Human Nutrition and Metabolism Research Communication Barley Bread Containing Lactic Acid Improves Glucose Tolerance at a Subsequent Meal in Healthy Men and Women1
It is possible to alter and optimize the GI features of carbohydrate foods by utilizing different food factors that reduce the rate of glucose delivery to the blood. Some of these food factors are related to characteristics of the raw material, and others to the choice of food process and processing conditions. One food factor capable of modulating the GI is fermentation and/or addition of organic acids. Thus, it has been established that the presence of certain organic acids such as those produced upon sourdough fermentation may reduce postprandial glycemia in healthy subjects (2). The physiologic mechanisms for the acute effects appear to vary; whereas lactic acid lowers the rate of starch digestion in bread (2), acetic and propionic acids appear instead to prolong the gastric emptying rate (3). In addition to the lowering of acute glycemia, a low GI breakfast meal may beneficially affect glycemia and insulinemia at a subsequent standardized lunch in healthy subjects (4 – 6). The suggested cause of this second-meal effect is that a prolonged absorptive phase after breakfast will favor a more efficient suppression of free fatty acids, thus improving insulin sensitivity at the time of the next meal (7). Previous studies in our laboratory showed that low GI foods may differ in their capacity to induce a second-meal effect. Consequently, with a low GI breakfast meal (GI ⫽ 64) consisting of a white wheat bread dressed with vinegar (acetic acid), no lowering of glycemia was seen after the subsequent lunch (5). In contrast, both a spaghetti breakfast (GI ⫽ 52) and a breakfast based on high amylose barley bread and -glucan–rich barley flakes (GI ⫽ 60) reduced glucose and insulin responses after the subsequent lunch meal, compared with a white bread breakfast (5). The present study was designed to evaluate further the potential effect of a low GI breakfast containing organic acids on the glucose tolerance at a subsequent lunch meal, ingested 4 h later. The organic acid tested was lactic acid, which was added to a barley bread at a level corresponding to that produced using a homofermentative starter culture (2).
(Manuscript received 18 December 2001. Initial review completed 12 January 2002. Revision accepted 11 March 2002.) ¨ stman,2 Helena G. M. Liljeberg Elmståhl Elin M. O and Inger M. E. Bjo¨rck Department of Applied Nutrition and Food Chemistry, Center for Chemistry and Chemical Engineering, Lund University, Sweden
ABSTRACT In the present study, we evaluated whether a low glycemic index (GI) breakfast with lactic acid bread had an effect on glucose tolerance and insulinemia at a subsequent high GI lunch meal. A barley bread containing lactic acid and a reference barley bread were consumed in the morning after an overnight fast in random order by 10 healthy men and women. Four hours after the breakfasts, the subjects ate a standardized high GI lunch, and the blood glucose and insulin responses were measured for the next 3 h. Significant lowerings of the incremental glycemic area (ⴚ23%, P ⴝ 0.033) and of the glucose response at 95 min were found after the lunch meal when the barley bread with lactic acid was given as a breakfast. At 45 min after the lunch meal, the insulin level was significantly lower (ⴚ21%, P ⴝ 0.045) after the lactic acid bread breakfast, compared with the barley bread breakfast without lactic acid. We concluded that barley bread containing lactic acid eaten at breakfast has the potential to improve second-meal glucose tolerance at a high GI lunch meal 4 h later. J. Nutr. 132: 1173–1175, 2002. KEY WORDS: ● second-meal tolerance ● glucose response ● insulin response ● glycemic index ● bread
SUBJECTS AND METHODS Bread products. Intact barley kernels without hulls (no. 8775) were provided by Svalo¨f Weibull AB (Svalo¨v, Sweden), and commercial white flour was obtained from Kungso¨rnen AB (Ja¨rna, Sweden). Before baking, the barley kernels were milled to pass through a 0.8-mm screen. Two bread products were made from the same basic recipe with 80% whole-meal barley flour and 20% white wheat flour. One of the bread products was baked with the addition of lactic acid, added in an amount corresponding to that formed during sourdough fermentation. Recipes. The whole-meal bread was prepared by using 3280 g water, 2960 g whole-meal barley flour, 740 g white wheat flour, 200 g yeast, 50 g NaCl, 50 g sucrose and 37 g monoacylglycerols. The dough was proofed for 50 min, divided into pieces of 600 g, and subjected to a second proofing for 20 min (38°C, 75% humidity). Baking was performed at 200°C for 30 min. The bread with lactic acid was baked from the same recipe but with the addition of 81 g lactic acid (the
A diet characterized by low glycemic index (GI) foods has been implemented as an important tool in the prevention and treatment of diseases related to insulin resistance (1). Examples of traditional starchy food products with a low GI are legumes, pasta, certain rice varieties, sourdough bread and bulgur-type products. However, the major carbohydrate sources in the Western diet, i.e., most potato products, common bread and breakfast cereals, are found in the upper GI range. 1 Supported by the Swedish Council for Forestry and Agricultural Research— SJFR (project no. 500615/96). 2 To whom correspondence should be addressed. E-mail:
[email protected].
0022-3166/02 $3.00 © 2002 American Society for Nutritional Sciences.
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lactic acid solution added was 72 g/100 g). The water content of the dough was corrected for the amount of added lactic acid solution. Chemical analysis. A portion of each bread was dried and milled (Cyclotech, Tecator, Sweden) before analysis. The products were analyzed for starch as described previously (8). Protein (Kjeldahl analysis) and fat (9) were also determined. The composition of the bread products was as follows (dry weight basis): both bread products contained 126 g/kg protein and 42 g/kg fat, whereas the bread without lactic acid had a starch content of 642 g/kg and the lactic acid bread contained 630 g/kg starch. The pH was 5.8 for the bread without lactic acid and 3.9 in the bread with added lactic acid (0.17 mol/kg). Breakfast meals. The barley breads, one with and one without lactic acid, were tested as breakfast meals in healthy subjects. Butter (80% fat) and cheese (10% fat) were served with both test meals, as well as 250 mL of water and 150 mL of tea or coffee. Both test meals contained 50 g available starch, 15 g protein and 12 g fat, providing 1549 kJ (369 kcal). The subjects were served the test meals in random order on two separate occasions, at the same time in the morning, after an overnight fast. All meals were consumed steadily over a 12to 14-min period. The postprandial blood glucose and insulin responses to the whole-meal barley bread breakfasts did not arise from this study, but were determined in a previous work with 12 healthy subjects (8). Data from the previous breakfast study have been included in Table 1. Standardized lunch meal. Four hours after the breakfast meals, the subjects were served a second meal in the form of a standardized high GI lunch. The lunch meal consisted of 100 g commercially available fried and deep-frozen meatballs (ICA Handlarna, Sweden), mashed potatoes (instant potato powder from Felix, Eslo¨ v, Sweden) and 60 g canned sweet corn (Erasco, Lu¨ beck, Germany). The meatballs were heated in a microwave oven for 2.5 min at 460 W, and the instant potato powder (55 g) was reconstituted with 250 mL water before being served. In addition, 250 mL water and 150 mL coffee or tea was served with each meal. The lunch meal was consumed steadily over 12–15 min. Subjects. Ten healthy nonsmoking volunteers, 2 men and 8 women, aged 23–52 y, with normal body mass indices (21.5 ⫾ 0.6, in kg/m2) and without drug therapy participated in the study. The study was performed over a period of 2 mo and all subjects were aware of the
TABLE 1 Acute postprandial blood glucose and serum insulin areas under the response curves after a standardized lunch meal following two different barley bread breakfasts After breakfast1 Area
Glucose WMB4 ⫹Lac
Insulin WMB ⫹Lac
FIGURE 1 Blood glucose responses in 10 healthy subjects immediately before and after a standardized lunch meal, served 4 h after breakfasts of barley bread with or without lactic acid. Values are means ⫾ SEM, n ⫽ 10; those with different letters differ, P ⬍ 0.05.
possibility of withdrawing from the study at any time. The Ethics Committee of the Faculty of Medicine at Lund University, Sweden gave approval of the study. Blood analyses. Capillary blood samples were taken before the breakfast meal for determination of the fasting blood glucose and insulin. Further, blood samples were taken immediately before the lunch meal (0 min, i.e., 4 h postbreakfast), and at 15, 30, 45, 70, 95, 120 and 180 min after lunch for analysis of glucose. Serum insulin was determined before (0) and at 15, 30, 45, 95 and 120 min after lunch. The blood glucose concentration was determined with a glucose oxidase peroxidase reagent and serum insulin levels with an enzyme immunoassay kit (Boehringer Mannheim GmBH, Germany). Statistical methods. For each subject and test meal, the glucose and insulin areas under the curves were calculated (GraphPad Prism, version 3.0; Graph Pad Software, San Diego, CA). All areas below baseline were excluded from the calculations. Values are presented as means ⫾ SEM and all statistical calculations were performed in MINTAB Statistical Software (release 13 for Windows; Minitab, State College, PA). Significance was evaluated with the general linear model (ANOVA), followed by Tukey’s multiple comparisons test. Values of P ⬍ 0.05 were considered significant.
RESULTS
After lunch meal2
0–95 min
⌬3
0–95 min
⌬
mmol/L 䡠 min
%
mmol/L 䡠 min
%
117.8 ⫾ 19.0 87.3 ⫾ 17.2*
100 74
171.0 ⫾ 23.0 131.8 ⫾ 15.1*
100 77
nmol/L 䡠 min
%
nmol/L 䡠 min
21.3 ⫾ 3.7 16.1 ⫾ 2.4*
100 76
16.9 ⫾ 1.6 15.1 ⫾ 1.0
100 89
1 Values are means ⫾ SEM; n ⫽ 12. Results from a previous study (8). * Different from the corresponding value of the reference product (whole-meal bread), P ⬍ 0.05. 2 Values are means ⫾ SEM; n ⫽ 10. * Different from the corresponding value of the reference product (whole-meal bread), P ⬍ 0.05. 3 Postprandial blood glucose and serum insulin area (0 –95 min), respectively, as a percentage of the reference value (whole-meal bread). 4 WMB, whole-meal barley bread (reference product); Lac, lactic acid.
The fasting blood glucose and insulin levels were in the normal range, and did not differ significantly before the test and the reference breakfasts. There were no differences in fasting blood glucose levels or blood glucose levels immediately before the lunch meal, i.e., 4 h after commencing the breakfast. The blood glucose and insulin levels immediately before and after the standardized lunch meal after the test and reference breakfasts, respectively, are shown in Figures 1 and 2. Significantly lower blood glucose levels (P ⬍ 0.05) were registered at 30 and 45 min after the lunch meal after the lactic acid– containing test breakfast, compared with the reference breakfast (Fig. 1). The area under the glucose curve was significantly lower at 95 min after lunch (P ⬍ 0.05) after the barley bread breakfast with lactic acid, compared with the corresponding area after the reference breakfast (Table 1). At 45 min after the lunch, the insulin response after the lactic acid bread breakfast was significantly lower than the response after the reference bread breakfast (Fig. 2). However, there were no differences between the insulin areas under the curve (0 –95 min) after the lunch, irrespective of the type of barley bread breakfast (Table 1).
LACTIC ACID IMPROVES GLUCOSE TOLERANCE
FIGURE 2 Serum insulin responses in 10 healthy subjects immediately before and after a standardized lunch meal, served 4 h after breakfasts of barley bread with or without lactic acid. Values are means ⫾ SEM, n ⫽ 10; those with different letters differ, P ⬍ 0.05.
DISCUSSION The present study clearly shows the potential of lactic acid as a tool for improving second-meal glycemia. In a previous study, it was hypothesized that a late net increment in postprandial glycemia after breakfast favored a reduction in metabolic response after lunch (5). In the present study, there was no indication of a difference in either blood glucose or insulin 4 h after the two different barley breakfasts. Because we did not measure the glucose and insulin concentrations between the breakfast and lunch meals, we cannot exclude the possibility that there could have been a difference in glycemia and insulinemia in the late postprandial phase after breakfast. It is important to acknowledge the variation in secondmeal glycemic features also between foods with similar and low GI properties. Consequently, an acetic acid– containing bread meal with a GI of 64 did not improve the second-meal glucose tolerance (5), whereas in the present study, the barley bread containing lactic acid with a somewhat higher GI (⬃74), did. These differences could arise because different gastrointestinal events are responsible for the lower GI. According to Wolever et al. (7), a prolonged digestive phase induces a prolonged suppression of plasma fatty acids, which has been shown to be associated with improved insulin action. The second-meal effect of the lactic acid barley bread in this study might be explained by this mechanism, whereas the lack of a secondmeal effect after the acetic acid– containing breakfast might be explained by the fact that in this case, the mechanism responsible for the lower GI is a delayed gastric emptying rate rather than a prolonged starch digestion (3). Another mechanism discussed in relation to the long-term metabolic effects of a low GI diet is the formation of short-
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chain fatty acids (SCFA) from fermentation of indigestible carbohydrates in the colon (10). Considering the relatively short time (4 h) between the breakfast and lunch meals, it is not likely that the formation of SCFA had started and was involved in the improvement of glucose metabolism after lunch. However, once formed, the SCFA have immediate effects on gastric motility (11). We conclude that barley bread supplemented with a realistic amount of lactic acid has the potential to improve second-meal glucose tolerance in healthy subjects. As shown and discussed by Liljeberg et al. (2), there is no reason to believe that the addition of lactic acid to a bread would affect the acute glycemia differently than lactic acid produced upon sourdough fermentation. No previous data are available concerning the second-meal effect of a sourdough fermented bread; thus it cannot be excluded that the generation of lactic acid through fermentation might affect the nonstarch polysaccharides differently than an addition of lactic acid. Further studies are required to evaluate the second-meal effect of a sourdough fermented bread and to establish potential long-term metabolic merits of cereal products containing lactic acid or other organic acids. LITERATURE CITED 1. FAO/WHO (1998) Carbohydrates in human nutrition: report of a joint FAO/WHO expert consultation. FAO Food and Nutrition Paper 66, pp.1–140. WHO, Geneva, Switzerland. 2. Liljeberg, H.G.M., Lo¨ nner, C. H. & Bjo¨ rck, I.M.E. (1995) Sourdough fermentation or addition of organic acids or corresponding salts to bread improves nutritional properties of starch in healthy humans. J. Nutr. 125: 1503– 1511. 3. Liljeberg, H.G.M. & Bjo¨ rck, I.M.E. (1998) Delayed gastric emptying rate may explain improved glycaemia in healthy subjects to a starchy meal with added vinegar. Eur. J. Clin. Nutr. 52: 368 –371. 4. Jenkins, D.J.A., Wolever, T.M.S., Taylor, R. H., Griffiths, C., Krzeminska, K., Lawrie, J. A., Bennett, C. M., Geoff, D. V., Sarson, D. L. & Bloom, S. R. (1982) Slow release dietary carbohydrate improves second meal tolerance. Am. J. Clin. Nutr. 35: 1339 –1346. 5. Liljeberg, H.G.M., Åkerberg, A.K.E. & Bjo¨rck, I.M.E. (1999) Effect of the glycemic index and content of indigestible carbohydrates of cereal-based breakfast meals on glucose tolerance at lunch in healthy subjects. Am. J. Clin. Nutr. 69: 647– 655. 6. Liljeberg, H.G.M. & Bjo¨rck, I.M.E. (2000) Effects of a low-glycaemic index spaghetti meal on glucose tolerance and lipaemia at a subsequent meal in healthy subjects. Eur. J. Clin. Nutr. 54: 24 –28. 7. Wolever, T.M.S., Bentum-Williams, A. & Jenkins, D.J.A. (1995) Physiological modulation of plasma free fatty-acid concentration by diet. Diabetes Care 18: 962–970. 8. Liljeberg, H.G.M. & Bjo¨rck, I.M.E. (1996) Delayed gastric emptying rate as a potential mechanism for lowered glycemia after eating sourdough bread: studies in humans and rats using test products with added organic acids or an organic salt. Am. J. Clin. Nutr. 64: 883– 893. 9. Lange, H. J. (1972) Fettbestimmung. (Fat analysis). In Untersuchungsmethoden in der Konservenindustrie (Analysis Methods in the Canning Industry) (Lange, H. J., ed.) pp. 211–213. Paul Parey, Berlin, Germany. 10. Thorburn, A., Muir, J. & Proitto, J. (1993) Carbohydrate fermentation lowers hepatic glucose output in healthy subjects. Metabolism 42: 780 –785. 11. Ropert, A., Cherbut, C., Roze´, C., Quellec, A. L., Holst, J. J., Fu-Cheng, X., Varannes, S.B.D. & Galmiche, J. P. (1996) Colonic fermentation and proximal gastric tone in humans. Gastroenterology 111: 289 –296.
