Evaluation of the Relative Available Energy of Several Dietary Fiber Preparations Using Breath Hydrogen Evolution in Healthy Humans
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J Nutr Sci Vitaminol, 60, 246–254, 2014 Evaluation of the Relative Available Energy of Several Dietary Fiber Preparations Using Breath Hydrogen Evolution in Healthy Humans Tsuneyuki OKU and Sadako NAKAMURA Graduate School of Human Health Science, University of Nagasaki, Siebold, Nagasaki 851–2195, Japan (Received December 9, 2013) Summary A standardized simple, indirect method for assessing the relative energy of dietary fiber carbohydrates is not yet established. There is a need for a standardized in vivo assay. The objective of the present study was to evaluate the relative available energy (RAE) for 9 major dietary fiber materials (DFMs) based on fermentability from breath hydrogen excretion (BHE) in subjects. Fructooligosaccharide (FOS) was used as a reference. The study was conducted using a within-subject, repeated measures design and approved by the Ethi- cal Committee of University of Nagasaki. After DFM ingestion, end-expiratory gas (750-mL) was collected at 1-h intervals for 8 h, as well as at 2-h intervals between 8 h and 14 h, and 30 min after waking up and 24 h after DFM ingestion. Breath hydrogen concentration was assessed with a gas chromatograph. The RAE of DFMs tested was evaluated based on the area under the curve (AUC) of BHE of FOS. Based on the ratio of AUC for 8 h, the RAE of polydextrose, partially hydrolysed guar gum, resistant maltodextrin and partially hydrolysed alginate was 1 kcal/g, and that of glucomannan, heat-moisture treatment and high-amy- lose cornstarch and cellulose was 0 kcal/g, while the RAE of all tested DEMs including cel- lulose and glucomannan was 1 kcal/g in the calculation based on AUCs for 14 h and 24 h in subjects. We suggest that a breath hydrogen collection period of 14 h or more could be used to measure RAE for a range of fiber preparations in vivo. Key Words relative available energy, dietary fiber, fermentability, breath hydrogen Dietary fiber (i.e., largely indigestible carbohydrates) However, this is not practical, because balance studies has beneficial effects for health and is actively used in are time-consuming, expensive, and very stressful for health foods and functional foods (1, 2). Dietary fiber subjects. Although an indirect and simple method to taken orally reaches the large intestine without being evaluate the available energy of nondigestible carbohy- digested by a-amylase or disaccharidases present in the drates is desirable, it has not been established yet. mucosa of the small intestine. In the large intestine, The amount of available energy of nondigestible dietary fiber is fermented to varying degrees by intes- and fermentable carbohydrates is dependent upon the tinal microbes and metabolized into short chain fatty amount of short-chain fatty acids produced in the fer- acids, carbon dioxide, hydrogen, methane, and bacterial mentation by intestinal microbes. Thus, energy produc- cell components (3–6). Among them, short-chain fatty tion is dependent on the fermentability of nondigestible acids are absorbed from the large intestine and used carbohydrates which reach the colon. We estimated the solely as the energy source of the host. That is, even relative available energy value (RAE) of dietary fiber carbohydrates that are not digested and not absorbed materials (DFMs) based on the breath hydrogen excre- provide available energy to a living body by being fer- tion (BHE) and calculated the relative ratio versus the mented and absorbed in the large intestine (5). amount of hydrogen excretion from the ingestion of Energy values for fermentable fibers are an important fructooligosaccharide (FOS), which is fermented com- matter for regulatory bodies as they are incorporated pletely by intestinal microbes. Therefore, the profile of into on-pack labels, and for weight control products, BHE seems to be different from the fiber sources. But, as a help to direct consumer choice (2). The available FOS is a convenient reference because it is fermented energy of nondigestible carbohydrate in humans is eval- completely by intestinal microbes. Besides, FOS has been uated using balance studies and other methods (7, 8). classified as a nondigestible carbohydrate of which the energy value is 2 kcal/g by the Japanese Health Promo- E-mail: [email protected] tion Law (9). In this study we expressed the energy val- Abbreviations: AOAC, Association of Official Analytical Chemists; AUC, area under the curve; BHE, breath hydrogen ues derived from the indirect method as the relative ratio excretion; DFMs, dietary fiber materials; FOS, fructooligosac- to FOS. charide; GM, glucomannan; HMT-HACS, heat-moisture treat- In the nutrition labelling for processed foods, the ed, and high amylose cornstarch; PD, polydextrose; PHAA, indication of energy is an essential item. The available partially hydrolysed alginic acid-Na; PHGG, partially hydro- energy derived from digestible carbohydrates is 4 kcal/g. lysed guar gum; RAE, relative available energy; RMD, resistant However, that of nondigestible carbohydrates is not maltodextrin. known because the available energy derived from nondi- 246 Evaluating Relative Energy of Dietary Fiber 247 Table 1. Preparation of test materials. Soluble fibers Polydextrose (Lytes; Danisco Japan Ltd.) Resistant maltodextrin (Fibersol-2; Matsutani Chemical Industry Co., Ltd.) 5 g of test substance was dissolved in 120 mL of soup. Partially hydrolyzed guar gum (Sunfiber-PG; Taiyo Kagaku Co., Ltd.) Partially hydrolyzed sodium alginate (Sorgin granule; Kaigen Co., Ltd.) Glucomannan 5 g of glucomannan was gelated in 120 mL of soft drink (Propol-A; Shimizu Chemical Corp.) over 24 h. Insoluble fibers HMT-HACS (Loadstar; Nihon Shokuhin-Kako Co., Ltd.) 5 g of test substance was suspended in 120 mL of potage. Cellulose (Avicel; Asahi Kasei Chemicals Corp.) Possitive control Fructooligosaccharide 5 g of FOS was dissolved in 120 mL of water. (Meiji Seika Kaisha Ltd.) HMT-HACS: heat-moisture treated, high amylose cornstarch. gestible and fermentable carbohydrates such as oligosac- to participate in the study. All experiments were carried charides cannot be evaluated for common foods listed in out in the Public Health Nutrition Laboratory of the standard food tables. To estimate the available energy Graduate School of Human Health Science, Siebold Uni- from nondigestible and/or nonabsorbable carbohydrates versity of Nagasaki. such as oligosaccharides and sugar alcohols, we pro- Subjects. Nine healthy females, aged 21.860.6 y posed a unique and simple method which enables calcu- and with a BMI of 20.162.4 kg/m2, voluntary partici- lation from the fermentation equations with the ratio of pated in this study. The exclusion criteria were a history short-chain fatty acids produced by intestinal microbes of gastrointestinal diseases, carbohydrate malabsorp- (10–13), and demonstrated that a carbohydrate which tion, obesity, or pulmonary disease. The average and is fermented completely has an energy available value standard deviation (SD) values of fasting blood glucose of 2 kcal/g. This value is used for nutrition labelling in levels of the subjects was 82.764.1 mg/100 mL. Prior The Japanese Health Promotion Law (9). The estimated to the experiments, we ensured that all of the subjects available energy based on BHE is classified into three were hydrogen producers and not methane producers. energy categories, 0 kcal/g, 1 kcal/g, and 2 kcal/g, The subjects had not taken antibiotics or laxatives for which are expressed as integers for the necessity of prac- 2 wk prior to the experiments. tical use in the calculation of nutritional intake. Materials. To evaluate the available energy, DFMs We have proposed an indirect and simple method and which are frequently used in foods for specified health tried to evaluate the energy available from some DFMs uses and functional foods were chosen. The water solu- based on the fermentability from BHE for 8 h (13). The ble dietary fiber materials were polydextrose (PD), resis- results obtained were different from the energy coef- tant maltodextrin (RMD), partially hydrolysed guar gum ficients of DFMs based on the fermentability obtained (PHGG), partially hydrolysed alginic acid-Na (PHAA) from animal and human experiments in the Japanese and glucomannan (GM); water insoluble dietary fiber Health Promotion Law. Furthermore, the values of materials were heat-moisture treated high amylose corn- available energy obtained were not correct because the starch (HMT-HACS) and cellulose. period of breath-gas collection for 8 h to calculate the PD (Lytes, Danisco Japan Ltd., Tokyo, Japan) was a fermentability was too short. Therefore, in the present mixture of polymers in which glucose, sorbitol and study, we collected breath gas for 24 h after the inges- citrate (90 : 9 : 1) were condensed under high pressure tion of DFMs, and tried to evaluate again the RAE of and high temperature, and had an average molecular DFMs in healthy human subjects. weight of 1,500. It contained ~25% of monosaccha- rides and oligosaccharides. The available energy of PD MATERIALS AND METHODS has been estimated as 0.8–1.2 kcal/g by other meth- All of the experiments complied with the code of eth- ods, administered orally as 14C-polydextrose to rats and ics of the World Medical Association (Declaration of humans (14, 15). RMD (Fibersol-2, Matsutani Chemical Helsinki, Oct. 2008). The study protocol was approved Industry Co., Ltd., Osaka, Japan) is a mixture of mono- by the Ethical Committee of Siebold University of Naga- saccharides, oligosaccharides and glucose polymers, saki (received No. 41–1, approval No. 39, Nagasaki, and contains 93.73% dietary fiber (by the Association of Japan). All subjects provided written informed consent Official Analytical Chemists (AOAC) method). The aver- 248 OKU T and NAKAMURA S age molecular weight was ~2,000. The available energy refrigerator overnight (13). of RDM has been estimated as 0.98 kcal/g by indirect Special meals for experiments. The period over which calorimetric measurements in healthy adults (7).