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Poult Sci 2008. 87:783-789. doi:10.3382/ps.2007-00271
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PHYSIOLOGY, ENDOCRINOLOGY, AND REPRODUCTION: Research Notes

Effects of Dietary Inulin on the Intestinal Short Chain Fatty Acids and Microbial Ecology in Broiler Chickens as Revealed by Denaturing Gradient Gel Electrophoresis

H. Rehman*,1, P. Hellweg{dagger}, D. Taras{dagger} and J. Zentek2

* Institute of Nutrition, University of Veterinary Medicine, Veterinärplatz 1, A 1210 Vienna, Austria; and {dagger} Institute of Nutrition, Faculty of Veterinary Medicine, Free University Berlin, Brümmerstr. 34, D-14195 Berlin, Germany

2 Corresponding author: zentek.juergen{at}vetmed.fu-berlin.de


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Inulin can stimulate the growth of the intestinal bacteria as well as alter the ratio among various short chain fatty acids (SCFA) produced. In the present study, we analyzed the effect of dietary inulin on the intestinal bacterial community as determined by denaturing gradient gel electrophoresis analysis of universal 16S rDNA after amplication with PCR and SCFA profile. Broilers were fed a diet primarily composed of corn-soybean meal or same diet with 1% inulin for 42 d. The relative weight of digesta-filled ceca of the inulin-fed group was higher (P < 0.01) than in the control group. Amongst SCFA, only acetate could be detected in the jejunal digesta, which tended to be higher (P = 0.09) in inulin-fed group compared with the control group. Inulin did not affect the total concentration of SCFA in the cecal digesta. The relative proportion of n-butyrate was elevated (P = 0.05) with a concomitant decrease in the concentration of n-valerate (P < 0.05) in the inulin-fed group compared with the control group. Dietary inulin did not affect the number of PCR-denaturing gradient gel electrophoresis bands nor their diversity in the jejunal and cecal digesta. Intragroup similarities were not different between the groups, nor were any differences between intra-and intergroup similarities in the jejunal and cecal samples. In conclusion, inulin altered the cecal microbial metabolic activity without any major impact on the composition of intestinal bacterial communities as measured by the present techniques.

Key Words: inulin • microbiota • short chain fatty acid • denaturing gradient gel electrophoresis • broiler


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The intestinal microbiota plays a vital role in the normal nutritional, physiological, immunological, and protective functions of the host animals (Vispo and Karasov, 1997). The composition and metabolic activity of the intestinal microbiota can be influenced by the diet (Rehman et al., 2007c). There is a growing interest in the use of a variety of oligosaccharides as prebiotics to promote animal health by altering the intestinal microbial community. Prebiotic is a selectively fermented ingredient that allows specific changes in the composition or activity of the gastrointestinal microbiota and is not digested by the host digestive enzymes (Gibson et al., 2004). Oligosaccharides have been shown to influence the short chain fatty acids (Zhan et al., 2003; Rehman et al., 2007a) and the intestinal bacterial community (Kleessen et al., 2003; Xu et al., 2003; Yusrizal and Chen, 2003; Cao et al., 2005) in broilers. However, others reported that inulin supplementation did not affect the intestinal bacteria (Biggs and Parsons, 2005).

Inulin, extracted from chicory (Cichorium intybus), contains molecules with a degree of polymerization (DP) of 3 to 60, mean being 10 (Crittenden, 1999). Therefore, inulin contains oligosaccharide components and polysaccharides. Because of the β(2->1) glycosidic bond, it is resistant to host-derived digestive enzymes and is believed to enhance the growth of health-promoting bacteria and to suppress the growth of potential pathogenic bacteria (Zentek et al., 2003). In a previous study (Rehman et al., 2007a), we found a significant increase in the jejunal lactate and M proportion of cecal butyrate in inulin-supplemented broilers, suggesting that inulin might have affected the intestinal microbiota.

We used a nucleic acid-based screening method, PCR, in combination with denaturing gradient gel electrophoresis (DGGE), to monitor the impact of dietary inulin supplementation on the composition of the intestinal bacteria as well as on the short chain fatty acids (SCFA) as main bacterial metabolic products in the jejunal and cecal contents.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Experimental Birds and Management
Day-old broilers of a commercial strain (Cobb 500, n = 90), procured from a commercial hatchery (Cobb Germany Avimex GmbH, Regenstauf, Germany), were randomly divided into 2 groups (control and inulin-fed), each composed of 45 birds. Birds in each group were placed in 3 pens, each pen containing 15 birds. The ambient temperature started at 33°C (from d 0 to 3) and was gradually reduced according to normal management practice (2 to 3°C/wk). During the first 3 d, chicks were provided with 24 h of light, after which lighting was decreased to 18 h until the end of the trial. The birds were weighed individually at the end of the experiment.

Diets
Chicks in the control group were fed an antibiotic-and coccidiostat-free diet, which was mainly composed of corn (Table 1Go), whereas birds in the treatment group were fed same basal diet supplemented with 1% inulin (Beneo GR, Orafti Active Food Ingredients, Tienen, Belgium) at the expense of corn. The inulin product contained pure inulin (90 to 94%, DP 2 to 60, average being 10 to 12), glucose and fructose (0 to 4%), and sucrose (4 to 8%) according to the manufacturer data sheet provided. Birds had free access to feed and water throughout the experiment.


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  		Table 1. Composition and analysis of experimental diet (DM basis)
 
Slaughtering and Sampling
On d 42, twenty birds from each group were randomly selected and killed by cervical dislocation. The jejunum was ligated 5 cm before and after the Meckel’s diverticulum and was cut with a sterile scalpel. Later, digesta was transferred into sterile polypropylene tubes with gentle squeezing. Afterwards, samples were immediately stored at –70°C until used for further analysis. Ceca from individual birds were removed and weighed. Later, cecal contents were collected into the sterile containers and stored at –70°C as described above.

SCFA Analysis
The SCFA were analyzed as described by Schäfer (1995) with minor modifications. Briefly, after thawing the intestinal contents on ice, 300 mg of digesta (n = 10) was collected and diluted in distilled water, homogenized, and centrifuged (Eppendorf, model 5415C, Hamburg, Germany) at 13,000 rpm for 15 min. Hexanoic acid (Sigma-Aldrich, Deisenhofen, Germany) was used as an internal standard (0.5 mmol/L). The sample (1.0 µL) was injected in a gas chromatograph (Agilent Technologies, model 6890N, Santa Clara, CA) fitted with HP-Innowax column model 19095N-123 (Agilent Technologies; length 30 m, internal diameter 530 µm with film thickness of 1.0 µm). The initial temperatures of the oven, injector, and flame-ionization-detector were 70, 230, and 250°C, respectively. Hydrogen gas produced by a gas generator (Parker ChromGas, model 9090, Parker Hannifin Corporation, Cleveland, MN) was the carrier gas with a flow rate of 30 mL/min.

Analysis of Intestinal Contents by PCR-DGGE
Genomic DNA Extraction.
Extraction and purification of total cellular DNA from the jejunal (n = 10) and cecal (n = 10) digesta for PCR-DGGE was carried out as described by Zoetendal et al. (2001) with modifications (Kraatz et al., 2006). Briefly, an aliquot of 1 g of sample was added to 3 g of glass beads (diameter 0.25 to 0.50 mm) and 10 mL of guanidinium isothiocyanate (GITC) solution (75 g of GITC/100 mL of citrate sarcosine buffer) in a cryotube, incubated at 60°C for 5 min, and vortexed for 2 min. The sediments were again diluted with the GITC solution (7.0 mL), incubated again at 60°C for 5 min, followed by renewed bead beating for another 2 min. The nucleic acids were extracted with phenol-chloroform, chloroform-isoamylalcohol, and 80% isopropanol. The nucleic acids were precipitated with 70% ethanol and purified on a Macherey-Nagel column (Nucleo-Spin-Tissue kit, Macherey-Nagel, Düren, Germany).

PCR Amplification.
Amplification of the variable V6-V8 region of bacterial 16S rDNA was performed using primer pairs F-0968-GC and RW-1401 (Kraatz et al., 2006). A 40-nucleotide G+C clamp was attached to the F primer at the 5' end. The PCR was performed using a Multiplex PCR kit (Qiagen, Hilden, Germany). The PCR amplification of the V6-V8 was carried out by the hot-start and touch-down program with a T1 Thermocycler (Biometra, Göttingen, Germany). The PCR program consisted of 35 cycles: initial activation step at 95°C for 15 min; a single cycle of 94°C denaturation for 60 s, 66°C annealing for 90 s and 72°C extension for 90 s; 20 thermal cycles in which the annealing temperature was decreased 0.3°C every other cycle; 14 cycles of 94°C for 30 s, 59°C for 90 s, and 72°C for 90 s; and final elongation at 72°C for 10 min.

Gel Electrophoresis.
The INGENYphorU vertical DGGE system (Ingeny International, Goes, the Netherlands) was used for subsequent nucleotide sequence-specific separation of PCR amplicons. To separate PCR fragments, 35 to 50% linear chemical DNA-denaturing gradient of urea and formamide [100% denaturing solution contains 40% (vol/vol) formamide and 7.0 M urea], was formed with a Gradient Former (BioRad model 485, Hercules, CA) in polyacrylamide gels consisting of 8% polyacrylamide (acrylamide-bisacrylamide ratio 37:5:1) and 0.5 Tris-acetate EDTA acid buffer (pH 8.3). The PCR amplicons were mixed with loading buffer and were placed in each sample well. Electrophoresis running time was at 60°C for 5 min at 200 V followed by 16 h at 120 V. After electrophoresis, gels were silver-stained and developed (Cairns and Murray, 1994).

Analysis of the DGGE Gels.
Scanned DGGE banding patterns were analyzed with computer software, Phoretix 1D (version 5.1, Phoretix International Limited, Newcastle upon Tyne, UK). Bands with an area of < 1% of all bands were omitted from further analysis (Collier et al., 2003; Konstantinov et al., 2004; Awati et al., 2005). The microbial diversity, Shannon index based on number (richness) and relative abundance (evenness) of PCR-DGGE bands, was calculated (Konstantinov et al., 2004). Sörensen pairwise similarity index, based on the total number and the number of common PCR-DGGE bands was calculated (Kraatz et al., 2006) and values were used to generate a dendrogram based on the unweighted pair-group method with arithmetic average as algorithm. Morisita and Renkonen indices were used for further semi-quantitative assessment of intestinal microbial community similarities (Kwak and Peterson, 2007). The advantage of these indices is that they take species abundance into account. Thus, a similarity value of <100% is obtained for 2 communities that contain the same species in different abundances.

All chemicals and reagents used were of analytical grade and were purchased from Sigma-Aldrich, Deisenhofen, Germany. The present experiment was conducted in accordance with the Ethical Committee of Animal Care, Institute of Animal Nutrition, Free University, Berlin, Germany.

Statistical Analyses
Kolmogorov Smirnov’s test was used to test the normal distribution of the data. The weight of birds, weight of digesta-filled ceca (relative to BW), SCFA, richness, evenness, and Shannon index were statistically analyzed with independent Student’s t-test. The similarity indices (Sörensen, Morisita, and Renkonen) were assorted according to treatment in 3 groups. Two groups, intragroups, were control and inulin-fed, respectively, whereas a third group, intergroup, was designated as control x inulin-fed. The similarity indices were compared by 1-way ANOVA. The group differences were determined by the Duncan’s multiple range test, and differences were considered significant at P < 0.05. Statistical tests were carried out as described by Kaps and Lamberson (2004) using SPSS (version 12.0, SPSS Inc., Chicago, IL).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
The mean body weight of birds in both groups (control and treatment) was comparable on d 0 (43.2 ± 0.4 g vs. 43.3 ± 0.6 g, P = 0.96) and d 42 (2,868.0 ± 54.2 g vs. 2,752.0 ± 38.9 g; P = 0.16). The relative weight of digesta-filled ceca was higher (P < 0.01) in the inulin-supplemented group (5.65 ± 0.27 g/kg of BW) compared with the control group (4.57 ± 0.17 g/kg of BW). Among principal SCFA, only acetate could be detected in the jejunal digesta and tended (P = 0.09) to be higher in the inulin-fed group (3.7 ± 0.6 µmol/g of digesta) compared with the control group (2.6 ± 0.3 µmol/g of contents). The dietary inulin did not affect the total SCFA concentration in the cecal digesta; however, cecal butyrate presented a larger proportion of total SCFA (P = 0.05) in the inulin-supplemented group. Moreover, concentration of n-valerate was lower (P < 0.05) in the inulin-fed group compared with the control group (Table 2Go).


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  		Table 2. Influence of supplementation of inulin on the short-chain fatty acid (µg) profile in the cecal digesta of broilers (n = 10)
 
Inulin supplementation caused no statistically significant differences in the number of PCR-DGGE bands or relative abundance of bands within the jejunal digesta (Table 3Go). Intra- and intergroup comparisons using Sörensen, Renkonen, and Morisita indices of similarity also showed no change with inulin supplementation (Table 4Go). The lack of difference is also apparent in the dendrogram calculated using unweighted pair-group method with arithmetic average clustering algorithm (Figure 1AGo). Similar outcomes were also observed in the cecal microbiota (Tables 3Go and 4Go, Figure 1BGo).


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  		Table 3. Influence of supplementation of dietary inulin on richness, Shannon index, and evenness of microbial community in the jejunal and cecal digesta of broilers (n = 10)1
 

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  		Table 4. Influence of supplementation of dietary inulin on the Renkonen, Sörensen, and Morisita indices in the jejunal and the cecal digesta of broilers (n = 10)
 

Figure 1
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  		Figure 1. Dendrogram illustrating the similarity of polymerase chain reaction-denaturing gradient gel electrophoresis banding patterns in the jejunal (A) and the cecal digesta (B) of broilers. The dendrogram was constructed using the Sörensen index and unweighted pair-group method with arithmetic average clustering algorithm. Dendrogram distances are measured in arbitrary units (C and I stand for control and inulin-fed groups, respectively).

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The composition of the intestinal microbiota and its metabolic activities has an important impact on the digestive process, the feed utilization, and the general development of the host. The composition of the intestinal bacterial community can be changed by a variety of factors, diet being one of them as it acts as a substrate for the indigenous intestinal microbiota (Crittenden, 1999; Rehman et al., 2007c). The present study describes the influence of dietary inulin on the metabolic profile in terms of SCFA and microbial ecology of the intestinal tract as revealed by the PCR-DGGE in broilers. Inulin did not affect the final body weight compared with control birds, which is in accordance with our previous findings (Rehman et al., 2007a,b). On the other hand, the relative weight of digesta-filled ceca of inulin-supplemented group was higher compared with control birds. A previous study already demonstrated that relative weights of cecal digesta and the cecal wall were higher in the inulin-supplemented groups (Rehman et al., 2007a). An increase in the cecal weight has also been demonstrated in broilers fed diets supplemented with sucrose thermal oligosaccharide caramel (Orban et al., 1997) or fructooligosaccharides (Ying and Shan, 2004) or fructooligosaccharides plus direct-fed microbes (Oyarzabal and Conner, 1996).

In the lower intestinal tract, fermentable complex carbohydrates may decrease the concentration of putrefactive compounds by providing the gut microbiota with an additional energy supply. These bacteria act as nitrogen sinks, utilizing the undigested protein and its metabolites in the presence of energy for their protein synthesis (Cummings et al., 1979). Complex fermentable carbohydrates serve as an energy source required to produce microbial protein. The use of inulin as a prebiotic is intended to stimulate selectively certain bacterial groups that might lead to a shift in the bacterial metabolism. We detected only a low concentration of acetate in the jejunal digesta that might reasonably be explained by the lower bacterial metabolic activity and short transit digesta time in this segment compared with the ceca. The higher proportion of n-butyrate in the cecal digesta is also consistent with our previous findings (Rehman et al., 2007a). Butyrate provides energy for epithelial growth (Topping and Clifton, 2001) and is involved directly or indirectly in various mechanisms regulating cellular differentiation, growth, permeability, and gene expression (Mroz et al., 2006). The butyrogenic effect of inulin and other oligosaccharides has repeatedly been reported in in vitro studies (Marounek et al., 1999) and in broilers (Zhan et al., 2003; Rehman et al., 2007a). In contrast, Juskiewicz et al. (2004) could not find changes in the cecal SCFA concentration in turkeys fed an inulin-supplemented diet. However, low levels of inulin (0.1 or 0.4%) decreased total cecal SCFA without affecting butyrate or valerate.

The assessment of the intestinal microbial population of animals has been hampered by the inability to cultivate the entire intestinal microbiota. Hence the knowledge of intestinal microbiota based on traditional culture techniques seems to be incomplete (Gong et al., 2002). Here, we describe the application of PCR-DGGE technique to monitor the changes in the intestinal microbiota of broilers fed an inulin-supplemented diet. This is a genetic fingerprinting technique that examines the microbial diversity based upon electrophoresis of PCR-amplified 16S rDNA fragments with gels containing a linear gradient of DNA denaturants (Muyzer et al., 1993). The PCR product banding pattern is indicative of the number of bacterial species or assemblages of groupings consisting of species that are present and thus allow visualization of the genetic diversity of microbial populations. These amplified fragments may be referred to as PCR products, fragments, bands, or amplicons. This technique provides a convenient method to evaluate microbial ecosystems and not only allows analysis of a large number of samples but also is useful for detecting shifts in predominant microbial populations. This molecular fingerprinting technique has been used successfully to describe the intestinal microbial community of broilers (van der Wielen et al., 2002; Knarreborg et al., 2002; Collier et al., 2003; Hume et al., 2006). However, no reports in broilers and only a few reports in dogs (Vanhoutte et al., 2005), pigs (Konstantinov et al., 2004), and rats (Schultz et al., 2004) are available using this technique to demonstrate the inulin-induced changes in the major intestinal microbial community. Results of current study showed that intestinal bacterial community remained unaffected by dietary inulin. The data regarding the influence of dietary inulin on the cecal microbiota of broilers are scanty and contradictory. By using traditional culture methods, it has been reported that supplementation of inulin (1%) did not affect the total aerobes and lactobacilli counts except lower population of Escherichia coli/coliforms in female broilers but not in male broilers in the small intestine and cecal digesta (Yusrizal and Chen, 2003). Rada et al. (2001) found that bifidobacteria were increased in numbers in inulin-fed hens. Biggs and Parsons (2005) could not observe any effect of inulin on the cecal microbiota in broilers. The apparent lack of response of the intestinal bacteria following inulin supplementation may be related to feed ingredients used in the study. It has been found that response of the intestinal bacteria is different in terms of their population and concentration of SCFA in broilers fed corn- or wheat-barley-based diets (Mathlouthi et al., 2002) or corn- or wheat/rye-based diets (Hübener et al., 2002). Dietary carbohydrates might act similar to a prebiotic as corn contains fermentable carbohydrates, simple sugars, pentosans, and other fiber components (Kereliuk et al., 1995; Malathi and Devegowda, 2001). However, the soybean meal contains much higher contents of nonstarch polysaccharide (NSP) compared with corn (Bach Knudsen, 1997). Little is known about the intestinal effects of the NSP, but some studies show that the ileal digestibility of starch from corn is usually high (Almirall et al., 1995). It has been found that starch in a corn-based diet fed to broilers was almost completely digested before reaching the ileum (Weurding et al., 2001). Another possibility for "prebiotic" effects of the basal diet is soybean meal, containing approximately 29 to 33% NSP, which are not digested completely in the small intestine and can be fermented by the intestinal microbiota (Smits and Annison, 1996; Malathi and Devegowda, 2001; Lan et al., 2007). It has been shown that supplementation of soybean meal oligosaccharides to broiler chickens increased the cecal population of a group of lactic acid bacteria (genera Lactobacillus, Pediococcus, Weissella, and Leuconosto; Lan et al., 2007).

In conclusion, dietary inulin affected the intestinal microbial activity without any obvious influence on the major intestinal bacterial populations.


   ACKNOWLEDGMENTS
 
The authors gratefully acknowledge K. Schäfer and K. Männer, Institute of Nutrition, Faculty of Veterinary Medicine, Free University Berlin, Germany, for their excellent technical assistance.


   FOOTNOTES
 
1 Present address: Department of Physiology and Biochemistry, Faculty of Bio-Sciences, University of Veterinary and Animal Sciences, Lahore, Pakistan. Back

Received for publication June 29, 2007. Accepted for publication December 22, 2007.


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 ABSTRACT
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 MATERIALS AND METHODS
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 DISCUSSION
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