Rye Bread Decreases Postprandial Insulin Response but Does Not Alter Glucose Response in Healthy Finnish Subjects

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Rye bread decreases postprandial insulin response but does not alter glucose response in healthy Finnish subjects

K Leinonen,1* K Liukkonen,2 K Poutanen,2 M Uusitupa1 and H MykkaÈnen1

1Department of Clinical Nutrition, University of Kuopio, P.O.Box 1627, 70211 Kuopio, Finland; and 2VTT Biotechnology and Food Research, P.O. Box 1500, FIN-02044 VTT, Finland

Objective: To compare if postprandial glucose and insulin responses to wholekernel rye bread are lower than to wheat bread, and to see if these responses to two types of rye breads are different. To explore starch digestion in more detail, rate of starch hydrolysis of same breads was measured in vitro. Design: Subjects were given test breads (43±61 g available carbohydrates by analysis) with standardized breakfast in a random order after a fast. Eight postprandial blood samples were collected during the following three hours. Rate of starch hydrolysis was determined by an in vitro enzymatic hydrolysis method. Subjects: 10 men and 10 women, aged 32 Æ 3 and 27 Æ 5 y, BMI 24.5 Æ 2.2 and 20.3 Æ 1.1 kg=m2, respectively, all had normal glucose tolerance. Results: Plasma insulin response to wholekernel rye bread was lower than to wheat bread (45 min P 0.025, 60 min P 0.002, 90 min P 0.0004, 120 min P 0.050, 150 min P 0.033), but there was no difference in glucose responses. In comparison of two types of rye breads, glucose response to wholemeal rye bread at 150 and 180 min was higher (P 0.018 and P 0.041, respectively) and insulin response at 60 min was lower (P 0.025) than those to wholemeal rye crispbread. Total sugar pro®les in vitro were similar for all breads. When free reducing sugars were subtracted, starch in wholekernel and wholemeal rye breads appeared to be hydrolysed slower than starch in wholemeal rye crispbread and wheat bread. Conclusions: Wholekernel rye bread produces lower postprandial insulin response than wheat bread, but there is no difference in glucose response. The latter is in accordance with in vitro results. Postprandial glucose and insulin may also be affected by type of rye bread. Characteristics of different types of rye breads must be further investigated to develop health properties of rye breads. Sponsorship: Vaasa Bakeries Ltd, P.O. Box 105, 00240 Helsinki, Finland and Fazer Bakeries Ltd, P.O. Box 40, 15101 Lahti, Finland. Descriptors: rye bread; wheat bread; glucose response; insulin response; starch hydrolysis

Introduction variables not only in diabetes and hyperlipidemia, but also in healthy subjects (BjoÈrck et al, 1994; Englyst & Hudson, Wholemeal sour rye breads are an essential part of the 1997). The glycemic index (GI) concept, although subject to Finnish diet. Rye products comprise approximately 36% some critique (Wolever, 1997), is a widely used method for of the total intake of cereals in Finland (Kleemola et al, classi®cation of different foods according to their effect on 1994). The energy and macronutrient contents of rye grain postprandial glucose levels. The glucose and insulin are similar to those of other cereals. Typical rye products responses of different rye breads and other rye products vary from country to country, variation being caused by have been reported to be variably lower than those of wheat variable ¯our yield and coarseness, the amount of other bread, as reviewed by Foster-Powell & Brand Miller (1995). ingredients (wheat ¯our, sour dough cultures), and the The lowest GI-values (66±80) have been reported for baking process. In Finland the traditional and still popular pumpernickel-type breads containing intact kernels (Jenkins rye breads are based on wholemeal ¯our, and are thus rich et al, 1985, 1986; Wolever et al, 1987, 1994). There is a in dietary ®bre (DF). The DF content of rye ¯our is consensus that intact botanical structure protects the encap- 15±17%, the main chemical constituents being arabin- sulated starch of the kernel against the hydrolysis (Brand et oxylans (8±10%), beta-glucan (2±3%) and cellulose al, 1990; Granfeldt et al, 1992). The amount of whole (1±3%) (HaÈrkoÈnen et al, 1997; AÊ man et al, 1995). kernels in the bread has been concluded to be more effective Mainly due to its high DF content, wholemeal rye bread in reducing the glucose and insulin responses than the high may reduce the health risks associated with coronary heart ®ber content as such (Jenkins et al, 1985, 1986; Wolever et disease (Pietinen et al, 1996) and colon, breast and prostate al, 1994; Liljeberg et al, 1992). cancer (Consensus meeting, 1997; Zhang et al, 1997). Heat processing is generally considered to increase the Slowly digestible carbohydrates have been suggested to GI of foods, mainly due to increased enzymatic accessi- be nutritionally most desirable, improving metabolic bility of the gelatinized starch. The best known exception to this rule is pasta manufacture, most pasta products having a *Correspondence: K. Leinonen, Department of Clinical Nutrition, GI-value of 50±70 (Foster-Powell & Brand Miller, 1995). University of Kuopio, P.O. Box 1627, 70211 Kuopio, Finland. Received 30 June 1998; revised 5 November 1998; accepted 16 November Low temperature and long-time baking may slow the 1998 digestion of bread by increasing the retrogradation of Rye bread decreases postprandial insulin response K Leinonen et al 263 amylose and hence the amount of resistant starch (RS) in was forbidden. Subjects were also asked to avoid heavy the product (BjoÈrck & Liljeberg, 1997). RS passes the small eating and heavy exercise one day before the tests and on intestine without digestion and is available as energy only the test day. A dietitian gave detailed written and oral after colon fermentation. Traditional Finnish rye bread is instructions on the dietary and study regimen. Dietary mostly baked on sour dough, which contains organic acids analysis of nutrient intake was calculated using the and their salts. The latter are supposed to lower postpran- Micro-Nutrica1 software package (Social Insurance Institu- dial glucose and insulin responses (Liljeberg & BjoÈrck, tion, Helsinki, Finland 1993) (Rastas et al, 1993). 1994; Liljeberg et al, 1995; Liljeberg & BjoÈrck, 1996) In the test morning an intravenous catheter was inserted either by interfering the action of hydrolytic enzymes in the in the antecubital vein of the arm. After the fasting blood small intestine or by delaying gastric emptying (BjoÈrck & sample was drawn, the subject had to eat the test meal Liljeberg, 1997). within 15±20 min. The mean times of eating breads were The majority of the studies concerning glycemic 8 min for wheat bread, 9 min for wholekernel rye bread, responses of rye bread have been conducted in diabetic 10 min for wholemeal rye bread and 11 min for wholemeal patients. In this study we wanted to determine in healthy rye crispbread. Blood samples were taken through the subjects whether the postprandial glucose and insulin catheter at 15, 30, 45, 60, 90, 120, 150 and 180 min after responses to rye bread (wholekernel bread) are lower than the start of eating the test meal. those to wheat bread. We also wanted to ®nd out if various Plasma glucose was analysed by the glucose oxidase types of rye breads give different glucose and insulin method (Glucose Auto & Stat, Model GA-110, Daiichi, responses (wholemeal crispbread vs wholemeal bread). Kyoto, Japan) and plasma insulin by the RIA-method To explore the starch digestion in more detail, the rate of (Phadaseph Insulin RIA 100, Pharmacia Diagnostica, starch hydrolysis of the same test breads was measured in Uppsala, Sweden). Maximal glucose and insulin responses vitro. were calculated by subtracting the highest value of blood glucose or insulin from the fasting value of blood glucose or insulin. The areas for glucose and insulin were calcu- Methods lated from initial rise of blood glucose or insulin, respec- Subjects tively, above the baseline (Ha et al, 1992). Twenty healthy Finnish adults (10 men and 10 women, Statistical signi®cances of differences in the postpran- aged 32 Æ 3 and 27 Æ 5 y, respectively) with normal glu- dial glucose and insulin responses between the test bread cose tolerance participated in the study. The body mass (wholekernel rye bread vs wheat bread, wholemeal rye index (BMI) of men was 24.5 Æ 2.2 kg=m2 and that of bread vs wholemeal rye crispbread) were assessed by the women 20.3 Æ 1.1 kg=m2. According to the four day food non-parametric Wilcoxon's test. records kept before the study, the mean energy intake by Approval of the human study was given by the Ethics the men was 9668 kJ=d (2302 kcal=d) (range 6145± Committee at the Kuopio University Hospital. 12243 kJ=d) and by the women 7510 kJ=d (1788 kcal=d) (range 5998±9731 kJ=d). The subjects were asked to main- Chemical composition of the test breads tain their body weight and their energy intake unchanged The moisture content was determined by oven drying at during the study. 130C for 1 h. The protein content was determined by the Kjeldahl method (nitrogen 6 6.25). The fat was determined Test breads and test meals gravimetrically by extraction in diethyl ether and petroleum The test breads were three commercial wholemeal sour rye ether after hydrolysis with acid (AOAC Of®cial Method breads and a white wheat bread as a reference. The breads 922.06, 1995). The dietary ®ber (DF) content was deter- were received from two Finnish bakeries (Fazer Bakeries mined according to Asp et al (1983). Enzymatically avail- Ltd and Vaasa Bakeries Ltd) and they are commonly used able starch contents of test breads were analysed by the in Finland. One of the rye breads was a dried product, method of McCleary et al (1994) using an assay kit of namely, crispbread. It, as well as the wholemeal rye bread, Megazyme (Ireland). Free sugars (glucose, fructose, mal- were produced from a ®nely milled wholemeal rye ¯our, tose, saccharose) were analysed as follows: The milled whereas the third rye bread contained in addition to whole- bread sample (1.80±3.11 g) was suspended in 30 ml of meal rye ¯our also coarse grain particles. Each test meal 0.05 M phosphate buffer, pH 6.9. The suspension was was planned to contain 50 g of available carbohydrate from transferred to the dialysis tubing (cut-off 12-14000) and the test bread, 40 g cucumber and 3 dl non-caloric orange incubated at 37C in a beaker with 800 ml of 0.05 M drink (sweetened with sweetening agent). Because the phosphate buffer, pH 6.9. Aliquots of the dialysate were analysed nutrient compositions of the test breads were not removed after 150 and 180 min incubations for analysis of available as the study started, the portions of the breads free sugar content (glucose, fructose, maltose, saccharose) were calculated using data received from the bakeries (rye by HPLC. The available carbohydrate was de®ned as the breads) or from the Finnish food table (wheat bread) sum of enzymatically available starch and free sugars (Rastas et al, 1993). (analysed by HPLC). Energy value (kJ) was calculated by using the formula 17 6 protein (%) 37 6 fat (%) Study design 17 6 available carbohydrate (%). The analysed data The subjects were fed the test breads in a randomised order on nutrient compositions are shown in Table 1. after an overnight fast. All tests were performed during a two-month period. The subjects were asked to follow their In vitro starch hydrolysis usual diet during the study. Dietary compliance was mon- The rate of in vitro starch hydrolysis in test breads was itored by food records kept for one day before each test determined by the enzymatic hydrolysis method according day. The subjects were not allowed to drink alcohol during to Granfeldt et al (1992). An equivalent amount of avail- two days before the tests, and smoking at the test morning able starch (1 g based on analysed data) from each test Rye bread decreases postprandial insulin response K Leinonen et al

264 Table 1 Nutrient composition of the test bread portions

Portion Available Dietary Energy size CHO a ®ber Protein Fat Moisture content Bread g slices g g g g g kJ

Wheat bread 121.1 5 61 (2.9) 2.3 10.5 3.4 40.8 1341 Wholekernel rye bread 148.4 3.5 55 (7.4) 13.5 9.2 2.2 61.4 1173 Wholemeal rye bread 98.2 4 43 (2.9) 10.1 9.3 2.3 25.4 974 Wholemeal rye Crispbread 79.4 14 45 (0.9) 12.1 8.7 2.2 2.5 994

aPotentially available starch free sugars (glucose, fructose, maltose, saccharose; amount of free sugars in parentheses).

bread was chewed by six subjects. In addition, test bread samples contained different amounts of free sugars which were mainly mono- and di-saccharides added to the dough or formed during baking. After chewing and incubation with pepsin, hydrolysis by pancreatic alpha-amylase was performed in a dialysis tube. At the same time the same amounts of milled (not chewed) bread samples were incubated without enzyme additions in a dialysis tube. Aliquots of the dialysate were removed for analysis of reducing sugar content by the 3,5-dinitro salicylic (DNS) method (Bernfeld, 1955).

Results

Postprandial glucose and insulin response The test bread portions were calculated to include 50 g available carbohydrate based on data received from bakeries and from Finnish food table. However, the analysed Figure 2 Plasma insulin concentrations in healthy subjects after inges- data of nutrient composition of the test breads (Table 1), tion of the test breads. Comparisons are made between wheat and whole- which was available after the in vivo study had begun, kernel rye bread (left) and wholemeal rye bread and wholemeal rye differed from the data received from the bakeries and the crispbread (right). Values are means, n 20. The values for wholekernel rye bread were signi®cantly lower at 45, 60, 90, 120 and 150 min as food table. It was therefore decided to compare two pairs compared to wheat bread, and those for wholemeal rye bread signi®cantly which had similar carbohydrate content based on analysed lower at 60 min as compared to wholemeal rye crispbread, P < 0.05. data: wholekernel rye vs wheat bread (two types of cereals) and wholemeal rye crispbread vs wholemeal rye bread (different types of rye breads). No differences in glucose responses were observed at any time points between the wholekernel rye bread and wheat bread (Figure 1). However, insulin values were signi®cantly smaller at 45 (P 0.025), 60 (P 0.002), 90 (P 0.0004), 120 (P 0.050) and 150 (P 0.033) minutes

Figure 1 Plasma glucose concentrations in healthy subjects after ingestion of the test breads. Comparisons are made between wheat and whole- Figure 3 Plasma glucose and insulin areas in healthy subjects after kernel rye bread (left) and wholemeal rye bread and wholemeal rye ingestion of the test breads. Comparisons are made between wheat and crispbread (right). Values are means, n 20. The values for wholemeal wholekernel rye bread (left) and wholemeal rye bread and wholemeal rye rye crispbread were signi®cantly lower at 150 and 180 minutes as crispbread (right). Values are means s.d., n 20.* Signi®cantly different, compared to wholemeal rye bread, P < 0.05. P 0.002, from wheat bread. Rye bread decreases postprandial insulin response K Leinonen et al 265 Table 2 Maximal glucose (mmol=L) and insulin (mU=L) responses of analysed by HPLC): 20 mg for wholemeal rye crispbread, the test breads (n 20) 50 mg for wheat bread, 74 mg for wholemeal rye bread and 156 mg for wholekernel rye bread. Therefore, the total Maximal response (mean Æ s.d.) contents of available carbohydrates in vitro were 1020 mg Bread Glucose Insulin for wholemeal rye crispbread, 1050 mg for wheat bread, 1074 mg for wholemeal rye bread and 1156 mg for whole- Wheat bread 2.0 Æ 1.0 42.8 Æ 25.3 kernel rye bread. Wholekernel rye bread 1.8 Æ 0.6 32.0 Æ 13.6a Total sugar pro®les which were determined as reducing Wholemeal rye bread 1.9 Æ 0.9 26.2 Æ 14.0 sugars due to starch hydrolysis and free reducing sugars in Wholemeal rye crispbread 1.8 Æ 0.9 30.3 Æ 14.0 bread (analysed by DNS method) in vitro were similar for aP 0.006, different from the wheat bread. all test breads (Figure 4a). When the free reducing sugars in the bread samples (analysed by DNS method) were subtracted from the total sugar, the breads showed different rates of enzymic starch hydrolysis (Figure 4b). Wholemeal for the wholekernel rye bread than for the wheat bread rye crispbread and wheat bread had the fastest and whole- (Figure 2). Consequently, insulin area for the wholekernel kernel rye bread the slowest rate of starch hydrolysis rye bread was signi®cantly smaller than for the wheat bread indicating that starch hydrolysis may be affected by the (P 0.002), but the respective glucose area was similar for type of cereal and bread making process. both breads (Figure 3). Maximal insulin response for the wholekernel rye bread was also lower than that for the wheat bread (P 0.006) (Table 2). Discussion Glucose responses to wholemeal rye bread and whole- In comparison of wholekernel rye bread to wheat bread the meal rye crispbread were statistically different at 150 main ®nding was that the rye bread gave glucose responses (P 0.018) and 180 (P 0.041) minutes (Figure 1) being almost similar to that of the reference wheat bread, but the lower for the wholemeal rye crispbread. Insulin response at rye bread produced signi®cantly lower insulin responses 60 min (P 0.025) (Figure 2) was lower for the wholemeal than the wheat bread. These results are not entirely in rye bread than for the wholemeal rye crispbread. In addi- accordance to previous studies which have shown that tion, plasma glucose reached the maximal concentration breads with whole kernels reduce GI (Granfeldt et al, faster after ingestion of the wholemeal rye bread than after 1992; Liljeberg et al, 1992; Wolever et al, 1994), and the wholemeal rye crispbread (34 and 40 min, respectively; wholegrain rye bread (80% whole kernels) markedly P 0.012). reduces both glucose and insulin responses in healthy subjects compared with wheat bread (Granfeldt et al, In vitro 1992; Liljeberg et al, 1992). Our results indicate that rye In in vitro study an amount of test bread containing 1 g of kernels in wholekernel rye bread may have been disrupted enzymatically available starch (based on analysed data) during boiling and baking processes, and thereby exposed was chewed by the subjects. The sample was 1.80 g for to gelatinization and increased enzymatic accessibility of wholemeal rye crispbread, 2.07 g for wheat bread, 2.45 g starch. On the other hand, the present results may have been for wholemeal rye bread and 3.11 g for wholekernel rye in¯uenced by the presence of free sugars in wholekernel bread. The bread samples also contained various amounts rye bread (7.4 g in the in vivo test bread portion; analysed of free sugars (glucose, fructose, maltose, saccharose; by HPLC). When the free sugars were included, the total sugar curves in vitro (analysed by DNS method) were similar for wholekernel rye bread and wheat bread, as were the in vivo postprandial glucose responses to these breads. In many previous in vivo studies test portions have been determined only based on calculated data or data received from food tables, and those do not necessarily correspond to the actual nutrient composition of the foodstuff con- sumed as noted in the present study. Further confusion in determining the portion size is caused by the poorly de®ned term `available carbohydrate'. When available carbohydrate is calculated as a difference of 100-(protein fat ash moisture DF) there is a risk of over- estimation due to the presence of non-digestible short-chain carbohydrates such as oligosaccharides which are lost in DF determination (Asp et al, 1983). These oligosaccharides, however, pass the upper gastrointestinal tract and are fermented in the colon, and as such they act like DF. Such compounds are for example fructans which are rich in rye Figure 4 (a) Content of total sugars (sugars from starch hydrolysis free (about 4% of dry matter; unpublished results). In this sugars in bread) following chewing and incubation of the bread sample present study the available carbohydrate was determined with pepsin and subsequent incubation with pancreatic a-amylase in a analytically to consist of available starch and free sugars dialysis tube. (b) Content of total sugarsÐfree sugars (determined after (glucose, fructose, maltose, saccharose) because these car- grinding and incubation of the bread sample without enzyme additions). (wheat bread s, wholekernel rye bread r, wholemeal rye bread m, bohydrates are absorbed in the small intestine and in¯uence wholemeal rye crispbread u). the postprandial glucose and insulin response. Determining Rye bread decreases postprandial insulin response K Leinonen et al 266 the portion size on the basis of available carbohydrate can wholemeal rye crispbread (0 min, 5.1 mmol/l; 150 min, be criticized, because the absolute portion sizes in grams 4.8 mmol/l; 180 min, 4.8 mmol/l), while plasma glucose may markedly differ between the various breads. Since approached the baseline concentration more slowly after people usually would eat the same number of slices of wholemeal rye bread (5.1, 5.1 and 4.9 mmol/l at respective bread, for comparison of different types of breads it may be time points). This ®nding suggests that wholemeal rye more practical to determine the test portions as grams of bread maintains the plasma glucose concentrations in the bread rather than based on available carbohydrate. non-fasting level longer than wholemeal rye crispbread. The discrepancy between glucose and insulin responses The reason for this ®nding may be the lower insulin in the comparison of the rye and wheat breads might be response after ingestion of wholemeal rye bread. unexpected. However, in healthy subjects insulin secretion is started immediately after glucose has reached the circulation or as soon as carbohydrate-rich food reaches the Conclusions stomach (Wallum et al, 1992). Therefore, it is possible This present study showed that wholekernel rye bread that in our subjects the blood glucose was effectively decreases postprandial insulin response compared to regulated by postprandial secretion of insulin, thereby wheat bread but there was no difference in glucose producing equal rise in plasma glucose after wholekernel response between these breads. In other words, less insulin rye bread and wheat bread. In subjects with impaired is required for regulation of postprandial plasma glucose glucose metabolism differences between rye and wheat concentrations in healthy subjects after rye bread than after breads could have been more pronounced. In fact, the wheat bread. Similarly, Albrink et al (1979) found lower only earlier study on various types of Finnish rye breads insulin response in healthy subjects after high-®ber meal by Heinonen et al (1985) showed in insulin-dependent than after low-®ber meal, but no difference in respective diabetic patients (IDDM) a lower glucose response to glucose responses. It remains to be shown whether the wholemeal rye bread than to mixed wholemeal rye and higher postprandial insulin concentration after wheat bread wheat ¯our (50:50) bread or wheat bread, and no differ- has any health consequence in healthy subjects. High ences in glucose responses or glucose areas between rye and plasma insulin has been shown to be an independent risk wheat breads in non-insulin-dependent diabetic patients factor for coronary heart disease (PyoÈraÈlaÈ, 1979; Despres et (NIDDM). Wholekernel rye bread (35% whole kernels al, 1996). The characteristics of the different types of rye and 65% wholemeal rye ¯our) differed from the wholemeal breads must be further investigated, both in vivo and in rye bread neither in NIDDM nor in IDDM patients. Unfor- vitro, in order to develop new products which could have tunately Heinonen et al (1985) did not have the same types more bene®cial health properties regarding glucose and of rye breads in their study as we had. insulin metabolism. The reason for the lower insulin response observed in the present study after ingestion of wholekernel rye bread as compared to wheat bread remains to be explained. Contributors Wolever et al (1994) estimated that 17% of the variability The idea of this study and the hypothesis was conceived by in GI values of foods is explained by their protein content, the senior authors (Hannu MykkaÈnen, Kaisa Poutanen, and whereas variability in insulin responses is accounted both Matti Uusitupa). They were responsible for the protocol by the glycemic response (23%) and the macronutrient design and planning of the study and writing and editing of content of the food (10%) (Holt et al, 1997). Both dietary the article. Katri Leinonen was responsible for the practical protein (Nuttall et al, 1984; Gannon et al, 1988) and fat coordination of the human study, data collection, statistical (Welch et al, 1987) modify glycemic response by either analysis and writing of the ®rst draft of the manuscript. stimulating insulin secretion (protein) or delaying gastric Kirsi Liukkonen was responsible for the in vitro study, its emptying (fat). In the present study the variation in the collection and analysis, and she also contributed to the protein and fat content between the test breads was too manuscript. small to in¯uence the results, but the possibility of delayed gastric emptying from other reason is not excluded. Acknowledgements ÐThis research was carried out as part of the TEKES Hagander et al (1987) found that rye ¯akes produce national technology programme `Innovation in Foods'. The fruitful dis- signi®cantly lower GIP and glucagon responses, but no cussions with MSC (Eng) Risto Viskari (Fazer Bakeries Ltd) and Dr differences in glucose responses as compared to wheat Sampsa Haarasilta (Cultor Ltd) are highly appreciated. Fazer Bakeries Ltd bread. These ®ndings are in agreement with our results and Vaasa Bakeries Ltd provided the breads and ®nancial support for the on lower insulin responses after the rye breads. Besides study. 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