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© 2004 The American Society for Nutritional Sciences J. Nutr. 134:1523-1528, June 2004

Nutrition and Cancer

Xylooligosaccharides and Fructooligosaccharides Affect the Intestinal Microbiota and Precancerous Colonic Lesion Development in Rats1

Cheng-Kuang Hsu*, Jiunn-Wang Liao{dagger}, Yun-Chin Chung**, Chia-Pei Hsieh** and Yin-Ching Chan**,2

* Department of Biological Science and Technology, Taichung Healthcare and Management University, Wufung, Taiwan, Republic of China; {dagger} Division of Applied Toxicology, Taiwan Agricultural Chemical and Toxic Substances Research Institute, Taichung, Taiwan, Republic of China; and ** Department of Food and Nutrition, Providence University, Taichung, Taiwan, Republic of China

2To whom correspondence should be addressed. E-mail: ycchan{at}pu.edu.tw.


   ABSTRACT
TOP
 ABSTRACT
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Certain nondigestible oligosaccharides can be selectively utilized by probiotics and reduce the risk of colon cancer. However, the inhibitory effects of xylooligosaccharides (XOS) on colon cancer are not well documented. This study evaluated the effects of xylooligosaccharides and fructooligosaccharides (FOS) on the alteration of cecal microbiota, cecal pH, cecal weight, and serum lipid levels, and also their inhibitory effect on precancerous colon lesions in male Sprague-Dawley rats. The rats were randomly assigned to 4 groups: control, treatment with 1,2-dimethylhydrazine (DMH) [15 mg/(kg body wt · wk) for 2 wk], treatment with DMH + 60 g XOS/kg diet, and treatment with DMH + 60 g FOS/kg diet. Rats were fed the experimental diets for 35 d, beginning 1wk after the second dose of DMH. Both XOS and FOS markedly decreased the cecal pH and serum triglyceride concentration, and increased the total cecal weight and bifidobacteria population. XOS had a greater effect on the bacterial population than did FOS. Moreover, both XOS and FOS markedly reduced the number of aberrant crypt foci in the colon of DMH-treated rats. These results suggest that XOS and FOS dietary supplementation may be beneficial to gastrointestinal health, and indicate that XOS is more effective than FOS.

KEY WORDS: • prebiotic • xylooligosaccharides • fructooligosaccharides • bifidobacteria • aberrant crypt foci

Differences in the colonic microflora have been suggested as an important factor contributing in the incidence of colon cancer. Recent reports indicate that bifidobacteria are associated with decreased illness and the suppression of potentially pathogenic and putrefactive bacteria in adults (1–4). Kubota (5) reports that the incidence of colon cancer and the population of Clostridium perfringens decrease as the population of bifidobacteria increases. Sanders (6) suggests that bifidobacteria could modulate the enzyme activities of colon bacterial populations that are associated with disease or tumor promotion in animals.

Certain indigestible oligosaccharides may benefit the gastrointestinal tract via fermentation and the proliferation of desirable bacterial species. For example, fructooligosaccharide (FOS)3 promotes the growth of bifidobacteria in vivo (1,2), and xylooligosaccharide (XOS) is extensively used by several species of bifidobacteria (7). Moreover, Jenkins et al. (8) showed that inulin and oligofructose (OF) markedly increase the population of colonic bifidobacteria, and this increase promotes both colonic and systemic health via modification of the intestinal microflora. Yazawa et al. (9) explained that bifidobacteria are able to suppress pathogenic bacteria (i.e., Escherichia coli) because they utilize oligo- and polysaccharides that other intestinal bacteria cannot use. Campbell et al. (10) suggested that FOS, OF, and XOS exert beneficial effects on gastrointestinal health by increasing the bifidobacteria population, supplying SCFAs, and lowering the colonic pH. These findings suggest that oligosaccharide supplementation could modify the population and metabolic characteristics of the gastrointestinal bacteria, which might in turn modulate enteric functions and provide resistance to colorectal cancers (11).

Aberrant crypt foci (ACF) are characterized by a larger size and thicker lining of epithelial cells than normal crypts, and they form putative preneoplastic lesions in colon cancer (12). Therefore, ACF could be used as a biomarker to study colon carcinogenesis (13–15). Several studies indicate that the administration of bifidobacteria or lactobacilli alone or with fermentable oligosaccharide could modify colonic microflora populations and decrease the development of aberrant crypts and tumors in the colon (11,16–19). Dietary XOS is also reported to promote the growth of bifidobacteria, lower the fecal pH, and maintain fecal water content within the normal range (7). However, the effects of XOS on colon cancer are still not well understood. Therefore, the present study evaluated the effects of XOS on the cecal microbiota, fecal pH level, cecal weight, and serum lipid levels, as well as its inhibitory effect on aberrant crypt formation, in rats treated with 1,2-dimethylhydrazine (DMH).


   MATERIALS AND METHODS
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 ABSTRACT
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 LITERATURE CITED
 
    Animals and diets. Male Sprague-Dawley rats (n = 40, age = 6 wk) were purchased from the National Laboratory Animal Center, Taipei, Taiwan. The rats were individually housed in suspended stainless-steel wire-bottom cages in an environmentally controlled room (25 ± 2°C, 65 ± 5% relative humidity) with a 12-h light–dark cycle. The rats were fed a standard nonpurified diet for 1 wk, then randomly assigned to 4 treatment groups (10 rats/group): control, DMH (Sigma) (positive control), DMH + FOS (Fructooligo-95P; Meiji), and DMH+XOS (Xylooligo-95P; Suntory) (Table 1). For the FOS and XOS treatments, the starch in the basal diet was partially replaced with the supplement (60 g/kg). The animal research ethics committee at Providence University, Taichung, Taiwan, approved the study protocol.


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  		TABLE 1 Composition of the experimental diets

 
    Experimental design. A preliminary study showed that 2 weekly applications of DMH (15 mg/kg body wt) induced aberrant crypt formation in rats (data not shown). The rats in the DMH, XOS, and FOS groups were gavaged with 2 weekly doses of DMH dissolved in soybean oil; the control group received the same amount of untreated soybean oil. Dietary treatment began 1 wk after the second application of DMH. The XOS and FOS groups were fed the XOS and FOS experimental diets, respectively, for 35 d; the control and DMH groups were fed the basal diet. The rats were allowed free access to water and food. The rats were weighed weekly. At the end of the experimental period, the rats were anesthetized and killed by decapitation. Blood samples were collected and centrifuged at 1200 x g for 10 min to obtain serum. Serum levels of triglyceride (TG), total cholesterol, glutamate oxaloacetate transaminase (GOT), glutamate pyruvate transaminase (GPT), blood urine nitrogen (BUN), and creatinine were assayed by a commercial analytical service center (Lian-Ming) using enzymatic methods and an automatic analyzer (Synchron CX-7; Beckman).

After necropsy, the liver, kidneys, spleen, and cecum were weighed immediately. The sealed cecum and colon with their contents were separately weighed to determine their total weight, then opened in an anaerobic chamber (Electrotek Anaerobic Cabinet AW 400SG) with an oxygen-free mixed-gas atmosphere (85:5:10 N2:CO2:H2). The cecal contents were diluted 1:9 with distilled water. The pH of the cecal contents was measured using a Fisher Scientific Accumet 1001 pH meter (Fisher Scientific) fitted with an MI-410 microcombination pH electrode probe (Microelectrodes). After the contents of the cecum and colon were removed, the tissues were cleaned with water, blotted dry, and weighed to determine the cecal and colonic wall weights.

    Microbial culture medium and microbiota analyses. Bifidobacterium iodoacetate medium 25 (BIM-25) (20), used to culture Bifidobacterium species, was composed of 51 g/L reinforced clostridial agar (BBL Microbiology), 2 g/L nalidixic acid, 0.85 g/L polymyxin B sulfate, 5 g/L kanamycin sulfate, 0.25 g/L iodoacetic acid, and 2.5 g/L 2,3,5-triphenyltetrazolium chloride. The medium used for Clostridium perfringens was Tryptose-sulfite-cycloserine (TSC) (21), containing 15 g/L tryptose, 5 g/L yeast extract, 5 g/L soytone, 1 g/L ferric ammonium citrate, 1 g/L sodium metabisulfite, 0.1 g/L D-cycloserine, 20 g/L agar, and 1 g/L egg yolk. Desoxycholate agar (22) was purchased from DIFCO (Becton Dickinson Microbiology). The anaerobic dilution buffer (23) contained 0.2 g/L gelatin, 20 g/L MgSO4 · 7H2O, 0.25 g/L FeSO4 · 7H2O, 0.4 g/L MnSO4 · 2H2O, 0.5 g/L NaCl, and 1 g/L resazurin. The anaerobic culture media (BIM-25 and TSC) and anaerobic dilution buffer were prepared by a prereduced anaerobically sterilized method (24).

To determine the microbial counts of Bifidobacterium species, C. perfringens, and Escherichia coli, a serial dilution was made by mixing the cecal contents with dilution buffer, and 0.1 mL of the mixture was cultured using the spread-plate method. The Bifidobacterium species and C. perfringens were cultured anaerobically (Electrotek Anaerobic Cabinet AW 400SG) in an oxygen-free mixed-gas atmosphere (85:5:10 N2:CO2:H2) at 37°C for 48 h. E. coli were cultivated in Desoxycholate agar at 37°C for 24 h in an aerobic incubator (MIR 260; Sanyo Electric). Cecal contents were cultured with triplicate plates for the microbial colony count. The microbial count data were expressed as colony forming units/g wet sample.

    Assessment of aberrant crypts and foci. The development of colonic preneoplastic lesions (aberrant crypts) in the distal colon was used as an index of colon cancer risk. The efficacy endpoints used in this study were reductions in total ACF/colon and multicrypt clusters of aberrent crypts (>=2 crypts/focus), as described by Reddy (19). Aberrant crypts and foci were enumerated on a 2 x 5-cm section of the distal colon, about 2 cm from the anal end, using the methods of Bird et al. (14) and Reddy et al. (19) with some modifications. The colon was sliced and rinsed thoroughly with 9 g/L saline solution to remove the fecal contents, then opened longitudinally and fixed flatly in a 10% formalin buffer between 2 slides. The tissues were stained for 20 min with 2 g/L methylene blue chloride (Sigma) in saline, the sample was placed on the slide with the mucosal side up, and the number of aberrant crypt foci and the distribution of ACF in the focus were assayed under a low-power stereomicroscope. Aberrant crypts were defined as easily recognizable mucosal alterations that were characteristically larger and more elongated than normal crypts. The criteria used to define ACF were those of McLellan et al. (13). Crypt multiplicity was counted as the number of crypts in each focus and categorized as those containing up to 2, 3, and 4 ACF (19).

    Statistical analyses. All data were expressed as means ± SEM and analyzed using SPSS 8.0 software (SPSS). Data were evaluated by one-way ANOVA. The least significant difference test was used for pairwise comparisons when the F-test was significant. The correlations of the cecal pH to the total, wall, and content weight of the cecum and the cecal bacteria population were assessed by Pearson’s correlation method. Differences were considered to be significant at values of P < 0.05.


   RESULTS
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 LITERATURE CITED
 
    Growth and serum biochemistry. The body weight and food intake of the rats did not differ among the control, DMH, and 2 oligosaccharide diet groups (data not shown). Rats in the XOS and FOS groups had significantly lower serum TG concentrations (0.82 ± 0.11 and 0.82 ± 0.11 mmol/L, respectively) than those in the DMH group (1.24 ± 0.17 mmol/L), whereas serum cholesterol, GOT, GPT, BUN, and creatinine concentrations did not differ among the groups (data not shown). The total cecum relative weights of the XOS and FOS groups did not differ from one another but were markedly greater than those of the control and DMH (positive control) groups (Table 2). The colonic and cecal wall relative weights of the DMH and XOS groups were markedly greater than those of the control and FOS groups. The cecal wet contents relative weight of the FOS group was greater than those of the control and DMH groups, whereas those of the XOS and control groups did not differ from one another. The liver, kidney, and spleen relative weights did not differ among the groups.


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  		TABLE 2 Relative weight of the liver, kidneys, spleen, and cecum of rats in the control, DMH, DMH + XOS, and DMH + FOS groups1

 
    pH and microbiota populations in the colon contents. Compared with the control and DMH treatments, the XOS and FOS supplementations significantly lowered the cecal pH level and increased the population of bifidobacteria, whereas the population of C. perfringens did not differ among the 4 groups (Table 3). The XOS group had a smaller population of E. coli than the DMH group. The cecal total, wall, and wet contents weights and the cecal bifidobacteria population were inversely associated with cecal pH (P < 0.05) (Fig. 1). The cecal E. coli count was negatively associated with the cecal bifidobacteria count. These results indicated that XOS and FOS supplementation markedly lowered cecal pH and increased both cecal weight and the bifidobacteria population, effects that may promote the health of intestinal tract.


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  		TABLE 3 pH and microbiota population of the cecum contents of rats in the control, DMH, DMH + XOS, and DMH + FOS groups1

 


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  		FIGURE 1 Pearson correlations of cecal pH vs. cecal total weight (A), cecal pH vs. cecal wall weight (B), cecal pH vs. cecal contents weight (C), cecal pH vs. cecal bifidobacteria population (D), and cecal bifidobacteria population vs. cecal Escherichia coli population (E) in all DMH-treated rats (DMH, DMH+XOS, and DMH+FOS groups).

 
    Aberrant crypt foci formation. Both the XOS and FOS groups had markedly fewer ACF than the DMH group (Table 4). The incidence of crypt multiplicity for 1, 3, and 4 crypts/focus was markedly lower in the XOS and FOS groups than in the DMH group, whereas the incidence of 2 crypts/focus was lower only in the XOS group.


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  		TABLE 4 Aberrant crypt foci in the distal colon of Sprague-Dawley rats in the control, DMH, DMH + XOS, and DMH + FOS groups1

 

   DISCUSSION
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
LITERATURE CITED
 
Supplementation of a standard diet with 60 g/kg of XOS or FOS for 35 d did not affect the body weight and food intake of male Sprague-Dawley rats treated with the carcinogen DMH. In our previous study, administration of 20 g XOS/kg diet by gavage for 100 d markedly increased the body weight and food intake of male ICR mice, whereas there were no differences in the females. Younes et al. (25) reported that a diet supplemented with 75 g/kg of FOS or XOS for 10 d does not affect the body weight and food intake of Wistar rats. Campbell et al. (10) and Howard et al. (26) also found that FOS and XOS do not affect the body weight and food intake of male BALB/C mice or Sprague-Dawley rats. These results indicate that the effects of oligosaccharides on body weight and food intake might be affected by differences in the animal model, animal gender, experimental period, supplemental method, and dose and type of oligosaccharide used.

In the present study, rats in both the XOS and FOS groups had significantly lower serum TG concentrations than those in the DMH group. Delzenne et al. (27) reported that supplementation with 100 g FOS/kg diet lowers the TG level in rats. Fiordaliso et al. (28) reported that the daily intake of a diet containing 100 g/kg of OF by normolipidemic male rats decreases plasma TG due to changes in liver lipid metabolism. Tokunaga et al. (29) and Williams (30) suggested that oligosaccharides decrease the expression of the enzymes for fatty acid synthesis. Delzenne and Kok (31) also reported that OF decreases the gene expression of lipogenic enzymes. In the present study, dietary supplementation with XOS or FOS did not affect serum cholesterol levels. Vanhoof and De Schrijver (32) showed that inulin has no effect on plasma cholesterol concentrations in hypercholesterolemic rats, whereas it reduces cholesterol levels in normocholesterolemic rats, presumably by increasing the excretion of fecal neutral steroids and bile acids. Fiordaliso (28) also stated that supplementation with 100 g OF/kg diet decreases plasma cholesterol levels in normolipidemic male rats. Daily ingestion of 6–12 g oligosaccharides for 2–3 mo reduces total serum cholesterol in humans by 0.226–0.566 mmol/L (33,34). One possible mechanism by which probiotic bacteria might reduce serum cholesterol levels is via alteration of the intestinal microflora (34). For example, Tahri et al. (35) showed that growing bifidobacteria cells can remove cholesterol both by precipitation and assimilation in vitro. De Smet et al. (36) also found that certain probiotic bifidobacteria can deconjugate bile acids by enzymatic means, thereby increasing their rate of excretion. However, the hypothesis of cholesterol assimilation by probiotics is still controversial (37).

In the present study, the total cecal weights relative to body weight of both the XOS and FOS groups was markedly higher than that of the control and DMH groups (Table 2). Campbell et al. (10) also found that supplementation with 60 g/kg diet of FOS, OF, or XOS for 14 d markedly increases the cecal total and wall weights, and they suggested that this increase might be caused via the normalization of epithelial cell proliferation by SCFAs. In an in vivo study, Frankel et al. (38) documented the trophic effect of SCFAs on epithelial cell proliferation in rats. Howard et al. (26) also reported that XOS increases cecal cell density via a modest enhancement of cecal epithelial cell proliferation. Therefore, the production of SCFAs from XOS and FOS fermentation may normalize epithelial cell proliferation, which would decrease mucosal atrophy and account for the observed increases in cecal and colonic weights. In the present study, the relative colonic wall and cecal wall weights of the XOS group were markedly greater than those of the FOS group, indicating that XOS more effectively increased epithelial cell proliferation than FOS.

Several in vivo studies demonstrate that diets that supply oligosaccharides (e.g., inulin, OF, FOS, and XOS) selectively increase the intestinal tract population of bifidobacteria in animals and humans (7,39). In the present study, both the XOS and FOS groups had greater intestinal bifidobacteria populations than the DMH group, which was consistent with the results of other studies. The higher intestinal bifidobacteria counts in the oligosaccharide groups might be explained by the fact that the oligosaccharides cannot be digested by enzymes in the small intestine and cannot be utilized by most intestinal microflora other than probiotic species, such as bifidobacteria and propionibacteria (1,7,40). The XOS and FOS groups also had lower cecal pH levels than the control and DMH groups (Table 3), and pH was negatively associated with the bifidobacteria population (Fig. 1). Bifidobacteria can digest XOS and FOS to produce lactate and SCFAs, such as acetate, butyrate, and propionate (18,41,42). The production of SCFAs lowers the pH in the intestinal tract, and this decrease in colon pH is one proposed mechanism for the effect of bifidobacteria on colon bacteria (43,44). Therefore, XOS and FOS might act as a source of SCFA to the large bowel, resulting in a lower pH in the intestine. The present data also showed negative correlations between pH and the cecal total, contents, and wall weights (Fig. 1). The aforementioned production of SCFAs could lower the pH and also normalize epithelial cell proliferation; thus, it was reasonable to find these negative correlations.

Numerous studies report a high correlation between the number of aberrant crypts and the number of tumors that subsequently develop (45,46). Thus, the ACF count was used to present the initial lesion of colon cancer development in this study. Supplementation with 60 g/kg diet of XOS and FOS to 6-wk-old male Sprague-Dawley rats for 5 wk decreased the mean number of multicrypt clusters of aberrent crypts (>=2 crypts/focus) by 81 and 56%, respectively. In a study of the effects of dietary OF and inulin on azoxymethane-induced aberrant crypts in 7-wk-old male F344 rats, Reddy et al. (19) found that ingestion of 100 g/kg diet of OF and inulin for 7 wk decreased the mean number of multicrypt clusters (>=2 aberrant crypts/focus) by 23 and 36%, respectively. The current experiment used lower doses over a shorter feeding period, compared to Reddy et al. (19). Therefore, the data suggest that XOS and FOS more effectively inhibited the development of ACF in the colon than inulin or OF. The administration of bifidobacteria and Lactobacillus acidophilus also decreases tumor incidence and aberrant crypt and ACF counts in the colon (16,47), and the combination of bifidobacteria and OF reduces the incidence of colon cancer in rats treated with a carcinogen (17). The current data and the results of these earlier studies suggest that either dietary oligosaccharides or consumption of bifidobacteria could decrease the incidence of colon cancer (11,17,18). Bifidobacteria also decrease the formation of toxic fermentation products in the gastrointestinal tract (2,7,48), suggesting that the lower ACF counts in the XOS and FOS groups might be due to the increase in the bifidobacteria population.

A comparison between the XOS and FOS groups revealed that the XOS group had markedly greater colonic wall and cecal wall relative weights, and also a greater bifidobacteria population. Tomomatsu (49) reported that the effective daily doses of oligosaccharides (pure form) in humans are 3.0 g for FOS and 0.7 g for XOS, indicating that XOS may be more effective than FOS. The authors concluded that the greater colonic wall and cecal wall relative weights found in the XOS group may be an indirect result of the higher bifidobacteria population in this group. Because XOS is utilized more efficiently by bifidobacteria, it is likely that SCFA production would be greater. This increase in SCFA levels, in turn, would increase cell proliferation. However, there was no difference in the pH of the cecal contents between the XOS and FOS groups. Therefore, the above-mentioned mechanism might not be the only possible explanation for the positive correlation between the bifidobacteria population and the colonic wall and cecal wall weights.

In conclusion, dietary supplementation with XOS and FOS inhibited the development of precancerous lesions, promoted the growth of bifidobacteria, and lowered the cecal pH in rats. Therefore, diets containing XOS and FOS may be beneficial to gastrointestinal health. Furthermore, XOS supplementation was more effective than FOS supplementation.


   ACKNOWLEDGMENTS
 
The authors thank the Suntory Co., Ltd., Osaka, Japan, for supplying the XOS samples.


   FOOTNOTES
 
1 Supported by the National Science Council (NSC-90-2745-P-126-002), Taiwan, Republic of China. Back

3 Abbreviations used: ACF, aberrant crypt foci; BIM-25, Bifidobacterium iodoacetate medium 25; BUN, blood urine nitrogen; DMH, dimethylhydrazine; FOS, fructooligosaccharide; GOT, glutamate oxaloacetate transaminase; GPT, glutamate pyruvate transaminase; OF, oligofructose; TG, triglyceride; TSC, Tryptose-sulfite-cycloserine; XOS, xylooligosaccharide. Back

Manuscript received 30 October 2003. Initial review completed 22 December 2003. Revision accepted 3 March 2004.


   LITERATURE CITED
TOP
 ABSTRACT
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 DISCUSSION
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