OBJECTIVE
To evaluate the effect of a prebreakfast high-protein snack upon postbreakfast hyperglycemia.

RESEARCH DESIGN AND METHODS
We studied 10 men and women with diet- and/or metformin-controlled type 2 diabetes. Metabolic changes after breakfast were compared between 2 days: breakfast taken only and soya-yogurt snack taken prior to breakfast.

RESULTS
There was a significant lower rise in plasma glucose on the snack day. The incremental area under the glucose curve was 450 ± 55 mmol · min/l on the snack day compared with 699 ± 99 mmol · min/l on the control day (P = 0.013). The concentration of plasma free fatty acids immediately before breakfast correlated with the increment in plasma glucose (r = 0.50, P = 0.013).

CONCLUSIONS
Consuming a high-protein prebreakfast snack results in almost 40% reduction of postprandial glucose increment. The second-meal effect can be applied simply and practically to improve postbreakfast hyperglycemia in people with type 2 diabetes

Chen, M.

Jovanovic, A.

Taylor, R.

English

Canterbury Research and Theses Environment

Utilizing the Second-Meal Effect in Type 2Diabetes: Practical Use of a Soya-YogurtSnackMEI JUN CHEN, BSCANA JOVANOVIC, MDROY TAYLOR, MDOBJECTIVE — To evaluate the effect of a prebreakfast high-protein snack upon postbreakfasthyperglycemia.RESEARCH DESIGN AND METHODS — We studied 10 men and women with diet-and/or metformin-controlled type 2 diabetes. Metabolic changes after breakfast were comparedbetween 2 days: breakfast taken only and soya-yogurt snack taken prior to breakfast.RESULTS — There was a significant lower rise in plasma glucose on the snack day. Theincremental area under the glucose curve was 450  55 mmol  min/l on the snack day comparedwith 699  99 mmol  min/l on the control day (P  0.013). The concentration of plasma freefatty acids immediately before breakfast correlated with the increment in plasma glucose (r 0.50, P  0.013).CONCLUSIONS — Consuming a high-protein prebreakfast snack results in almost 40%reduction of postprandial glucose increment. The second-meal effect can be applied simply andpractically to improve postbreakfast hyperglycemia in people with type 2 diabetes.Diabetes Care 33:2552–2554, 2010P revious studies (1,2) have shown aconsiderable reduction in hypergly-cemia after the second meal of theday, provided that breakfast had beentaken. The preservation of this effect intype 2 diabetes was not confirmed untilrecently (3). Postprandial hyperglyce-mia acts as an independent risk factorfor cardiovascular disease (4 – 6), a ma-jor cause of death in subjects with type 2diabetes (7).We hypothesized that postbreakfasthyperglycemia in subjects with type 2 di-abetes could be improved nonpharmaco-logically by using a high-protein, low-carbohydrate prebreakfast snack.RESEARCH DESIGN ANDMETHODS — Ten subjects (four fe-male, six male) with type 2 diabetestreated by diet and/or metformin were re-cruited (aged 61  2.3 years, waist-to-hipratio 0.96  0.01, BMI 28.8  1.0 kg/m2,body fat 33.4  2.6%, and A1C 6.7 0.1%). The Newcastle and North Tyne-side Research Ethics Committee No. 2 ap-proved the study. All participants gavewritten informed consent.Design and protocolEvery subject was studied on 2 separatedays in random order with 2–4 week in-tervals. On both days, breakfast (51 g car-bohydrate; 4.8 g fat; 5.8 g protein) wasgiven at 10:00 A.M. On the snack day only,a snack (30 g soya beans; 75 g yogurt) wasgiven 2 h before the breakfast. The detailsof metabolic testing, hormone, and me-tabolites assays were as previously de-scribed (3,8).Statistical analysisData are expressed as means  SEM.Paired Student t test was performed bySPSS (version 17.0; SPSS, Chicago). In-cremental area under the curve (IAUC)was computed by the trapezoidal rule.RESULTSPlasma glucoseAt baseline, 2 h before breakfast, fastingplasma glucose was similar on the 2 studydays (6.6  0.3 and 6.6  0.4 mmol/l).The snack induced a small peak in plasmaglucose at 60 min (7.3  0.4 mmol/l).The concentrations of plasma glucose im-mediately before breakfast (t  0 min) didnot differ significantly between the 2 days(6.6  0.3 vs. 6.4  0.3 mmol/l, P 0.45) (Fig. 1A).Following breakfast, the rise inplasma glucose was lower on the snackday. IAUC was 450  55 mmol  min/lcompared with 699  99 mmol  min/l forsnack and control day, respectively (P 0.013) (Fig. 1B). The 2-h postprandialplasma glucose concentration was signif-icantly lower on the snack day comparedwith the control day (9.8  0.3 vs. 10.8 0.4 mmol/l, P  0.001). Plasma glucoselevels were identical in the two groups 5 hafter breakfast.Plasma free fatty acidThe fasting plasma free fatty acid (FFA)concentrations on both study days weresimilar (0.57  0.05 and 0.57  0.04mmol/l, P  0.9). After ingestion of thesnack, plasma FFA concentration de-clined, falling to 70% of the fasting levelsjust before breakfast (0.41  0.04 mmol/l). After breakfast, plasma FFA levels inboth groups were suppressed (0.16 0.02 vs. 0.14  0.02 mmol/l for snackand control days, respectively) (Fig. 1C).FFA concentration before breakfast waspositively correlated with the postpran-dial IAUC for plasma glucose (r  0.50,P  0.013).Serum insulin and C-peptideFasting mean serum insulin levels weresimilar on the 2 study days (13.4  2.4and 13.2  2.7 mU/l). On the snack day,● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ●From the Newcastle Magnetic Resonance Centre, Campus for Ageing and Vitality, Newcastle University,Newcastle upon Tyne, U.K.Corresponding author: Roy Taylor, roy.taylor@newcastle.ac.uk.Received 25 March 2010 and accepted 7 July 2010.M.J.C. and A.J. contributed equally to this study.DOI: 10.2337/dc10-0552© 2010 by the American Diabetes Association. Readers may use this article as long as the work is properlycited, the use is educational and not for profit, and the work is not altered. See http://creativecommons.org/licenses/by-nc-nd/3.0/ for details.The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be herebymarked “advertisement” in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.See accompanying editorial, p. 2709.C l i n i c a l C a r e / E d u c a t i o n / N u t r i t i o n / P s y c h o s o c i a l R e s e a r c hB R I E F R E P O R T2552 DIABETES CARE, VOLUME 33, NUMBER 12, DECEMBER 2010 care.diabetesjournals.orgDownloaded from http://diabetesjournals.org/care/article-pdf/33/12/2552/605543/zdc01210002552.pdf by Canterbury Christ Church University user on 16 April 2024insulin concentration rose promptly afteringestion of the snack to 26.5  4.0 mU/lat 60 min and fell before breakfast (Fig.1D). Following breakfast, insulin levelsincreased similarly on both days (58.5 7.9 vs. 51.2  7.6 mU/l) at 60 min. Themean insulin-to-C–peptide ratios fromthe area under the curves (t  0–5 h)were similar on both days (13.6  3.2 vs.16. 9  1.4 mU/nmol, P  0.36) imply-ing similar hepatic insulin extraction.Substrate oxidationFasting glucose oxidation rates were notsignificantly different on the 2 study days(0.55  0.18 vs. 0.77  0.25 mg/kg min, P  0.37). On the snack day, glucoseoxidation rate increased to 1.38  0.24mg/kg  min at 90 min after breakfastcompared with 1.09  0.25 mg/kg  minon the control day (P  0.11). Fastinglipid oxidation rates were similar (0.7 0.1 vs. 0.63  0.12 mg/kg  min) and 90min after breakfast decreased to 0.39 0.09 vs. 0.51  0.09 mg/kg  min, respec-tively (P  0.09).CONCLUSIONS — This study dem-onstrated for the first time that the provi-sion of a practical, high-protein, low-carbohydrate snack prior to breakfastreduced by 40% the postprandial plasmaglucose increment in people with type 2diabetes. These findings confirm a potentexpression of the second-meal effect inpeople with type 2 diabetes similar to thatresulting from intravenous arginine infu-sion (3). The importance of the presentobservation is that a more practical meansof improving glucose tolerance could po-tentially be of therapeutic benefit in peo-ple with type 2 diabetes.We observed no effect of the priorsnack on insulin secretion after breakfast.The mechanism underlying the second-meal effect has been shown to be due tosuppression of plasma FFA, allowinggreater storage of glucose as muscle gly-cogen (2). We previously demonstrated astrong negative correlation between thedecrease of preprandial plasma FFA levelsand the postmeal glucose increment. Inthe present study, a significant positivecorrelation was found between prebreak-fast plasma FFA and the rise in postpran-dial plasma glucose concentration. Thisobservation is analogous to the acute ef-fect of the antilipolytic nicotinic acid an-alog acipimox (9).The snack used in the present studywas empirically designed. It will be im-portant to optimize both the compositionof the snack and the interval before break-fast to maximize the benefit of this ap-proach. In everyday life, the gap betweensnack and breakfast would have to be ac-Figure 1—Metabolic changes between the 2 study days in 10 subjects with type 2 diabetes. A: Plasma glucose concentrations. B: Incremental areaunder the plasma glucose curves during the 5-h postbreakfast period. C and D: Change in FFA and insulin concentrations, respectively. *P  0.05;**P  0.02; ***P  0.01; , snack day; F, control day.Chen, Jovanovic, and Taylorcare.diabetesjournals.org DIABETES CARE, VOLUME 33, NUMBER 12, DECEMBER 2010 2553Downloaded from http://diabetesjournals.org/care/article-pdf/33/12/2552/605543/zdc01210002552.pdf by Canterbury Christ Church University user on 16 April 2024commodated, for instance, by delayingbreakfast until mid-morning. Althoughthe snack induced a small increase inplasma glucose, it was minimal and un-likely to contribute to the hyperglycemicburden. The sample size was dictated byprior power calculation (80% power with10 subjects).We have demonstrated that a high-protein, low-carbohydrate snack beforebreakfast attenuates postbreakfast hyper-glycemia, and further studies must deter-mine whether long-term use is associatedwith improvement in A1C.Acknowledgments— This work was sup-ported by Wellcome Trust Grant 073561 andthe Newcastle National Institute for Health Re-search Biomedical Research Centre in Ageing.No potential conflicts of interest relevant tothis article were reported.M.J.C. conducted the study, researchedthe data, and drafted the manuscript. A.J.designed the study and revised the manu-script. R.T. conceived the overall researchquestion, researched the data, and revisedthe manuscript.We thank Heather Cook of the Institute ofCellular Medicine, Newcastle University, forlaboratory expertise; Jean Gerrard and Dr. EeLin Lim, both of the Institute of Cellular Med-icine, Newcastle University, for clinical re-search support; and the volunteers for theirtime and cooperation.References1. Carey PE, Halliday J, Snaar JE, Morris PG,Taylor R. Direct assessment of muscle gly-cogen storage after mixed meals in normaland type 2 diabetic subjects. Am J PhysiolEndocrinol Metab 2003;284:E688–E6942. Jovanovic A, Leverton E, Solanky B, Ravi-kumar B, Snaar JE, Morris PG, Taylor R.The second-meal phenomenon is associ-ated with enhanced muscle glycogen stor-age in humans. Clin Sci 2009;117:119–1273. Jovanovic A, Gerrard J, Taylor R. The sec-ond-meal phenomenon in type 2 diabe-tes. Diabetes Care 2009;32:1199–12014. de Vegt F, Dekker JM, Ruhé HG, Stehou-wer CD, Nijpels G, Bouter LM, HeineRJ. Hyperglycaemia is associated with all-cause and cardiovascular mortality in theHoorn population: the Hoorn Study. Dia-betologia 1999;42:926–9315. The DECODE Study Group on behalf ofthe European Diabetes EpidemiologyGroup. Glucose tolerance and mortality:comparison of WHO and American Dia-betes Association diagnostic criteria. Lan-cet 1999;354:617–6216. Meigs JB, Nathan DM, D’Agostino RBSr, Wilson PW, Framingham OffspringStudy. Fasting and postchallenge glyce-mia and cardiovascular disease risk: theFramingham Offspring Study. DiabetesCare 2002;25:1845–18507. Laakso M. Hyperglycemia and cardiovas-cular disease in type 2 diabetes. Diabetes1999;48:937–9428. Carey PE, Gerrard J, Cline GW, DallaMan C, English PT, Firbank MJ, CobelliC, Taylor R. Acute inhibition of lipolysisdoes not affect postprandial suppres-sion of endogenous glucose production.Am J Physiol Endocrinol Metab 2005;289:E941–E9479. Vaag A, Skött P, Damsbo P, Gall MA,Richter EA, Beck-Nielsen H. Effect of theantilipolytic nicotinic acid analogue acipi-mox on whole-body and skeletal muscleglucose metabolism in patients withnon-insulin-dependent diabetes mellitus.J Clin Invest 1991;88:1282–1290Second-meal effect as therapy2554 DIABETES CARE, VOLUME 33, NUMBER 12, DECEMBER 2010 care.diabetesjournals.orgDownloaded from http://diabetesjournals.org/care/article-pdf/33/12/2552/605543/zdc01210002552.pdf by Canterbury Christ Church University user on 16 April 2024

Utilizing the second-meal effect in type 2 diabetes: practical use of a soya-yogurt snack

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Utilizing the second-meal effect in type 2 diabetes: practical use of a soya-yogurt snack

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