Eur J Nutr DOI 10.1007/s00394-015-0985-z
ORIGINAL CONTRIBUTION
Effects of wheat bran extract rich in arabinoxylan oligosaccharides and resistant starch on overnight glucose tolerance and markers of gut fermentation in healthy young adults Elin V. Johansson Boll1 · Linda M. N. K. Ekström1 · Christophe M. Courtin2 · Jan A. Delcour2 · Anne C. Nilsson1 · Inger M. E. Björck1 · Elin M. Östman1
Received: 5 March 2015 / Accepted: 1 July 2015 © Springer-Verlag Berlin Heidelberg 2015
Abstract Purpose Specific combinations of dietary fiber (DF) have been observed to result in improved glucose tolerance at a subsequent standardized breakfast. Arabinoxylan oligosaccharides (AXOS) are considered as DF with prebiotic potential, but so far no studies have investigated their metabolic effects in humans. This randomized cross-over study evaluated the overnight impact of breads containing AXOS-rich wheat bran extract and resistant starch (RS, Hi-Maize), separately or combined, on glucose tolerance, related metabolic parameters and markers of gut fermentation in healthy subjects. Methods Evening reference and test products were: (1) reference white wheat flour bread (WWB), WWB supplemented with (2) AXOS and RS (WWB + AXOS + RS), (3) an increased content of either AXOS (WWB + hiAXOS) or (4) RS (WWB + hiRS). At the subsequent standardized breakfast, blood was sampled for 3 h to monitor glucose, insulin, nonesterified fatty acids, glucagon-like peptide (GLP)-1 and GLP-2. Breath hydrogen (H2) and short chain fatty acids (SCFA) were measured as markers of gut
Electronic supplementary material The online version of this article (doi:10.1007/s00394-015-0985-z) contains supplementary material, which is available to authorized users. * Elin M. Östman Elin.Ostman@food‑health‑science.lu.se 1
Food for Health Science Centre, Lund University, Lund, Sweden
2
Laboratory of Food Chemistry and Biochemistry and Leuven Food Science and Nutrition Research Centre (LFORCE), Department of Microbial and Molecular Systems (M2S), KU Leuven, Leuven, Belgium
fermentation, and subjective appetite was rated using visual analog scales. Results Dose-dependent decreases in glucose responses were observed with increased AXOS over the duration of 3 h. Insulin sensitivity index was improved in the morning after the WWB + hiAXOS evening meal. An increase in breath H2 concentration and circulating SCFA was observed in the morning after both evening meals containing AXOS. Conclusion The present study indicates that AXOS have the potential of improving glucose tolerance in an overnight perspective and suggested mechanisms are improved insulin sensitivity and increased gut fermentation. Keywords Arabinoxylan oligosaccharides · Resistant starch · Glucose tolerance · Gut fermentation · Healthy subjects · Overnight
Introduction The world prevalence of diabetes is rapidly increasing and is estimated to go from 285 million adults in 2010 to 439 million in 2030 [1]. The metabolic syndrome (MetS) is a cluster of cardiovascular risk factors that predict a high risk of developing diabetes. Consequently, individuals with MetS and insulin resistance have up to fivefold higher risk of developing diabetes than healthy individuals [2]. The importance of a tight glycemic control has been identified as preventive against manifestations of the MetS, such as obesity, diabetes and cardiovascular disease [3]. This makes it relevant to investigate and explore novel food ingredients and their ability to influence the postprandial blood glucose responses in healthy subjects. The mechanisms whereby specific foods, e.g., starchy products, influence
13
acute glycemia involve both physiological factors, such as enzymatic availability, and food properties such as food structure, e.g., botanical, physical and/or chemical structure [4, 5]. In addition, the presence of certain food components (e.g., slow or indigestible carbohydrates) has shown to beneficially affect the glycemic response at a subsequent meal, through mechanisms related to gut fermentation [6, 7]. Previously, we have shown that a white wheat flour-based bread (WWB), with added dietary fiber (DF) in form of nonstarch polysaccharides (NSP) from barley, and resistant starch (RS) from high amylose maize, in levels corresponding to those of a whole-kernel based barley bread, induced similar benefits to overnight glucose tolerance as a wholekernel barley bread [8]. The overnight benefits on glucose tolerance were suggested to be mediated by gut fermentation of the specific mix of indigestible substrates. A relatively new candidate substrate evaluated for its prebiotic potential is the arabinoxylan oligosaccharides (AXOS). These are degradation products of arabinoxylans (AX) which are formed during treatment of wheat with xylanase enzymes [9]. So far, AXOS have been shown to modulate intestinal fermentation and overall gastrointestinal properties in healthy humans [10], with specific growth of bifidobacteria in both adults [11, 12] and preadolescent children [13]. Furthermore, supplementation of AXOS for 8 weeks improved specific gut hormones and markers of inflammation in diet-induced obese mice [14]. However, to the best of our knowledge, there is no information about metabolic effects of AXOS on, e.g., semi-acute glycemic regulation and gut hormones in humans. The aim of this study was to investigate the potential metabolic benefits of AXOS-rich wheat bran extract (WBE), alone or in combination with RS, in white wheat flour-based breads on overnight glucose tolerance, markers of gut fermentation as well as changes in gut-derived hormones in healthy young adults. To further explore specific metabolic effects of RS, white wheat flour-based breads with increased amounts of RS were included in the study.
Experimental methods Test subjects Nineteen healthy volunteers, 9 men and 10 women aged 23 ± 0.4 years, with normal body mass index, 22.2 ± 0.4 kg/m2, participated in the study. The inclusion criteria were 20–35 years, BMI 19–25 kg/m2, nonnicotine user (smoking, snuff) and no known metabolic disorders or food allergies. Furthermore, the test subjects were instructed to not consume antibiotics or probiotics during the previous 2 weeks and throughout the study. Recruitment of test subjects was performed by local
13
Eur J Nutr
advertisement around Lund University, and the study was performed between April and December 2009. This study was conducted according to the guidelines laid down in the Declaration of Helsinki, and the study was approved by the Regional Ethical Review Board in Lund, Sweden (668/2008). Written informed consent was obtained from all subjects. Study design and sampling procedures Four bread products (three test products and one reference product) were included in the study. The test and reference products were provided to the test subjects as late evening meals in a randomized, cross-over design. Both the test and reference products, as well as the standardized breakfast, were equi-carbohydrate portions of 50 g potentially available starch. Each subject participated on four different occasions, approximately 1 week apart. The subjects were instructed to standardize their meal pattern and to avoid alcohol, excessive physical exercise or food rich in DF during the entire day before each experiment. The test and reference products were given to the subjects as frozen portions, and they were instructed to eat the four products in a pre-decided randomized order. At the day of consumption, the bread portion was thawed in ambient temperature, still wrapped in aluminum foil and in the plastic bag. The bread was consumed together with 250–300 ml water at 21.30 hours (h) in the evening. After ingestion of the test or reference product, the subjects were fasting until the standardized breakfast was served in the experimental unit. The subjects arrived at 07.40 h in the morning, and an intravenous cannula (BD Venflon, Becton–Dickinson) was inserted into an antecubital vein for blood sampling. Fasting blood samples were collected, and subjective appetite sensations and breath H2 were registered before the breakfast, which was then served 10.5 h after consumption of the evening meal. The breakfast was served with 300 ml water and had to be finished within 15 min. Test variables were determined repeatedly in the postprandial period (3 h) after the breakfast. Blood (b)-glucose, serum (s)insulin, plasma (p)-GLP-1, breath H2 and subjective appetite ratings (measured with visual analog scales, VAS [15]) were obtained at fasting and 15, 30, 45, 60, 90, 120 and 180 min after commencing the breakfast. Samples for s-nonesterified fatty acids (s-NEFA) and p-GLP-2 were collected at fasting, and samples for p-SCFA were measured at fasting and 120 min. The test subjects were instructed to maintain a low physical activity during the experiments. The test subjects were instructed to complete a tolerance questionnaire with questions regarding the acceptance of the evening test and reference products related to gastrointestinal discomfort. The questionnaire was completed at two occasions for each test product. The first questionnaire was completed just before the onset of the evening test or
Eur J Nutr
reference meal and the second questionnaire approximately 48 h later.
Table 1 Theoretical contents of AXOS, glucans and RS in the evening bread meals Meals
Description of standardized breakfast, reference and test products White wheat flour bread was used both as the reference product and as the standardized breakfast. All three test products were based on white wheat flour but varied in amounts of AXOS and/or RS. The first test product (WWB + AXOS + RS) was designed to mimic the combined NSP + RS product studied previously [8]. However, the major contribution of indigestible material in the present product originated from AXOS-rich WBE as opposed to the previously studied NSP from barley. The second product was a WWB supplemented with increased content of RS only (WWB + hiRS), and the third product was a WWB with increased content of AXOS (WWB + hiAXOS) and no added RS. All bread products were baked in a home bread-making machine according to the standardized procedure described previously [16]. Common ingredients were: white wheat flour (Vetemjöl special, Kungsörnen AB, Järna, Sweden), dry yeast (KronJäst, Jästbolaget AB, Sollentuna, Sweden) and NaCl (Falksalt, AB Hanson & Möhring, Halmstad, Sweden). After cooling, the crust was removed and the bread was sliced. Portions corresponding to 50 g potentially available starch were wrapped in aluminum foil, put into plastic bags and stored in a freezer (−20 °C). The theoretical contents of AXOS and RS in the bread products are shown in Table 1. WWB (reference product and standardized breakfast): 540 g white wheat flour, 360 g water, 4.8 g dry yeast and 4.8 g NaCl. WWB + AXOS + RS: 480 g white wheat flour, 360 g water, 120 g high amylose maize starch (Hi-Maize™ 260, Ingredion Incorporated, Bridgewater, NJ, USA), 90 g AXOS-rich WBE (Brana Vita™ 200, Fugeia NV, Heverlee, Belgium), 6 g dry yeast and 6 g NaCl. WWB + hiAXOS: 495 g white wheat flour, 330 g water, 165 g AXOS-rich WBE (Brana Vita™ 200, Fugeia NV, Heverlee, Belgium), 5.5 g dry yeast and 5.5 g NaCl. WWB + hiRS: 400 g white wheat flour, 400 g water, 270 g hi-amylose maize starch (Hi-Maize™ 260, Ingredion Incorporated, Bridgewater, NJ, USA), 5 g dry yeast and 5 g NaCl. Chemical analysis of evening meals and standardized breakfast The WWB and test products were analyzed with respect to potentially available starch [17]. In addition, the test
Glucansa
RSb
Portion size
Dry matter
AXOS
g
%
g/portion (wet weight)
WWB
116.2
55.0
–
WWB + AXOS + RS
140.5
57.1
8.9
WWB + hiAXOS
141.4
60.8
18.4
WWB + hiRS
137.9
52.4
–
ORIGINAL CONTRIBUTION
Effects of wheat bran extract rich in arabinoxylan oligosaccharides and resistant starch on overnight glucose tolerance and markers of gut fermentation in healthy young adults Elin V. Johansson Boll1 · Linda M. N. K. Ekström1 · Christophe M. Courtin2 · Jan A. Delcour2 · Anne C. Nilsson1 · Inger M. E. Björck1 · Elin M. Östman1
Received: 5 March 2015 / Accepted: 1 July 2015 © Springer-Verlag Berlin Heidelberg 2015
Abstract Purpose Specific combinations of dietary fiber (DF) have been observed to result in improved glucose tolerance at a subsequent standardized breakfast. Arabinoxylan oligosaccharides (AXOS) are considered as DF with prebiotic potential, but so far no studies have investigated their metabolic effects in humans. This randomized cross-over study evaluated the overnight impact of breads containing AXOS-rich wheat bran extract and resistant starch (RS, Hi-Maize), separately or combined, on glucose tolerance, related metabolic parameters and markers of gut fermentation in healthy subjects. Methods Evening reference and test products were: (1) reference white wheat flour bread (WWB), WWB supplemented with (2) AXOS and RS (WWB + AXOS + RS), (3) an increased content of either AXOS (WWB + hiAXOS) or (4) RS (WWB + hiRS). At the subsequent standardized breakfast, blood was sampled for 3 h to monitor glucose, insulin, nonesterified fatty acids, glucagon-like peptide (GLP)-1 and GLP-2. Breath hydrogen (H2) and short chain fatty acids (SCFA) were measured as markers of gut
Electronic supplementary material The online version of this article (doi:10.1007/s00394-015-0985-z) contains supplementary material, which is available to authorized users. * Elin M. Östman Elin.Ostman@food‑health‑science.lu.se 1
Food for Health Science Centre, Lund University, Lund, Sweden
2
Laboratory of Food Chemistry and Biochemistry and Leuven Food Science and Nutrition Research Centre (LFORCE), Department of Microbial and Molecular Systems (M2S), KU Leuven, Leuven, Belgium
fermentation, and subjective appetite was rated using visual analog scales. Results Dose-dependent decreases in glucose responses were observed with increased AXOS over the duration of 3 h. Insulin sensitivity index was improved in the morning after the WWB + hiAXOS evening meal. An increase in breath H2 concentration and circulating SCFA was observed in the morning after both evening meals containing AXOS. Conclusion The present study indicates that AXOS have the potential of improving glucose tolerance in an overnight perspective and suggested mechanisms are improved insulin sensitivity and increased gut fermentation. Keywords Arabinoxylan oligosaccharides · Resistant starch · Glucose tolerance · Gut fermentation · Healthy subjects · Overnight
Introduction The world prevalence of diabetes is rapidly increasing and is estimated to go from 285 million adults in 2010 to 439 million in 2030 [1]. The metabolic syndrome (MetS) is a cluster of cardiovascular risk factors that predict a high risk of developing diabetes. Consequently, individuals with MetS and insulin resistance have up to fivefold higher risk of developing diabetes than healthy individuals [2]. The importance of a tight glycemic control has been identified as preventive against manifestations of the MetS, such as obesity, diabetes and cardiovascular disease [3]. This makes it relevant to investigate and explore novel food ingredients and their ability to influence the postprandial blood glucose responses in healthy subjects. The mechanisms whereby specific foods, e.g., starchy products, influence
13
acute glycemia involve both physiological factors, such as enzymatic availability, and food properties such as food structure, e.g., botanical, physical and/or chemical structure [4, 5]. In addition, the presence of certain food components (e.g., slow or indigestible carbohydrates) has shown to beneficially affect the glycemic response at a subsequent meal, through mechanisms related to gut fermentation [6, 7]. Previously, we have shown that a white wheat flour-based bread (WWB), with added dietary fiber (DF) in form of nonstarch polysaccharides (NSP) from barley, and resistant starch (RS) from high amylose maize, in levels corresponding to those of a whole-kernel based barley bread, induced similar benefits to overnight glucose tolerance as a wholekernel barley bread [8]. The overnight benefits on glucose tolerance were suggested to be mediated by gut fermentation of the specific mix of indigestible substrates. A relatively new candidate substrate evaluated for its prebiotic potential is the arabinoxylan oligosaccharides (AXOS). These are degradation products of arabinoxylans (AX) which are formed during treatment of wheat with xylanase enzymes [9]. So far, AXOS have been shown to modulate intestinal fermentation and overall gastrointestinal properties in healthy humans [10], with specific growth of bifidobacteria in both adults [11, 12] and preadolescent children [13]. Furthermore, supplementation of AXOS for 8 weeks improved specific gut hormones and markers of inflammation in diet-induced obese mice [14]. However, to the best of our knowledge, there is no information about metabolic effects of AXOS on, e.g., semi-acute glycemic regulation and gut hormones in humans. The aim of this study was to investigate the potential metabolic benefits of AXOS-rich wheat bran extract (WBE), alone or in combination with RS, in white wheat flour-based breads on overnight glucose tolerance, markers of gut fermentation as well as changes in gut-derived hormones in healthy young adults. To further explore specific metabolic effects of RS, white wheat flour-based breads with increased amounts of RS were included in the study.
Experimental methods Test subjects Nineteen healthy volunteers, 9 men and 10 women aged 23 ± 0.4 years, with normal body mass index, 22.2 ± 0.4 kg/m2, participated in the study. The inclusion criteria were 20–35 years, BMI 19–25 kg/m2, nonnicotine user (smoking, snuff) and no known metabolic disorders or food allergies. Furthermore, the test subjects were instructed to not consume antibiotics or probiotics during the previous 2 weeks and throughout the study. Recruitment of test subjects was performed by local
13
Eur J Nutr
advertisement around Lund University, and the study was performed between April and December 2009. This study was conducted according to the guidelines laid down in the Declaration of Helsinki, and the study was approved by the Regional Ethical Review Board in Lund, Sweden (668/2008). Written informed consent was obtained from all subjects. Study design and sampling procedures Four bread products (three test products and one reference product) were included in the study. The test and reference products were provided to the test subjects as late evening meals in a randomized, cross-over design. Both the test and reference products, as well as the standardized breakfast, were equi-carbohydrate portions of 50 g potentially available starch. Each subject participated on four different occasions, approximately 1 week apart. The subjects were instructed to standardize their meal pattern and to avoid alcohol, excessive physical exercise or food rich in DF during the entire day before each experiment. The test and reference products were given to the subjects as frozen portions, and they were instructed to eat the four products in a pre-decided randomized order. At the day of consumption, the bread portion was thawed in ambient temperature, still wrapped in aluminum foil and in the plastic bag. The bread was consumed together with 250–300 ml water at 21.30 hours (h) in the evening. After ingestion of the test or reference product, the subjects were fasting until the standardized breakfast was served in the experimental unit. The subjects arrived at 07.40 h in the morning, and an intravenous cannula (BD Venflon, Becton–Dickinson) was inserted into an antecubital vein for blood sampling. Fasting blood samples were collected, and subjective appetite sensations and breath H2 were registered before the breakfast, which was then served 10.5 h after consumption of the evening meal. The breakfast was served with 300 ml water and had to be finished within 15 min. Test variables were determined repeatedly in the postprandial period (3 h) after the breakfast. Blood (b)-glucose, serum (s)insulin, plasma (p)-GLP-1, breath H2 and subjective appetite ratings (measured with visual analog scales, VAS [15]) were obtained at fasting and 15, 30, 45, 60, 90, 120 and 180 min after commencing the breakfast. Samples for s-nonesterified fatty acids (s-NEFA) and p-GLP-2 were collected at fasting, and samples for p-SCFA were measured at fasting and 120 min. The test subjects were instructed to maintain a low physical activity during the experiments. The test subjects were instructed to complete a tolerance questionnaire with questions regarding the acceptance of the evening test and reference products related to gastrointestinal discomfort. The questionnaire was completed at two occasions for each test product. The first questionnaire was completed just before the onset of the evening test or
Eur J Nutr
reference meal and the second questionnaire approximately 48 h later.
Table 1 Theoretical contents of AXOS, glucans and RS in the evening bread meals Meals
Description of standardized breakfast, reference and test products White wheat flour bread was used both as the reference product and as the standardized breakfast. All three test products were based on white wheat flour but varied in amounts of AXOS and/or RS. The first test product (WWB + AXOS + RS) was designed to mimic the combined NSP + RS product studied previously [8]. However, the major contribution of indigestible material in the present product originated from AXOS-rich WBE as opposed to the previously studied NSP from barley. The second product was a WWB supplemented with increased content of RS only (WWB + hiRS), and the third product was a WWB with increased content of AXOS (WWB + hiAXOS) and no added RS. All bread products were baked in a home bread-making machine according to the standardized procedure described previously [16]. Common ingredients were: white wheat flour (Vetemjöl special, Kungsörnen AB, Järna, Sweden), dry yeast (KronJäst, Jästbolaget AB, Sollentuna, Sweden) and NaCl (Falksalt, AB Hanson & Möhring, Halmstad, Sweden). After cooling, the crust was removed and the bread was sliced. Portions corresponding to 50 g potentially available starch were wrapped in aluminum foil, put into plastic bags and stored in a freezer (−20 °C). The theoretical contents of AXOS and RS in the bread products are shown in Table 1. WWB (reference product and standardized breakfast): 540 g white wheat flour, 360 g water, 4.8 g dry yeast and 4.8 g NaCl. WWB + AXOS + RS: 480 g white wheat flour, 360 g water, 120 g high amylose maize starch (Hi-Maize™ 260, Ingredion Incorporated, Bridgewater, NJ, USA), 90 g AXOS-rich WBE (Brana Vita™ 200, Fugeia NV, Heverlee, Belgium), 6 g dry yeast and 6 g NaCl. WWB + hiAXOS: 495 g white wheat flour, 330 g water, 165 g AXOS-rich WBE (Brana Vita™ 200, Fugeia NV, Heverlee, Belgium), 5.5 g dry yeast and 5.5 g NaCl. WWB + hiRS: 400 g white wheat flour, 400 g water, 270 g hi-amylose maize starch (Hi-Maize™ 260, Ingredion Incorporated, Bridgewater, NJ, USA), 5 g dry yeast and 5 g NaCl. Chemical analysis of evening meals and standardized breakfast The WWB and test products were analyzed with respect to potentially available starch [17]. In addition, the test
Glucansa
RSb
Portion size
Dry matter
AXOS
g
%
g/portion (wet weight)
WWB
116.2
55.0
–
WWB + AXOS + RS
140.5
57.1
8.9
WWB + hiAXOS
141.4
60.8
18.4
WWB + hiRS
137.9
52.4
–
