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Can bread processing conditions alter glycaemic response?

Contents lists available at Can bread processing conditions alter glycaemic response? Evelyn Lau Yean Yean Soong Weibiao Zhou , Jeyakumar Henry , a Clinical Nutrition Research Centre, Singapore Institute for Clinical Sciences, 14 Medical Drive, #07-02, Singapore 117599, Singaporeb Food Science and Technology Programme, Department of Chemistry, National University of Singapore, S14 Level 5, Science Drive 2, Singapore 117543, Singaporec Department of Biochemistry, Yong Loo Lin School of Medicine, National University of Singapore, 14 Medical Drive, #14-01, Singapore 117599, Singapore Bread is a staple food that is traditionally made from wheat flour. This study aimed to compare the starch Received 7 July 2014 digestibility of western baked bread and oriental steamed bread. Four types of bread were prepared: Received in revised form 12 September western baked bread (WBB) and oriental steamed bread (OSB), modified baked bread (MBB) made with the OSB recipe and WBB processing, and modified steamed bread (MSB) made with the WBB recipe and Accepted 7 October 2014 OSB processing. MBB showed the highest starch digestibility in vitro, followed by WBB, OSB and MSB.
Available online 19 October 2014 A similar trend was observed for glycaemic response in vivo. MBB, WBB, OSB and MSB had a glycaemicindex of 75 ± 4, 71 ± 5, 68 ± 5 and 65 ± 4, respectively. Processing differences had a more pronounced effect on starch digestibility in bread, and steamed bread was healthier in terms of glycaemic response.
BreadGlycaemic response The manipulation of processing conditions could be an innovative route to alter the glycaemic response of carbohydrate-rich foods.
Ó 2014 Elsevier Ltd. All rights reserved.
Bread is a staple food that is traditionally made from wheat flour. It is consumed in different parts of the world, albeit in differ- are quantitatively the most important dietary ent forms due to variations in the choice of ingredients used, and energy source for humans, typically accounting for 45–70% of total processing techniques employed. The GI value of bread was energy intake They play an reported to range from 40 to 97 important role in energy metabolism and glucose homeostasis.
). The wide-ranging GI values may be Carbohydrate foods that increase blood glucose rapidly are known due to: (a) differences in molecular configuration of starch present, as high glycaemic index (GI) foods, and those that increase blood (b) variations in cooking and processing methods that resulted in glucose gradually are known as low GI foods ( differing degrees of starch gelatinization, (c) differences in They may be divided into low GI (GI 6 55), medium structure of bread in terms of compactness and viscosity, and GI (56 6 GI 6 69) or high GI (GI P 70). Diet is known to play a cri- (d) possible interactions with other food components, such as tical role in the aetiology and management of obesity and diabetes starch–protein and starch–lipid interactions, that could impede (A large number of studies, including starch digestibility observational prospective cohort studies as well as randomized In Asia, notably China and its surrounding regions, steamed controlled trials, show a positive association between consumption bread is a popular staple. In contrast to baked bread, oriental of low GI food in the prevention of obesity, diabetes and cardiovas- steamed bread is typically made using low to medium protein con- tent wheat flour that undergoes fermentation and is further cooked The glycaemic response is also influenced by the by steaming, rather than baking. A distinction should be made quantity of carbohydrates consumed. Glycaemic load (GL) is a between steamed bread (‘‘mantou'') and steamed bun (‘‘baozi'').
measure to quantify the overall glycaemic effect of a portion of Mantou is plain steamed bread without any filling, whereas baozi food, and takes into account the amount of carbohydrates present is steamed bread containing sweet or savoury fillings made of bean paste or minced meat. Thus, western oven-baked bread and orien-tal steamed bread vary in both the ingredients used, preparationmethods, and heating methods applied. Although glycaemic ⇑ Corresponding author at: Singapore Institute for Clinical Sciences, Clinical response of western bread has been researched intensively in Nutrition Research Centre, 14 Medical Drive, #07-02, Singapore 117599, Singapore.
recent years, there is a dearth of information related to the glycae- Tel.: +65 6407 0793; fax: +65 6776 6840.
mic response and glycaemic index of oriental steamed bread. This E-mail address: (J. Henry).
0308-8146/Ó 2014 Elsevier Ltd. All rights reserved.
E. Lau et al. / Food Chemistry 173 (2015) 250–256 study aimed to compare the in vitro starch digestibility and in vivo were carried out in triplicates, with two measurements per analy- glycaemic response of western baked bread and oriental steamed sis. The total available carbohydrate content of each type of bread bread. More importantly, the study focused on investigating how was determined using Megazyme assay kit (Megazyme, Ireland).
differences in macronutrient composition and processing condi-tions (namely, mixing time, mixing intensity, proofing period and 2.4. In vitro analysis of starch digestibility method of cooking) influenced glycaemic response.
vitro starch hydrolysis and quantification of sugars released during digestion were carried out according to previously Materials and methods described methodology (). About 2.5 g of each type of bread was weighed and Chemicals, reagents and bread ingredients analysed. Rapidly digestible starch (RDS) and slowly digestiblestarch (SDS) were quantified. RDS was defined as starch that was Sodium hydroxide pellets and concentrated hydrochloric acid rapidly digested within 20 min into pancreatic digestion phase, whereas SDS defined as starch that was digested within Germany). Pancreatin (P7545, 8X USP specifications), pepsin 20–120 min of pancreatic digestion phase. Triplicates were carried (800–2500 units/mg) and amyloglucosidase (P300 U/ml) used in out for the in vitro analysis of starch digestibility.
the in vitro digestion protocol were purchased from Sigma–AldrichCompany Ltd. (St. Louis, USA). Amyloglucosidase (E-AMGDF, 2.5. In vivo analysis of glycaemic response 3260 U/ml) used for the secondary digestion in the reducing sugarassay was obtained from Megazyme International (Wicklow, Ireland). Absolute ethanol was obtained from Fisher Scientific healthy subjects (seven male and eight female; age Company (Fairfield, USA). Milli-Q ultrapure water was used 24 ± 5 years old; BMI 21.2 ± 1.8 kg/m2; values expressed as throughout the experiments (Billerica, USA). The maleate (0.2 M/ means ± SD) participated in the study. The inclusion criteria for pH 6) and acetate (0.1 M/pH 5.2) buffers were prepared according healthy subjects were: age between 21 and 50 years old, BMI to previously described methods Lancets values ranging between 18.0 and 24.9 kg/m2, blood pressure values were purchased from Abbott (Abbott, UK) for in vivo GI testing.
6120/80 mmHg, and fasting blood glucose levels 66.0 mmol/l.
Glucotrol (Eurotrol, Sweden) was used for daily quality checking Subjects who smoked, had metabolic diseases or took part in sports of glucose metres to ensure reliability of results.
at competitive levels were excluded from the study. Ethics High protein wheat flour (Prima bread flour, Singapore), med- approval was given by the National Healthcare Group Domain ium protein wheat flour (Hong Kong Bake King Flour, Singapore), Specific Review Board. Written informed consent was obtained vegetable shortening (Bake King, Singapore), yeast (SAF instant, from subjects prior to participation in the study.
France), salt (Fairprice, Singapore) and sugar (Fairprice, Singapore)were purchased from the local supermarket. Potable water was 2.5.2. Study design used for preparation of bread.
study protocol used was in accordance with procedures recommended by the FAO/WHO/ISO (The subjects Bread making process were instructed to avoid vigorous exercise and excessive alcoholthe day before the test, and to consume dinner in standard portions Four types of bread were prepared for this study the evening before in order to avoid the second meal effect Western baked bread (WBB) was prepared using standard recipe ingredients (with the use of high protein flour) and processing requested to fast for at least 10 h prior to the test, and to report steps, including baking at 210 °C, and oriental steamed bread to the testing site between 0800 and 0900 h on the day of the test (OSB) was prepared using standard recipe ingredients (with the session. Bread was presented to subjects in a randomized order on use of medium protein flour) and processing steps, including four separate test sessions. Each portion of bread served was steaming at 100 °C. The standard recipes for WBB and OSB were equivalent to 50 g of total available carbohydrate content to adapted from previously described methods account for differences in recipe formulation. The reference food ). Modified baked bread (MBB) was 50 g of anhydrous glucose dissolved in 250 ml of potable was prepared using oriental steamed bread recipe ingredients water. The mean glycaemic response of reference food, calculated and baked bread processing steps (baking at 210 °C). Modified as the average glycaemic response from three separate test ses- steamed bread (MSB) was prepared using western baked bread sions of consumption of 50 g glucose, was used for the calculation recipe ingredients and steamed bread processing steps (steaming of GI of test bread. This was done to account for inter-day variabil- at 100 °C). Bread was freshly prepared on the morning of the study.
ity of subjects. There was at least a 1 day gap between GI measure-ments to minimise carry-over effects. The test and reference food Analytical methods were served with plain drinking water. Subjects were instructedto finish the test food within 15 min, and physical activity was kept Protein, fat and moisture contents were determined according to a minimum during the test.
to AACC methods 46-11.02, 30-25.01 and 44-01.01 respectively blood samples were taken at 5 min and 0 min. Fingers ). Protein content was analysed with were gently massaged prior to finger pricking. Baseline values FOSS Kjeltec Systems (FOSS, Denmark). Fat content was analysed were calculated as a mean of the two values with coefficient of var- with FOSS Soxtec 2055 (FOSS, Denmark). Dough, proofed dough iation <4%. The test food was consumed after taking baseline mea- and bread volume were determined with a VSP 600 Volscan Profi- surements, and timing started with the first bite of the test food.
ler (Stable Micro System Ltd., UK). The sample was mounted on a Further blood samples were taken at 15, 30, 45, 60, 90 and stand, and a laser sensor was used to scan the rotating sample to 120 min. Blood glucose was measured with a HemoCue Glucose measure the contours of the sample at regular intervals for calcu- 201+ RT analyser (HemocueÒ Ltd., Sweden). The glucose metres lation of volume using the installed computer software. Specific were checked daily using Glucotrol to ensure reliability of the mea- volume was determined by calculating the ratio between the surements. Incremental area under blood glucose curves (IAUC) volume of the dough or bread and its weight. These measurements was calculated geometrically (GI value of

1Ingredients and processing parameters for WBB, MSB, OSB and MBB.
Western baked bread Modified steamed bread made with conventional Oriental steamed bread Modified baked bread made with steamed bread baked bread recipe – Mix dry ingredients at level 1 intensity for – Mix dry ingredients at level 1 intensity for – Mix dry ingredients at level 1 intensity for – Mix dry ingredients at level 1 intensity for – Add water, mix at level 1 intensity for 1 min, – Add water, mix at level 1 intensity for 1 min, – Add water, mix at level 1 intensity for 1 min, – Add water, mix at level 1 intensity for 1 min, followed by level 3 intensity for 7 min followed by level 2 intensity for 4 min followed by level 2 intensity for 4 min followed by level 3 intensity for 7 min Baking at 210 °C, 11 min Steaming at 100 °C, 10 min Steaming at 100 °C, 10 min Baking at 210 °C, 11 min a Resting was carried out at room temperature.
b Proofing was carried out at 40 °C, 85% relative humidity.
E. Lau et al. / Food Chemistry 173 (2015) 250–256 bread for each subject was calculated by expressing the IAUC of despite having higher protein content. This suggested that specific bread as a percentage of IAUC of the mean of the three glucose volume of bread was not only dependent on protein content, but tests. The GI of each type of bread was calculated as the mean GI was also influenced by processing parameters.
for all the subjects. The GL of each type of bread was calculated optimal dough development, gluten proteins are by: (GI  50 g total available carbohydrate)/100.
hydrated and undergo dis-aggregation, in which glutenins alignand form cross links with glutenins, and cross-linked protein Statistical analysis sheets are layered one over another to form the gluten network(Energy input during dough development Data processing was carried out using SPSS software (version increased with mixing intensity and duration. The gluten network 16, USA). Data was presented as means ± standard deviation (SD) has been shown to be weakened and ruptured with excessively or means ± standard error of mean (SEM), as indicated. The specific high energy input, resulting in reduced dough visco-elasticity volume results were analysed using Kruskal–Wallis test, and post hoc comparisons were carried out using Mann–Whitney U test ing the length of fermentation time also had a positive effect on with Bonferroni's correction. In vitro starch digestibility results bread volume for optimally developed dough, in which the expan- were evaluated using one-way ANOVA, and post hoc comparisons sion of gas cells brought about an increase in porosity of bread were carried out using Bonferroni's correction. For in vivo GI analy- crumb. The use of higher mixing speed, longer mixing times and sis, differences in postprandial blood glucose concentrations, IAUC longer proofing period during the WBB and MBB bread making and GI values were evaluated using repeated-measures ANOVA procedure resulted in WBB and MBB with significantly higher spe- with Bonferroni's correction. The glycaemic response of the differ- cific volume for both proofed dough and bread, as compared to OSB ent types of bread was evaluated using repeated measures ANOVA, and MSB. In addition, bread typically experiences oven-spring with Bonferroni's correction. The differences in IAUC and GI upon heating, due to further expansion of gas volumes at elevated between male and female subjects were compared using indepen- temperatures (). The use of higher tempera- dent samples t-test. Statistical significance was set at p < 0.05 for tures during baking (210 °C), as compared to steaming (100 °C) may have resulted in a faster rate of temperature increase of doughfor baked bread as compared to steamed bread, resulting in higherspecific volumes for WBB and MBB, as compared to OSB and MSB.
Results and discussion MSB had the lowest specific volume, possibly due to under-development of dough. High protein flour was used for preparation Specific volume of bread of MSB, but underwent a short mixing period with low intensity,and this could have resulted in insufficient development of the glu- The specific volume of dough, proofed dough and bread were ten network. The combination of low energy input during dough measured to compare the development of bread structure ().
development, as well as a shortened fermentation period, resulted MBB dough had the highest specific volume, and specific volume in MSB having the least porous structure as compared to other for other types of dough did not differ significantly (p > 0.05).
types of bread.
Increased protein content of flour has previously been found tohave a positive effect on bread specific volume WBB had the highest specific volume for both 3.2. Starch digestibility proofed dough and baked bread, followed by MBB, OSB and MSB.
The higher protein content in WBB (may result in the for- 3.2.1. In vitro starch digestibility mation of a more extensive gluten network during dough develop- was subjected to in vitro enzymatic digestion under con- ment which enabled the more effective retention of gas during trolled conditions to quantify the amount of rapidly digestible proofing, thereby resulting in a higher specific volume as compared starch (RDS) and slowly digestible starch (SDS) (). In a pre- to MBB. On the other hand, the specific volumes of MSB proofed vious study, RDS had been found to show good correlation with dough and bread were found to be significantly lower than OSB, in vivo glycaemic response, and it could therefore be a proxy indi-cator of GI value RDS wasfound to be the predominant starch fraction in all four types of bread, as most of the starch was fully gelatinized, and bread typi- Specific volume (ml/g) of dough, proofed dough and bread of WBB, MSB, OSB and cally has an open structure, rendering starch highly accessible to hydrolysis by amylase Comparing MBB with WBB (different recipe ingredients and same processing procedures), it was found that MBB had significantly higher RDS content than WBB. Simi- larly, comparing OSB with MSB (different recipe ingredients and Values are represented as means ± SD. Values within a row with different super- same processing procedures), OSB had significantly higher RDS script letters are significantly different (p < 0.05).
content than MSB. Although more sugar was used in the recipe 3Nutrient composition of wheat flours (g/100 g), WBB, MSB, OSB and MBB (per 50 g available carbohydrate portion).
Total available carbohydrate (g)

E. Lau et al. / Food Chemistry 173 (2015) 250–256 Fig. 1. Rapidly digestible starch and slowly digestible starch contents of WBB, MSB, OSB and MBB.
for preparing WBB and MSB, the medium protein content wheat In vivo glycaemic response flour used for preparing OSB and MBB had a higher available carbo- The postprandial blood glucose responses to steamed and baked hydrate content as compared to the high protein content wheat bread showed different temporal profiles as shown in . In flour used for preparing WBB and MSB Even though less agreement with a previous study (), there were sugar was used in the recipe for OSB and MBB, it resulted in higher no significant differences in IAUC and GI between male and female RDS amounts being detected during in vitro studies.
subjects. Peak glycaemic response for OSB and MSB was observed conditions had a marked effect on in vitro digestibil- at 30 min, whereas WBB and MBB showed a delayed peak glycae- ity. Baked breads (WBB and MBB) were found to have higher RDS mic response at 45 min. WBB and MBB gave rise to higher peak content. This could be attributed to the higher specific volume glucose concentrations than OSB and MSB, and the higher blood and porosity, resulting in increased accessibility of amylases to glucose concentrations were sustained until 120 min. This resulted starch granules, rendering starch more susceptible to hydrolysis.
in higher IAUC for WBB and MBB, but the differences were not A previous study has shown that an increase in degree of mixing significant amongst the four types of bread. Physical structure in dough results in higher amounts of RDS content, possibly due was found to be an important factor in determining glycaemic to a weakened gluten matrix that renders starch granules more response of bread, as reported in previous studies accessible to enzymatic digestion (WBB The manipulation of physical and MBB were found to have significantly higher SDS content than structure, and in turn, starch digestibility, was brought about by MSB and OSB (p < 0.05). Rapid evaporation of water from the out- differences in processing procedures. A more compact bread struc- ermost region of dough in the presence of dry heat resulted in ture could have hindered the accessibility of amylase to starch incomplete gelatinization of starch granules ( granules, resulting in a slower rate of glucose release, and reduced ). Digestibility has been glycaemic response in OSB and MSB.
shown to reduce with decreased gelatinization, as limited swelling The total IAUC of MBB was slightly higher than WBB, with GI and hydration decreases the chemical reactivity of starch granules values of 75 and 71 respectively (). MBB and WBB were pre- towards amylolytic enzymes ). The use of pared using different recipe ingredients, but underwent the same moist heat during steaming did not result in crust formation, processing procedure. A similar trend was observed for OSB and accounting for the significantly lesser SDS content found in OSB MSB, which had GI values of 68 and 65, respectively. The modest differences in glycaemic response in this study suggested that Fig. 2. Blood glucose responses to 50 g equivalent portions of bread in healthy subjects (n = 13).
E. Lau et al. / Food Chemistry 173 (2015) 250–256 4Postprandial blood glucose characteristics of WBB, MSB, OSB and MBB.
Max incremental peak rise (mmol/L) Time of peak rise (min) Incremental area under curve (IAUC) Values are represented as means ± SEM. Values within a row with same superscript letters are not significantly different (p > 0.05).
macronutrient composition played a minor role in digestibility of starch. Digestion of starch is known to be hindered in the presenceof proteins and lipids, as proteins may encapsulate starch granules study demonstrated for the first time that even with the to form a protective barrier against enzymatic hydrolysis, and use of identical bread recipe ingredients, the application of varied starch, particularly amylose, may form complexes with lipids to processing conditions, namely mixing time, mixing intensity, resist breakdown. The lower protein and fat content in MBB and proofing period and method of cooking, resulted in lower starch OSB, as compared to WBB and MSB (did not change post- digestibility in vitro and reduced glycaemic response in vivo as prandial glycaemic response markedly. MBB showed a slightly compared to baked bread. Processing played a major role in affect- higher glycaemic response than WBB in vivo, and had significantly ing the physical structure of bread. It has been customary to use higher in vitro starch digestibility than WBB. Despite having a food ingredients such as b-glucan, galactomannan, non-starch lower specific volume, the greater extent of starch digestibility of polysaccharides and polyols to reduce the glycaemic index of high MBB, both in vitro and in vivo may be partly attributed to the lower GI foods (). The observation that processing para- protein content in the flour used for the preparation of MBB. MBB meters could impact on glycaemic response of wheat-based foods dough was subjected to intense energy input during dough devel- provides us with a new approach to manipulate the glycaemic opment, and the weakened gluten network in MBB, as seen from index of carbohydrate-rich foods. Work is in process to elucidate the lower specific volume of bread, as compared to WBB, could the differences in the microstructure of bread to understand the have resulted in reduced resistance during enzymatic digestion, potential links between food microstructure and glycaemic and correspondingly a higher glycaemic response.
In vitro starch digestibility and in vivo glycaemic response results were in agreement and showed the same ranking for thefour types of bread. MBB was found to have the highest glycaemic Conflict of interest response, followed by WBB, OSB and MBB. This indicated thatdigestibility of starch and the release of glucose were consistent of the authors declare any conflict of interest.
in both studies. Bread was predominantly made up of RDS, andthe amount of SDS was comparatively too low to significantly impact on the glycaemic response. Hence, the higher SDS contentsdid not contribute to reduced glycaemic response in this case. The This research was funded by the A⁄STAR Health and Lifestyle physical structure of bread could be manipulated by processing Grant (Grant No. 112 177 0033). We would also like to thank conditions (namely mixing time and duration, fermentation period Dr. Tan Sze Wee, Deputy Director of Biomedical Research Council, and method of cooking), resulting in pronounced changes in gly- for his continued support.
caemic response. When ascertaining whether macronutrient com-position or processing parameters had a greater impact on glycaemic response, the latter was found to play a more pivotalrole in this study, as both types of steamed bread, OSB and MSB, demonstrated lower starch digestibility in vitro and reduced gly- caemic response in vivo. It has been reported that the risks of developing cardiovascular diseases is associated with an elevated blood glucose levels in healthy individuals ). Modest increases in postprandial blood glucose levels could also reduce the long-term risk of developing Type 2 diabetes ). In this study, steamed bread emerged as a ‘‘healthier'' alternative to baked Glucose tolerance is known to decrease with age due to impaired insulin secretion and action. Higher postprandial glucose concentrations after consumption of a mixed meal has been observed in elderly adults as compared to younger individuals ). Subjects within the age band of 19–50 years are typically recruited for GI studies how- ever, the mean age of the subjects recruited for this study was 24 years. It is important to recognise that the results in elderly adults, compared to the relatively young adults in our study, could be different. Future studies could be carried out to assess the gly- caemic response and insulinemic index in elderly adults.
E. Lau et al. / Food Chemistry 173 (2015) 250–256

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