Original Communication

European Journal of Clinical Nutrition (2003) 57, 1254–1261. doi:10.1038/sj.ejcn.1601680

Lower glucose-dependent insulinotropic polypeptide (GIP) response but similar glucagon-like peptide 1 (GLP-1), glycaemic, and insulinaemic response to ancient wheat compared to modern wheat depends on processing

S Bakhøj1, A Flint1, J J Holst2 and I Tetens1

  1. 1From The Research Department of Human Nutrition, The Royal Veterinary and Agricultural University, Frederiksberg, Denmark
  2. 2The Department of Medical Physiology, The Panum Institute, University of Copenhagen, Denmark

Correspondence: I Tetens, Research Department of Human Nutrition, The Royal Veterinary & Agricultural University, Rolighedsvej 30, DK-1958 Frederiksberg C, Denmark. E-mail: ite@kvl.dk.

Guarantor: I Tetens.

Contributors: SB codeveloped the study design and was involved in subject recruitment, data collection, statistical analysis and drafted the first manuscript. AF codeveloped the study design, was involved in data collection and the statistical analyses and commented on the first draft of the paper. JJH codeveloped the study design, was involved in the analysis of the gut hormones and commented on the first draft of the paper. IT conceived the idea of the study, codeveloped it into a project. IT was involved in the data collection, writing the first draft and corefined it into the final draft. All contributors participated in the development of the paper.

Received 21 December 2001; Revised 15 August 2002; Accepted 24 September 2002.

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Abstract

Objective: To test the hypothesis that bread made from the ancient wheat Einkorn (Triticum monococcum) reduces the insulin and glucose responses through modulation of the gastrointestinal responses of glucose-dependent insulinotrophic polypeptide (GIP) and glucagon-like peptide 1 (GLP-1) compared to the responses to bread of modern wheat (Triticum aestivum).

Design: The 3-h postprandial insulinaemic, glycaemic, GIP, and GLP-1 responses to bread made from Einkorn were compared to responses to a traditional Danish wheat loaf. The bread from Einkorn was prepared by 3 different processing methods: leavening with honey–salt added, leavening crushed whole grain, and conventional leavening with yeast added. Bread made from modern wheat was prepared by conventional leavening with yeast added.

Subjects: A total of 11 healthy young men.

Results: The postprandial GIP response was significantly (P<0.001) reduced by the Einkorn breads processed with honey–salt leavening and by using crushed whole grain bread compared to the yeast leavened bread made from modern wheat or from Einkorn. No significant differences were found in the responses of GLP-1, insulin or glucose.

Conclusion: Einkorn honey–salt leavened and Einkorn whole grain bread elicit a reduced gastrointestinal response of GIP compared to conventional yeast bread. No differences were found in the glycaemic, insulinaemic and GLP-1 responses. Processing of starchy foods such as wheat may be a powerful tool to modify the postprandial GIP response.

Sponsorship: The Directorate for Food, Fisheries and Agri Business, the Danish Ministry of Food, Agriculture and Fisheries and Agronomic Businesses.

Keywords:

incretin hormones, insulin, glucose, rapidly available glucose (RAG), einkorn (Triticum aestivum), wheat (Triticum monococcum)

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Introduction

The incretin hormones glucose-dependent insulinotrophic polypeptide (GIP) and glucagon-like peptide 1 (GLP-1) are responsible for the insulinotropic effect induced by food intake (Holst, 1997). The potential role of GLP-1 in the regulation of appetite and food intake (Flint et al, 1998; Gutzwiller et al, 1999) and the potential role of GLP-1 and GIP of lipid metabolism (Thomsen et al, 1999) have been investigated recently. A positive correlation between the postprandial GIP response and the subjective satiety sensation was observed in healthy normal weight subjects (Raben et al, 1996). One mechanism to explain this effect could be that the presence of rapidly available starch in the small intestine acts as a stimulus on GIP-secreting cells in the duodenum and proximal jejunum. A recent study confirmed this mechanism by showing that intraduodenal glucose infusion resulted in significantly increased levels of plasma GIP and GLP-1 concentrations compared with intraduodenal infusion of saline in healthy individuals (Lavin et al, 1998). A specific physiological role of GIP on the metabolism of adipose tissues has been suggested. Thus, GIP has been reported to have a specific anabolic effect on adipose tissue by stimulating fatty acid synthesis and enhancing insulin-stimulated incorporation of fatty acids into tryglycerides (Yip & Wolfe, 2000). The effect of GIP in promoting the accumulation of fat in adipose tissues was confirmed recently in rats (Miyawaki et al, 2001).

High glycaemic and insulinaemic responses are extensively discussed as an important risk factor for development of metabolic syndromes, including the affluent diseases diabetes, atherosclerosis and obesity (Björck et al, 2000). Constant exposure to high plasma glucose concentrations and the consequently high insulin levels may lead to insulin resistance (Daly et al, 1997). On this basis, it is recommended that large amounts of rapidly digestible carbohydrates in the diet be avoided (FAO/WHO, 1998). A lowering of the glucose response, which follows the intake of slowly digestible foods, provides a comparatively lower insulin response, and may thus improve metabolic parameters in diabetic, obese or hyperlipidemic patients (Liljeberg & Björck, 1994; Buyken et al, 2001). Rather than excluding carbohydrates, the use of low glycaemic index (GI) products in the diet should be advocated.

White wheat bread is one of the most important sources of carbohydrates in the Western diet (Holt et al, 1992), and various attempts have been made to reduce the glycaemic and insulinaemic responses to wheat bread (Liljeberg & Björck, 1994). Methods of slowing the rate of carbohydrate digestion and absorption from bread involve use of intact whole grains, use of additional dietary fibre or use of alternative cereal sources (Rasmussen et al, 1991; Holt et al, 1992; Brand Miller et al, 1992). Also, the use of different processing methods such as sourdough leavening has shown to be promising ways of decreasing GI of cereal foods (Liljeberg & Björck, 1996).

Anecdotally, bread made from the ancient wheat variety Einkorn (Triticum monococcum) has been postulated to have different nutritional and sensoric qualities, and to produce different appetite sensations than modern wheat varieties (Triticum aestivum). However, there is no scientific evidence to support these claims. Comparing the physicochemical characteristics of Einkorn and modern wheat, Einkorn generally has a higher content of protein, lysine, ash, and carotenoids (Vallega, 1992; D'Egidio et al, 1993; Abdel-Aal et al, 1997). The starch granules of Einkorn are smaller than those of modem wheat, and the cell walls are relatively soft. These physicochemical properties may therefore require use of alternative processing methods for making bread from Einkorn.

The aim of the present study was therefore to test the hypothesis that gastrointestinal responses of GIP and GLP-1, and insulinaemic and glycaemic responses were significantly reduced in healthy subjects after ingestion of bread made from ancient wheat Einkorn (Triticum monococcum) compared to bread made from modern wheat. A specific objective included comparison of the gastrointestinal responses to different processing methods relevant for production of bread from Einkorn.

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Subjects and methods

Subjects

The participants comprised 11 healthy male adults (mean plusminuss.d.: age 25plusminus2 y, BMI 23plusminus4 kg/m2) recruited from universities in Copenhagen. None of the participants took any medication regularly and all were nonsmokers. Physical activity levels and eating habits on the day before the test day were standardized for each volunteer and the participants were fasted for 10 h prior to the test. The study was approved by the Ethics Committee of Copenhagen and Frederiksberg (Journal no. KF 01-198/99).

Bread products

Four different test breads were produced for the study: three made from Einkorn and one from modem wheat. The three Einkorn breads comprised (1) honey–salt leavened bread made by mixing whole grain flour and water, adding honey and salt, raising for 17 h and baking at 150°C for 5 h, (2) crushed whole grain bread produced by soaking the grains for 12 h in tap water, grinding the whole grains, raising for 2 h, and baking for 21/2 h at 150°C; and (3) yeast leavened bread using a conventional bread production procedure of mixing flour, salt and water, adding bakers yeast, raising for 1 h and baking for 2 h at 220°C. This latter processing procedure was also used for making the modern wheat bread, which was included as a reference bread. Einkorn was obtained from Svanholm, Denmark and was a mix of the varieties French dehulled and Gamlein plus and the bread was manufactured at Aurion Bakery, Hjørring, Denmark. The reference wheat flour was obtained from Valsemøllen, Esbjerg, Denmark and comprised the varieties Dragon, Alidos, Hereward and Rialto. The content of energy, carbohydrates, protein, and fat of the four breads was calculated using the Danish food tables (National Food Agency, 1996) and data obtained from the Biotechnological Institute, Kolding, Denmark. The content of dry matter, rapidly available glucose (RAG) and dietary fibre were measured in our laboratory (see below).

Test meals

The test meals were taken after a 10 h overnight fast. The four different breads were served in portions of 50 g of available carbohydrates, corresponding to served portions of 127, 129, 127, and 118 g for Einkorn honey–salt, Einkorn crushed whole grain, Einkorn yeast and modern wheat yeast bread (reference), respectively. The bread was served together with 250 ml of tap water. The subjects were instructed to consume the meal within 10 min.

Experimental protocol

The participants were divided into four groups of three people, participating once a week on the same weekday, for four consecutive weeks. The test meals were served in random order, serving each test meal once to each participant. On arrival, the participants were weighed in light clothing and without shoes before an intracatheter (Venflon72, ø1, 4/45 mm, BOC Ohmeda, Sweden) was placed in an antecubital vein. Blood samples for glucose and insulin measurements were taken 15 and 0 min prior to the test meal, and again at 15, 30, 45, 60, 90, 120, and 180 min after the test meal. Blood samples for GLP-1 and GIP measurements were collected at 0, 30, 60, 90, 120, and 180 min after ingestion of the test meal. After centrifugation, plasma and serum was kept frozen at -20°C until further analysis.

Analysis

The plasma glucose was measured by a standard glucose oxidase method using a Roche Cobas Mira. Serum insulin concentrations were measured against standards of human insulin by radioimmunoassay as described by Flint et al, (1998). GIP and GLP-1 concentrations in plasma were measured using specific radioimmunoassays after extraction of plasma with 70% ethanol (vol/vol, final concentration). For the GIP assay we used the C-terminally directed antiserum R 65, which crossreacts fully with human GIP, but not with GIP 8000, whose chemical nature and relation to GIP secretion is uncertain (Krarup et al, 1983). Human GIP and 125-I human GIP (70 MBq/nmol) were used for standards and tracer. The GLP-1 concentrations were measured against standards of synthetic GLP-1 7-36 amide using antiserum code no. 89390, which is specific for the amidated C-terminus of GLP-1 and therefore mainly reacts with GLP-1 of intestinal origin (Ørskov et al, 1994). For both assays sensitivity was below 1 pmol/l, intrassay coefficient of variation below 6% at 20 pmol/l, and recovery of standard, added to plasma before extraction, was about 100% when corrected for losses inherent in the plasma extraction procedure.

Measurements of rapidly available glucose (RAG) followed the method described by Englyst et al (1999). Triplicate samples of approximately 1.0 g of bread were used for the analysis with duplicates of 0.8 g wheat flour (Englyst starch kit prod. no. 61-008) used as external standard. RAG, defined as the total amount of glucose in the sample after 20 min of enzymatic hydrolysis, was determined as the sum of separate measurements of free glucose and glucose released from starch after 20 min of enzymatic hydrolysis.

Dry matter was determined in triplicates by oven drying at 100°C for 24 h. The pH value was measured in the Einkorn honey–salt dough using a dough pH-meter (Mettler DL 21, Struers Kebo Lab A/S, Albertslund, Denmark) before and after the 17 h of rising. Nonstarch polysaccharides (NSP) were determined in duplicates as alditol acetates by gas–liquid chromatography and Klason lignin was determined gravimetrically (Bach Knudsen, 1997). Total dietary fibre was calculated as the sum of these components.

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Calculations

Postprandial response curves of the concentration of GIP, GLP-1, insulin, and glucose vs time were constructed to compare the physiological responses to the four breads. The fasting level, peak value, and time to peak were calculated as the average value of the 11 volunteers. A single sample was obtained to determine the fasting level of GIP and GLP-1, whereas the fasting levels of glucose and insulin were calculated as the average of the two blood samples taken before ingestion of the test meals at time -15 and 0 min, respectively. Values of incremental area under the curve (iAUC value) were calculated using the trapezoidal rule (Wolever & Jenkins, 1986). The average fasting level was used as baseline (zero value) and only values above the fasting level were included in the calculation. The calculation of the indexes (GIP, GLP-1, insulinaemic, and glycaemic) followed the equation

Unfortunately we are unable to provide accessible alternative text for this. If you require assistance to access this image, please contact help@nature.com or the author

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Statistical analysis

All results in tables are given as means plusminus s.d. The level of significance was set at P<0.05. The response curves were analysed by an ANOVA using mixed linear models with repeated measurements in SAS®System for Windows (release 6.12, SAS Institute Inc., Cary, NC, USA, 1998). The covariance structure used was spatial power, which is an autoregressive structure where the actual difference in time between two observations is taken into account. The summary statistics (iAUC, indices, peak, time to peak) were analysed using an analysis of covariance (ANCOVA) with three factors in PROC GLM in the SAS®System. The average fasting levels of glucose, insulin, GIP, and GLP-1, respectively, were used as covariate in the following ANCOVA tests of the response parameters. Where the tests showed significant differences, the investigated parameters were tested using the PDIFF (paired t-test) procedure in the SAS® System. The differences in RAG between the four breads were tested using an analysis of variance (ANOVA) in PROC GLM in SAS®System. Where the ANOVA test showed a significant effect of the investigated parameter, the differences were tested using the PDIFF (paired t-test) procedure in the SAS®System.

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Results

All participants completed the study and ingested the test meals completely within the 10 min. Initial average body mass index (22.7plusminus4.0 kg/m2) did not change significantly during the 4-week study period.

Bread composition

The energy and macronutrient contents of the four breads were per 100 g bread: energy content 946plusminus35 kJ, protein content 7.2plusminus0.3 g, fat content 2.8plusminus0.9 g, and total carbohydrate content 42.2plusminus1.7 g. The content of dietary fiber ranged from 3.0/100 g in the modern wheat bread to 5.6 g in the Einkorn yeast bread. The content of free glucose increased with increasing time of bread processing: From 0.1 g free glucose/100 g in the two yeast produced breads to 0.5/100 g in Einkorn whole grain bread and 1.3/100 g in einkorn honey–salt leavened bread. The RAG values differed significantly from 38.1/100 g in the modern wheat bread to 30.4/100 g in the Einkorn bread leavened with honey–salt bread (Table 1). During the rising of the Einkorn bread leavened with honey–salt, pH in the dough decreased from 5.89 to 5.60.


Postprandial responses in GIP, GLP-1, insulin, and glucose

No significant differences were found in fasting concentrations of GIP, GLP-1, insulin, or glucose. Postprandial concentrations of GIF are shown in Figure 1. The GIP responses were lower after ingestion of the Einkorn bread leavened with honey–salt and Einkorn whole grain bread compared to the yeast leavened bread from either Einkorn or modem wheat (P<0.001). No significant differences were seen in the postprandial concentrations of GLP-1 (Figure 2), insulin (Figure 3), or glucose (Figure 4).

Figure 1.
Figure 1 - Unfortunately we are unable to provide accessible alternative text for this. If you require assistance to access this image, please contact help@nature.com or the author

Plasma concentrations of GIP in 11 healthy subjects after a test meal of 50 g available carbohydrates from four different breads (meanplusminuss.e.m).

Full figure and legend (64K)

Figure 2.
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Plasma concentrations of GLP-1 in 11 healthy subjects after a test meal of 50 g available carbohydrates from four different breads (meanplusminuss.e.m.).

Full figure and legend (52K)

Figure 3.
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Serum insulin concentrations in 11 healthy subjects after a test meal of 50 g available carbohydrates from four different breads (meanplusminuss.e.m.).

Full figure and legend (62K)

Figure 4.
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Plasma glucose concentrations in 11 healthy subjects after a test meal of 50 g available carbohydrates from four different breads (meanplusminuss.e.m.).

Full figure and legend (65K)

The results of the summary statistics of the metabolic responses to the four test meals are shown in Table 2. The results of the gastrointestinal hormonal response showed significant differences in the GIP responses with regard to the iAUC values (P<0.01), the calculated GIP index (P<0.001) and the peak values (P<0.01). The values were significantly reduced for the Einkorn bread leavened with honey–salt added and Einkorn whole grain bread compared to the yeast leavened breads of Einkorn or modern wheat. No differences were seen in the values of time to peak. No significant differences between the test breads were seen with respect to response of GLP-1, insulin or glucose.


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Discussion

The results from the present study do not fully support our hypothesis that bread made from the ancient wheat Einkorn (Triticum monococcum) causes lower gastrointestinal and metabolic responses. Whether made from Einkorn or modern wheat bread processed in the same way gave rise to similar GIP, GLP-1, insulin, and glucose responses. However, when the Einkorn bread was processed in a different way, as was the case in the honey–salt leavened bread and the crushed whole grain bread, the gastrointestinal responses of GIP were significantly lower. A tendency to lower insulin responses was observed with these latter two breads, but the differences did not attain statistical significance. No differences were seen with respect to GLP-1 or glucose responses.

The site of secretion of GIP and GLP-1 in the gastrointestinal tract may explain the more pronounced effect on the GIP response compared to the GLP-1 response in the present study. GIP is synthesized and released from the duodenum and proximal jejunum, whereas GLP-1 is primarily synthesized and released from the ileum (Hoist, 1997; Näslund et al, 1999). It is therefore likely that a larger portion of bread per test meal would lead to more pronounced differences in the GLP-1 responses.

Earlier studies have suggested that both the chemical composition and the physical structure of starchy foods are important determinants for the gastrointestinal and metabolic responses to individual foods (O'Dea et al, 1980; Liljeberg & Björck, 1994,1996; Larsen et al, 1996). In the present study, the overall macronutrient content of the four breads tested was similar. However, looking specifically at the carbohydrate composition, differences were seen between the breads that may partly explain the observed differences in GIP response.

The natural fermentation process that occurred during the processing of the Einkorn bread leavened with honey–salt resulted in an increased content of free glucose (1.3/100 g bread) compared to the Einkorn bread leavened with yeast (0.1/100 g bread) (Table 1). The fermentation also led to a reduction of the total dietary fiber content from 6.6/100 g Einkorn bread leavened with yeast to 4.3/100 g Einkorn bread leavened with honey–salt. This reduction was mostly because of a reduction in the content of soluble arabinoxylans in the Einkorn bread leavened with honey–salt (results not shown).

In the present study, we measured the content of RAG in the test breads to explore this in vitro method as a tool for predicting the metabolic responses to foods. A previous study by Englyst et al (1999) showed RAG to be an important food-related determinant of the glycaemic response. The RAG values in the present study were significantly (P<0.05) lower in the Einkorn breads compared to the modern wheat bread (Table 1). Contrary to the traditional chemical analysis of individual carbohydrates, use of an in vitro measurement like RAG takes into consideration the importance of not only amount and type, but also the physical form of the dietary carbohydrates under investigation and possible interactions between nutrients. The RAG values in the present study ranged from 30.4/100 g in the Einkorn bread leavened with honey–salt to 38.1/100 g in the modern wheat bread, but this difference was probably too small to lead to significant differences in the GI values measured.

The importance of the total dietary fiber content and the composition of the dietary fiber have been much discussed as determinants for the digestibility of foods and the subsequent glycaemic index (GI). Wolever showed that total dietary fibre was significantly related to GI in 25 different food items (r=0.461, P<0.05) (Wolever, 1990). Further multiple-regression analysis of the selected foods showed that the combination of pentoses, hexoses, and uronic acids in soluble and insoluble fibre explained only 50% of the GI variability.

During processing of both the Einkorn bread leavened with honey–salt added and Einkorn crushed whole grain bread, glucose was degraded to organic acids as measured indirectly in the honey–salt bread by the reduction of the pH in the dough from 5.89 to 5.60 during the 17 h leavening process. It is possible that the presence of organic acids resulting from the fermented starch may be one of the contributing factors to the lower GIP response measured after consumption of the Einkorn breads leavened with honey–salt and leavened with whole grain.

Previous studies by Liljeberg and Björck revealed that bread with added sodium propionate or lactic acid with pH values of 6.1 and 3.9, respectively, result in lower glucose and insulin responses in healthy subjects compared to a whole-meal bread with a pH value of 5.8 (Liljeberg & Björck, 1996). Recently, it was shown that the physiological mechanism responsible for the effects of the sodium propionate added to bread can be explained through a delay in the rate of gastric emptying (Darwiche et al, 2001), whereas the suggested mechanism responsible for the effects of lactic acid added to bread has been an obstruction of the digestive system (Liljeberg & Björck, 1996; Björck et al, 2000). The findings of the present study suggest that another mechanism behind the lowered glucose and insulin response to organic acids present in bread may be the lower GIP response.

The significantly lower GIP response to the Einkorn whole grain bread can be explained by the content of coarse grains, supporting earlier findings that the physical structure of a meal is an important determinant for the GIP response (Peracchi et al, 2000).

The only study reported in the literature on the effects of food processing on GIP response is the recent study by Peracchi et al (2000). However, the study design was very different from that of the present study. Peracchi and co-workers compared the postprandial hormonal release of a semisolid vegetable meal (vegetable/cheese/crouton/oil) to that of an isoenergetic homogenized meal. The meal size was considerably larger (2.6 MJ/meal) than that of our test meals (0.97 MJ/meal). Our findings thus suggest that processing of starchy foods such as wheat bread may be a powerful tool for modifying the postprandial GIP response. This may be of particular importance for the response of appetite sensations to the meals, and/or for modulation of fat accumulation. On a long-term basis, a lower GIP response and a lower strain on the insulin release of the pancreas may imply a lower risk for development of metabolic syndromes.

The importance of the manufacturing processes of bread for the gastrointestinal postprandial response needs to be confirmed in modern wheat in test meals and long-term studies. The importance of meal size should be studied separately.

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Conclusion

No differences in the gastrointestinal responses of GIP, GLP-1, insulinaemic or glycaemic responses were measured in healthy subjects after ingestion of bread made from the ancient wheat Einkorn compared to the response to the modern wheat. However, our study showed that the processing of wheat bread is an important determinant for the GIP response. The Einkorn bread leavened with honey–salt added and Einkorn crushed whole grain bread elicited a reduced gastrointestinal response of GIP compared to bread made conventionally by adding yeast. This new finding is of nutritional interest because of the new lines of evidence that suggest that GIP may be involved in modulating fat accumulation in adipose tissue.

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Acknowledgements

We thank the Aurion Bakery, Hjørring, Denmark and Valsemøllen, Esbjerg, Denmark for providing the Einkorn and wheat flour for the breads, and Eva Lydeking Olsen for skillfully baking of the Einkorn whole grain breads. We thank Dr Knud Erik Back Knudsen, The Danish Agricultural Research Center, Foulum, for providing the values for dietary fibre and Trine Rasmussen for excellent technical assistance.

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