al. Relative Validity of Nutrient Intakes Assessed by Questionnaire, 24-Hour Recalls, and Diet Records Compared With Urinary Recovery and Plasma Concentration Biomarkers: Findings for Women. Am. J. Epidemiol. 2017 doi: 10.1093/aje/kwx328.

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