Effects of Fructooligosaccharides Intake on the Intestinal Microflora and Defecation in Healthy Volunteers

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1 Effects of Fructooligosaccharides Intake on the Intestinal Microflora and Defecation in Healthy Volunteers Takahisa Tokunaga, 1* Yuko Nakada, 1 Tashiro Yasuhito, 1 Masao Hirayama 1 and Hidemasa Hidaka 1 1* Bio Science Laboratories. Meiji Seika Kaisha, Ltd. ABSTRACT The effects of fructooligosaccharides (FOS) intake (1 g, 3 g and 5 g/day) for 2 weeks on the intestinal microflora and defecation were studied in 27 healthy volunteers (male 21, female 6) of three groups. The number of Bifidobacterium was significantly (p < 0.01 or p < 0.05) increased during FOS intake period in all the dose levels. Fecal excretion was also investigated in all subjects during the study. Significant increase of stool frequency (p < 0.05) and softening effect on stool (p < 0.01) were observed. Key words: fructooligosaccharides, Bifidobacterium, fecal microflora, defecation INTRODUCTION The fructooligosaccharides (FOS hereafter) is the mixture of nondigestible sugars containing the I-ketose, nistose and fuructofuranosilnistose, and is made enzymatically from sucrose 3. This sweetener has following properties; low calorie content 6, low decay 7 and improving effect on intestinal microflora 2, 5. The effect of FOS intake on intestinal microflora has been studied in aged persons (1-8 g/day dose level) 4, 12, patients with hyperlipidemic and diabetes (1-4 g/day dose level) 11 and patients with chronic kidney failure 16. However, in trails in aged persons and/or patients, several factors such as decline in digestive function, taking the drug and diet restriction may affect intestinal microflora 10. Here, effects of FOS intake (1-5 g/day) on intestinal microflora and defecation were studied in healthy volunteers. * Chiyoda, Sakado , Japan 143

2 MATERIALS AND METHODS 1) Examinees and medication methods FOS intake trials have been performed in 27 healthy volunteers (21 males (36.8 ± 9.0 years old), 6 female (25.2 ± 3.3 years old)), who are classified into 3 groups according to the dose level (1, 3, 5 g/day) as shown in Table 1. Dosing samples (FOS) are prepared by mixing the MEI -OLIGIO G solution (FOS content of 44.6%; Meiji seika kaisha Ltd.) and sucrose, and have the same degree of sweetness for 3 groups. The amount of dosing per 1 meal is 70 g ( g carbohydrate), and amount of FOS are optimized at 1, 3 and 5 g/day for each group, respectively. Testing was conducted for six weeks, which is divided into 3 periods; (i) 2 weeks before FOS intake, (ii) 2 weeks during FOS intake and (iii) 2 weeks after FOS intake. Examinees were not informed about daily dose. During FOS intake period, examinees took dosing sample just after breakfast. During the study, examinees were not placed on a restricted diet, although intake of some food containing nondigestible sugars, fermented food and lactic acid bacterial beverage such as yogurt and fermented soybeans are restricted. 2) Stool sampling We took sampling of full stool specimen 1 time at the last day or a day before the last day of each period (before, during and after FOS intake), totally 3 times. Samples kept in plastic bags were stored at 5 ºC, and were used for intestinal microflora screenings in 4 hours. 144

3 3) Intestinal microflora screenings After homogenization of samples, intestinal microflora screenings were performed in reference to the method of Mitsuoka et al 9, 13. But, for screening of Clostridium perfringens, traditional NN medium and modified NN medium developed by Endo et al 1 (0.015% neomycin is replaced with % novobiocin (Sigma) or % colymicin (Kaken Pharmaceutical)) were used. The one where the number of bacteria is higher was made into the number of Clostridium perfringens. 4) Research on defecation During whole period, 27 volunteers filled out the survey sheet (as shown in Table 2) every day. After this work, the survey sheets were collected. 5) Statistical analysis Intestinal microflora: The number of cell was expressed with the common logarithms per 1 g of stool, and 145

4 occurrence is percentage of volunteers by whom the cell was detected. The paired t-test was performed for the number of cells of the same volunteer in each period (before, during and after FOS intake) by taking into account individual difference. Simple correlation analyses are performed between increase of Bifidobacterium during FOS intake period and the number of Bifidobacterium before FOS intake period. In addition, simple correlation analyses are performed also between the average count of Bifidobacterium in each dosing period (before, during and after FOS intake) for each dose level (1, 3, 5 g/day) and occurrence of Clostridium perfringens. Defecation: The average frequency of defecation was obtained by dividing frequency in each period (before, during and after FOS intake; 2 weeks for each) by days. Several factors such as quantity, hardness, color and odor of stool and feeling after defecation are quantified as reported by Nakagawa et al 14 (see Table 2) and were analyzed as the average score per 1 defecation. The paired t-test was used for this analysis. This work is based on the Helsinki declaration and was performed with informed consent. RESULTS Effects of FOS intake on intestinal microflora analyzed for 15 types of bacteria are shown in Table 3. The number of Bifidobacterium significantly increased during FOS intake period in all the dose levels. Even in the case of the 1 g/day dose level, the number of Bifidobacterium increased from /g to /g (about 2.5 times). As the dose level increased, 146

5 the number of Bifidobacterium also increased during FOS intake period; about 3.2 times for the 3 g/day dose level, and about 4 times for the 5 g/day dose level. As shown in Figure 1, a significant (p < 0.01) negative correlation (r = ) was observed between logarithm of the number of Bifidobacterium before FOS intake and that of the increase of Bifidobacterium during FOS intake. Moreover, the increase of Bifidobacterium during FOS intake was large in volunteers with few Bifidobacterium before FOS intake. The number of Eubacterium significantly increased during FOS intake period in all the dose levels, and that after FOS intake period is significantly larger than that before FOS intake period. The total counts also significantly increased during and/or after FOS intake period (there are significances in 1 and 5 g dosing levels). Significances were observed also for Bacteroidacease, Enterobacteriaceae, Streptococcus and Lactobacillus, though it is not clear that these significances are from the effects of FOS intake. For Clostridium perfringens, occurrence decreased during FOS intake in all the dose levels. A significant (p < 0.05) negative correlation (r = ) was observed 147

6 between the average number of Bifidobacterium and the occurrence of Clostridium perfringens in healthy volunteers (see Figure 2). The ph of stool decreased on an average of 0.4 in the 1 g/day dose level, but its significance was not observed. There was no effect of FOS intake on the ph of stool in the 3 and 5 g/day dose levels. Effects of FOS intake on defecation in 27 healthy volunteers are shown in Table 4. By FOS intake, frequency significantly increased (p < 0.05), and hardness of stool became softer (p < 0.01). Since all volunteers are healthy adults, the average scores of frequency and hardness remain at levels which are considered as normal values (Frequency = 1-2 times/day; Hardness of stool = 3(medium) -4(soft)). To analyze obtained results in more detail, volunteers are categorized into 3 types; subjects liable to be constipated who have no defecation for more than 2 days before FOS intake period (1-2 weeks), subjects liable to be diarrhea who have more than 3 times/day frequency before FOS intake period (1-2 weeks), and others. Effects of FOS intake on frequency and hardness of stool in each type are shown in Figure 3 and 4. Especially for subjects liable to be constipated, significant increase of frequency and softening of stool by FOS intake are observed. DISCUSSIONS It has been confirmed by experimental results of a poll of healthy adults that the number of Bifidobacterium is FOS intake -dependent; it significantly increased during FOS intake period even in low dose levels (2.5, 3.2 and 4 times in 1, 3 and 5 g/day dose levels, respectively), and it returns to the initial level after stop FOS intake. This result is almost consistent with previously reported results of a poll of aged person 4, 12 and patients with diabetes (more than 8 g/day dose level) 15. The increase of Bifidobacterium during FOS intake is large in volunteers with few Bifidobacterium before FOS intake. It is attributed to the fact that these volunteers take less Bifidobacterium growth factors in daily diet, and thereby Bifidobacterium growth was more stimulated by FOS intake in them than in other volunteers. The number of Bacteroidaceae and Eubacterium also significantly increased during FOS intake period. Unlike Bifidobacterium, these counts were maintained at high level even after FOS intake period. These results suggest that while the number of Bifidobacterium strongly dependent on FOS intake, those of Bacteroidaceae and Eubacterium are affected by indirect effect of FOS intake 148

7 such as changing balance of intestinal microflora. In order to confirm this hypothesis, further experiments will be needed. Although it has been reported that FOS intake result in increase of short-chain fatty acid in stool 2 and thereby ph of stool decrease 12, significant decrease of ph was not observed in this study. On the other hand, it has been reported that although 60% of FOS are metabolized to short-chain fatty acid when about 6 g of 14 C-labeled FOS is taken, the amount of radioactive carbon in stool is less than 10%, meaning that almost all short-chain fatty acid is absorbed into large intestine 6. In the case of high FOS intake, a large amount of short-chain fatty acid would be produced, and some amount of them may be not absorbed into large intestine resulting in decrease of ph. However, in the case of low FOS intake as in this study, almost all short-chain fatty acid may be absorbed into large intestine because of its fewer amounts. Therefore, it can be concluded that FOS intake did not affect ph of stool in this study. Although effects of FOS intake on defecation were observed as significant increase of frequency and softening of stool, they were not dependent on FOS dose levels. There was no significant correlation between the number of Bifidobacterium and defecation. As shown in Figure 3 and 4, these factors may be largely dependent on individual constitute of volunteers. Prior to this work, a survey was conducted on the opinions of healthy adults about defecation to understand their wish and current condition about defecation. As a result, it has been revealed that more than half of healthy adults think that appropriateness of frequency and hardness of stool are the important factor of improvement of defecation, and that they want improvement of frequency (to 1-2 times/day) and hardness of stool (to medium-soft hardness). According to the national nutrition survey by Ministry of Health and Welfare (Japan) 8, persons who have no defecation for more than 2 days are defined as constipated persons; that means defecation frequency of 1 or 2 times/day is considered to be appropriate. For that reason, the fact that average frequency was increased and hardness of stool was improved from hard to medium or soft in volunteers who are categorized as subjects liable to be constipated may be the expression of curative properties against defecation by FOS intake (i.e. intestinal function control). It can be thought that intestinal function control may be expressed by improvement of intestinal microflora induced by increase of Bifidobacterium. In order to understand a correlation between Bifidobacterium and expression of intestinal function control by FOS intake, further experiments will be needed. REFERENCES (1) Endo, K., M. Kumemura, K. Nakamura, T. Fujisawa, K. Suzuki, Y. Benno, and T. Mitsuoka Effect of high cholesterol diet and polydextrose supplementation on the microflora, bacterial enzyme activity, putrefactive products, volatile fatty acids (VFA) profile, weight, and ph of the feces in healthy volunteers. Bifidobacteria Microflora 10: (2) Hidaka, H., T. Eida, T. Takizawa, T. Tokunaga, and Y. Tashiro Effects of fructo-oligosaccharides on intestinal flora and human health. Bifidobacteria Mic roflora. 5:37-50 (3) Hidaka, H., M.Hirayama, and N. Sumi A fructooligosacchardie-producing enzyme from Aspergillus 149

8 niger ATCC Agric. Biol. Chem. 52: (4) Hidaka, H., M.Hirayama T. Tokunaga, and T. Eida The effects of undigestible fructo-oligosaccharides on intestinal microflora and various physiological functions on human health, p In I. Furda and J. Brine (eds), Advances in experimental medicine and biology, volume 270, New developments in dietary fiber, Plenum Press New York. (5) Hidaka, H.,Y. Tashiro, and T. Eida Proliferation of Bifidobacteria by oligosaccharides and their useful effect on human health. Bifidobacteria Mic roflora 10: (6) Hosoya, N., B. Dhorranintra, and H. Hidaka Utilization of [U-14C] Fructooligosaccharides in man as energy resources. J. Clin. Biochem. Nutr. 5: (7) Ikeda, T., T. Kurita, H. Hidaka, S.M. Michalek, and M. Hirasawa Low-cariogenicity of the tetrasaccharide nystose. Gen. Pharmacol. 21: (8) Ministry of Health and Welfare Actual status of nation s nutrition, p. 52. Daiichi shuppan, Tokyo. (9) Tomotari Mitsuoka World of intestinal bacteria, p Soubunsya, Tokyo. (10) Mitsuoka, T., H. Hidaka, and T. Eida Recent trends in research on intestinal flora. Bifidobacteria Microflora 1: (11) Tomotari Mitsuoka, Hata Yoshiya, Yuichiro Takahashi Long-term administration test of Neo-Sugar. edt. Narimasa Hosoya, 3rd Neo-Sugar debrief session, p Association of Neo-Sugar workshop, Tokyo. (12) Mitsuoka, T., H. Hidaka, and T. Eida Effect of fructooligosaccharides on intestinal flora. Die Nahrung 31: (13) Mitsuoka, T., T. Sega, and S.Yamamoto Eine verbresserte Methodik der gralitativen und quantitativen analyse der darmflora von menshen und tieren. Zentralbl. Bakteriol. I. Abt. Orig. A195: (14) Yasue Nakagawa, Hiroshi Okamatsu, Yasuhiro Fujii Effects of poly-dextrose intake on feeling after defecation in adult female. Journal of Japanese Society of Nutrition and Food Science 43: (15) Takashi Sano Application of Neo-Sugar to patients with diabetes. 2nd Neo-Sugar debrief session, p Association of Neo-Sugar workshop, Tokyo. (16) Yuichiro Takahashi, Yu Takagi, Masayo Toda, Chiyoko Kashiwabara, Reiko Ishiyama, Toshio Kinoshita Application of Neo-Sugar to patients with chronic renal failure. 2nd Neo-Sugar debrief session, p Association of Neo-Sugar workshop, Tokyo. 150

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