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© 2006 American Society for Nutrition J. Nutr. 136:1198-1202, May 2006

Nutrient Physiology, Metabolism, and Nutrient-Nutrient Interactions

Inulin Alters the Intestinal Microbiota and Short-Chain Fatty Acid Concentrations in Growing Pigs Regardless of Their Basal Diet1–3,

Gunnar Loh*,4, Markus Eberhard*,4, Ronald M. Brunner*, Ulf Hennig*, Siegfried Kuhla*, Brigitta Kleessen{dagger} and Cornelia C. Metges*,5

* Research Institute for the Biology of Farm Animals, Dummerstorf, Germany and {dagger} Institute of Bacteriology and Mycology, Veterinary Faculty, University of Leipzig, Germany

5 To whom correspondence should be addressed. E-mail: metges{at}fbn-dummerstorf.de.


   ABSTRACT
TOP
 ABSTRACT
MATERIAL AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Inulin stimulates intestinal bifidobacteria in humans and rodents but its effect in pigs is inconsistent. We assessed the effect of inulin on the intestinal microbiota by fluorescent in situ hybridization in growing pigs (age 9–12 wk). Pigs (n = 64) were assigned to 2 types of basal diets [wheat and barley (WB) or corn and wheat gluten (CG)] with or without 3% inulin (WBI or CGI) for 3 and 6 wk (n = 8/group) to test whether naturally occurring dietary fibers influence the inulin effect. Intestinal organic acids, pH values, and residual inulin were determined. The composition of the microbiota was highly individual. The duration of feeding did not affect any of the variables tested; therefore, data for the 2 periods were pooled. Bifidobacteria were detected in less than half of the pigs. Inulin did not stimulate lactobacilli and bifidobacteria numbers irrespective of the basal diet, although 20–50% of inulin was degraded in the jejunum. The number of pigs with colonic bifidobacteria was higher in those fed diets containing inulin (40 vs. 13%; P < 0.05). Total colonic short-chain fatty acid (SCFA) concentrations were lower in both inulin-fed groups due to reduced acetate (P < 0.05). Proportions of colonic butyrate were higher in pigs fed inulin-supplemented diets (P < 0.05). Colonic pH tended to be lower in the WB groups (WB; 6.6 ± 0.6), and was higher due to inulin (CGI, 7.1 ± 0.1; P < 0.05). In conclusion, inulin affected intestinal SCFA and the number of pigs harboring bifidobacteria; this effect was independent of the basal diet.

KEY WORDS: • bifidobacteria • intestinal microbiota • inulin • pig • SCFA

Prebiotics are thought to improve the host's health by inducing favorable changes in intestinal microbiota (1,2). Nondigestible oligosaccharides (NDO)6 and inulin, in particular, selectively stimulate beneficial bifidobacteria and lactobacilli in vitro (3,4) and in human subjects and rodents (5,6). Intestinal and fecal short-chain fatty acid (SCFA) concentrations, and especially butyrate, which is the preferred energy source of colonocytes (7), increase when NDO are consumed (1,5). Increased concentrations of SCFA also lower the intestinal pH, which is associated with a suppression of pathogens in pigs (8).

However, it appears that inulin does not have a clear-cut prebiotic effect in pigs in vivo (2). In one study, inulin significantly increased bifidobacteria and lactobacilli + enterococci (9), whereas others found no alterations of intestinal bacteria (10,11). This discrepancy may be explained by the different basal diets fed to the pigs. Pig diets consist mainly of cereal grains and especially wheat grain, and wheat by-products are some of the richest natural sources of short-chain fructans (12). Other major components of pig diets are soybean products that contain galactooligosaccharides, which were shown to exert prebiotic effects in pigs (13). Thus, we hypothesized that a prebiotic effect of inulin could be masked by the naturally occurring fiber and investigated whether the type of basal diet influences the inulin effects on the intestinal microbiota and SCFA.


   MATERIAL AND METHODS
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 ABSTRACT
 MATERIAL AND METHODS
RESULTS
 DISCUSSION
 LITERATURE CITED
 
    Animals and diets. Male castrated piglets (n = 64; German Landrace), weaned at the age of 28 d, were housed in groups with free access to a commercial starter diet [Ferkelstart Plus; wheat, soybean meal, barley, corn flakes, wheat bran, milk powder, soy oil, beet sugar; 13.4 MJ metabolizable energy (ME), 17.5% crude protein, 1.23% lysine, 4.3% crude lipids, 4% fiber; Trede & von Pein] and water. On d 42 of life, pigs were randomly assigned to 1 of 4 feeding groups; 2 groups were fed wheat and barley–based diets without (WB) and with (WBI) the addition of inulin (Table 1). Another 2 groups were fed semipurified diets low in nonstarch polysaccharides (NSP; pentosans, ß-glucans) and with a different formulation, based on ground corn and wheat gluten, again without (CG) or with the addition of inulin (CGI) (Table 1). Inulin was added at a level of 3% at the expense of microcellulose (Table 1). All 4 diets were fed for 3 and 6 wk to explore whether time is a factor in the adaptation process of the intestinal microbiota. Diets were formulated to meet or exceed the NRC recommendations for growth (14). Pigs were housed individually to avoid transfer of intestinal bacteria. Feed was provided at a level of 80 g·(kg0.75·d)–1 and was offered twice daily. Pigs consumed water ad libitum. Feed intake and body mass were recorded weekly and feed allowance was adjusted accordingly. The experimental protocol was approved by the Animal Welfare Committee (Landesveterinaer- und Lebensmitteluntersuchungsamt State Mecklenburg-Vorpommern, Germany; permission no. LVL M-V/310–4/7221.3–2.3–018/02).


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  		TABLE 1 Ingredient and chemical composition of the WB and CG diets without or with inulin fed to growing pigs for 3 and 6 wk

 
    Sampling. After 3 and 6 wk, 8 pigs per group were slaughtered 3 h after the last meal. Digesta from the jejunum, ileum, and colon (according to anatomically determined sections) were collected on ice and processed within 20 min.

    Oligonucleotide probes and bacterial enumeration. Bacteria reported to ferment NDO in vitro (Bifidobacterium spp., Lactobacillus spp., Klebsiella spp., Bacteroides spp. (3,15,16) as well as dominant bacteria in the porcine intestine (17) were enumerated by fluorescent in situ hybridization (FISH) with 5'-Cy3 labeled 16S or 23S rRNA oligonucleotide probes (Supplemental Table 1). Bacterial cells were fixed and hybridization experiments were carried out as described (18). Results were expressed as log10 bacterial counts/g wet intestinal contents. The detection limit of the method was determined to be log10 4.

    Chemical analyses. Diets were analyzed for dry matter (DM), total dietary fiber, and crude fat using a standard procedure (19). Crude protein was calculated using total N values determined by combustion analyzes (LECO, CNS-2000). Inulin concentrations of the WBI and CGI diets, and 8 selected jejunal and colonic samples from WBI and CGI pigs were determined according to AOAC method 997.08 (20). Dietary starch, ß-glucans, and pentosan concentrations were measured as described (21–23). Organic acids were analyzed in 6 jejunal and colonic samples of each feeding group. Concentrations of SCFA were determined by GC with i-capronic acid as internal standard (24); lactic acid was determined colorimetrically (25). The pH was measured in jejunal and colonic samples from 6 pigs of each group using a combination electrode.

    Statistical analysis. We used the Statistical Package for the Social Sciences (SPSS). The experiment was designed as a 2 x 2 x 2 factorial arrangement with 2 basal diets (WB, CG), inulin (with or without), and 2 feeding periods (3, 6 wk). However, in the stepwise development of the model, "feeding period" was not a significant factor (P > 0.370) and no interactions among the factors "basal diet," "inulin," and "feeding period" occurred (P > 0.540). Thus, data were pooled and analyzed by the factors "basal diet" and "inulin" and 1 interaction to increase the sample size in all 4 groups.

Data were tested for Gaussian distribution, and influences of diet on intestinal bacterial communities were checked by ANOVA followed by Dunnett-T3. For data with non-Gaussian distribution, the Kruskal-Wallis-test followed by the Wilcoxon-Test was used. Dietary effects on microbial metabolites and pH were tested by ANOVA followed by Tukey's test. In addition, diet-dependent differences in frequencies of pigs harboring bifidobacteria were tested with a nonparametric Mann-Whitney test. Differences were considered significant at P < 0.05. Values in the text are means ± SD.


   RESULTS
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 ABSTRACT
 MATERIAL AND METHODS
 RESULTS
DISCUSSION
 LITERATURE CITED
 
    Animal performance. Neither diet nor inulin affected food intake (3 wk: 588 ± 13; 6 wk: 692 ± 35 g/d; P = 0.98) or body mass gain (3 wk: 247 ± 53; 6 wk: 332 ± 36, g/d; P = 0.77).

    Bacterial enumeration. The composition of the intestinal microbiota was highly individual. Total bacterial counts increased from jejunal to colonic digesta (log10 8.2 ± 0.5; 10.0 ± 0.2/g wet intestinal contents; P < 0.05) but were not affected by dietary treatment. Bifidobacteria were detected in <40% of all pigs and were also unaffected by dietary treatment (log10 6–7/g wet intestinal contents). However, 40% of the pigs fed the WBI or CGI diets harbored bifidobacteria in the colon, whereas this was the case in only 13% of the pigs fed WB or CG (P < 0.05) (Table 2). Lactobacilli (log10 7–8/g wet intestinal contents) and enterococci (7.5–8.5 log10/g wet intestinal contents) were not affected by the different diets.


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  		TABLE 2 Numbers of enterobacteria, members of the C. histolyticum- and C. lituseburense-group of growing pigs fed WB and CG diets with or without inulin, and the proportion of pigs harboring bifidobacteria1

 
The incidence of enterobacteria in the small intestine was very low (Table 2). In the colon, enterobacterial counts were higher in pigs fed the WB diets. Members of both the C. histolyticum and the C. lituseburense groups were suppressed in the colon when WB diets were fed (Table 2). With WB feeding, the C. histolyticum group was higher in the jejunum (P = 0.05) but reduced in the ileum (P < 0.05). Members of the Eubacterium rectale/Clostridium coccides cluster did not differ between the groups and the mean concentration calculated from all samples was log10 7.6 ± 0.2/g wet intestinal contents. Bacteroides spp. was detected occasionally only in single pigs. Overall, the oligonucleotide probes chosen allowed us to assign ~50% of the total bacteria to distinct bacterial groups.

    Inulin concentrations, microbial metabolites, and pH-values in intestinal samples. In pigs consuming inulin diets (WBI, CGI) 20–50% of the inulin disappeared in the jejunum, irrespective of the basal diet; <0.02% was recovered in colonic samples. In the jejunum, the main fermentation product was lactate (13–16 mmol/kg wet intestinal contents); low concentrations of acetate (<5 mmol/kg wet intestinal contents) but no propionate or butyrate were detected. The jejunal pH ranged from 6.6 to 7.0. Diet did not affect these measurements.

In the colon, acetate was the major bacterial metabolite followed by propionate and butyrate (Table 3), with lactate scarcely detected. Due to the high colonic acetate contribution, total SCFA concentrations were highest in WB, which resulted in the lowest pH (Table 3). Inulin supplementation of both types of diet decreased total SCFA concentrations and increased the pH value, which was due mainly to a reduced concentration of acetate. However, the relative contribution of butyrate was higher (P < 0.05).


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  		TABLE 3 Colonic SCFA concentrations, molar percentages and pH in growing pigs fed WB and CG diets with or without inulin12

 

   DISCUSSION
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 ABSTRACT
 MATERIAL AND METHODS
 RESULTS
 DISCUSSION
LITERATURE CITED
 
Diet and intestinal microbiota are the major components of "gut health" in pigs (26); with the EU ban on feed antibiotics, it is necessary to find alternatives to improve "gut health" of pigs (2). Inulin was added to the diets in a concentration comparable to studies in humans, rodents (5,6), and pigs (9,10,27). In line with previous observations, 20–50% of inulin was degraded in the jejunum (10,27,28). Overall, our data do not suggest a prebiotic effect in terms of stimulation of bifidobacteria and lactobacilli. However, a higher proportion of pigs fed inulin diets harbored bifidobacteria in the colon, suggesting that inulin supplementation stabilized the bifidobacteria population.

The reported prebiotic effects of inulin or other NDO in pigs are not in agreement (9–11,27,28). Our hypothesis was that possible reasons for these discrepancies were related to differences among the naturally occurring fibers in the basal diets. However, our results suggest that the difference in the NDO content and pattern apparently did not disguise a possible effect of inulin on intestinal bacterial communities measured in this study. This is surprising because wheat and barley are some of the richest natural sources of short-chain fructans (12). That the pigs already consumed a starter diet high in fructan before the start of the experimental feeding could have resulted in an adaptation of the intestinal microbiota. Thus, additional inulin appeared not to further increase the bifidobacteria and lactobacilli numbers beyond the detectable level. In this context, we should note that other NDO such as galactooligosaccharides in soy products might behave differently in pigs (13). Generally, due to the low incidence of bifidobacteria in the pigs studied here, an assessment of a bifidogenic effect of inulin was constrained. As noted earlier for humans, the initial number of bifidobacteria seems to influence the extent of stimulation of bifidobacteria in response to the consumption of NDO, independent of the dose of the fructan used (29). Commonly, bifidobacteria are not a dominant group in the porcine intestine (log10 7–log10 9/g wet intestinal contents or fecal sample; 27,30,31). At times, their absence was noted (17,31) as was the case in ~60% of all pigs investigated in this study. It has to be kept in mind that the detection limit of FISH is comparably high, which might partly explain the low number of pigs harboring bifidobacteria.

Although alteration in colonic enterobacteria proved to be significant, differences were small and the biological significance remains uncertain. The higher numbers in WB than in CG diets might be related to a higher digesta viscosity caused by soluble NSP and supportive of motile enterobacteria (32). The nonmotile Klebsiella spp. were also detected by the probe chosen. These can ferment inulin (16) and might benefit from the substrate. Thus, the suppression of possible pathogens (33), another beneficial effect of NDO in pig nutrition, was not observed, which is in line with previous observations (10,27,28).

Little is known about the effects of NDO on Eubacterium spp., Clostridium spp., and Bacteroides spp., which are dominant in the porcine gut (17). The Eubacterium rectale/Clostridium coccoides cluster was not affected by diet. When B. fragilis and B. distasonis specific probes were used, bacteria were detected only occasionally, although B. fragilis was reported to utilize inulin (15). This indicates that these 2 species were not important members of the Bacteroides spp. in our pigs. There were higher numbers of C. histolyticum and related species in the ileum and colon and members of the C. lituseburense group in the colon when the CG diets were fed. Due to the broad range of bacteria within these groups (including potential pathogens), this finding is difficult to interpret although a depressing effect of NDO on C. difficile, a member of the C. lituseburense group, was shown in vitro (34). However, it must be kept in mind that in our study, C. difficile was detected together with at least 15 further bacteria of the C. lituseburense group (35).

Total SCFA and in particular acetate concentrations in the colon were lower in the groups fed inulin diets, whereas the proportion of butyrate was increased, which largely agrees with previous studies (36). The lower acetate concentration could be a consequence of acetate utilization in crossfeeding of other microbes (37). It is also worthwhile to note that the lactate concentration was extremely low in the colon, suggesting bacterial utilization of lactate to generate butyrate (38). However, butyrate producers, such as members of the Eubacterium rectale/Clostridium coccoides cluster (29) were not stimulated. In the literature, there is disagreement concerning the association of dietary NDO with SCFA (9,13,27,30). In any case, SCFA concentrations are always simply a snapshot of the situation because most of the SCFA formed during the fermentation will be immediately utilized by the colonic mucosa (39) or other bacteria.

In summary, the pigs investigated in this study harbored a highly variable microbiota that was relatively inert. Although 20–50% of the dietary inulin was degraded in the jejunum, no general stimulation of bifidobacteria and lactobacilli counts by inulin was found. In intestinal digesta, the proportion of the butyrate contribution was higher when inulin diets were fed, whereas total SCFA concentrations were lower. We conclude that the pattern of naturally occurring dietary fibers did not disguise the effect of inulin in pigs previously adapted to cereal grain–based diets containing already high concentrations of fiber.


   ACKNOWLEDGMENTS
 
We thank Dr. B. Stabenow, Dr. M. Kwella, H. Sievert, R. Gaeth, and H. Pröhl for animal care and excellent technical assistance. Dr. V. Guiard is gratefully acknowledged for statistical consultancy. Inulin was generously provided by ORAFTI Active Food Ingredients, Belgium.


   FOOTNOTES
 
1 Presented in abstract form at the 59th annual meeting of the Society of Nutrition Physiology, March 8–10, 2005, Stuttgart-Hohenheim, [Loh G, Eberhard M, Brunner RM, Hennig U, Kwella M, Metges CC. Inulin supplementation of a semi-synthetic diet does not affect the microbiota in the small and large intestine of growing pigs. Proc Soc Nutr Physiol. 2005;14:76]. Back

2 Funded by a grant (Me 1420/4-1) of the Deutsche Forschungsgemeinschaft, Germany. Back

3 Supplemental Table 1 is available with the online posting of this paper at www.nutrition.org. Back

4 These authors contributed equally to this work. Back

6 Abbreviations: CG, corn-gluten diet; CGI, corn-gluten diet with inulin; DM, dry matter; FISH, fluorescent in situ hybridization; ME, metabolizable energy; NDO, nondigestible oligosaccharide; NSP, nonstarch polysaccharides; SCFA, short-chain fatty acids; WB, wheat-barley diet; WBI, wheat-barley diet with inulin. Back

Manuscript received 13 October 2005. Initial review completed 9 November 2005. Revision accepted 31 January 2006.


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