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© 2007 American Society for Nutrition J. Nutr. 137:2399-2404, November 2007

Nutrient Physiology, Metabolism, and Nutrient-Nutrient Interactions

Cecum Is the Major Degradation Site of Ingested Inulin in Young Pigs1,2

Koji Yasuda3, Roberto Maiorano3, Ross M. Welch4, Dennis D. Miller5 and Xin Gen Lei3,*

Departments of 3 Animal Science and 5 Food Science and 4 USDA-Agricultural Research Service, U.S. Plant, Soil and Nutrition Laboratory, Cornell University, Ithaca, NY 14853

* To whom correspondence should be addressed. E-mail: XL20{at}cornell.edu.


   ABSTRACT
TOP
 ABSTRACT
Introduction
 Materials and Methods
 Results
 Discussion
 LITERATURE CITED
 
Two groups have reported >90% of inulin digestion occurs before the cecum in pigs and argued against pigs as a proper animal model for humans in this regard. Two experiments were conducted with weanling pigs to characterize the hydrolysis profile of inulin in their digestive tracts. In Expt. 1, 12 pigs (weighing 7.7 ± 0.2 kg) were fed a low-iron (54 mg/kg) corn-soy basal diet (BD) or BD + 4% inulin (Synergy 1, Orafti) for 6 wk. All pigs were killed at the end of the trial and digesta samples were collected from the stomach, upper and lower jejunum, cecum, and proximal, mid-, and distal colon. Inulin was detected in digesta from the first 3 segments (0.4–5.5% dry matter) but not from the large intestine of pigs fed inulin. Fructose concentrations in digesta from the stomach and jejunum were greater (P < 0.05) in pigs fed inulin than in those fed BD. To further determine whether inulin was degraded in the ileum or cecum, we conducted Expt. 2 with 12 pigs (weighing 11.2 ± 1.1 kg) for 8 wk as in Expt.1 except that digesta samples were collected from the ileum instead of upper jejunum. Likewise, inulin was detected only in digesta from stomach, jejunum, and ileum of pigs fed inulin. Although inulin-degrading activity was detectable in digesta from the ileum, cecum, and proximal colon of both groups, the highest activity (P < 0.05) was found in the cecum digesta of pigs fed inulin. Digesta from the cecum and colon, but not from the ileum, was able to degrade added inulin in in vitro incubations. We conclude that supplemental dietary inulin in young pigs was mainly degraded in their cecum.


   Introduction
TOP
 ABSTRACT
 Introduction
Materials and Methods
 Results
 Discussion
 LITERATURE CITED
 
Inulin is a unique polydisperse D-fructofuranose polymer linked by ß(2–1) bonds at the anomeric C2 and is found in tissues of many plant species (1). Supplemental dietary inulin has been shown to improve bioavailability of calcium and magnesium to animals and humans (2–6). Using young anemic pigs as a model for humans, we demonstrated a positive effect of supplemental inulin on dietary iron bioavailability (7). But little is known about the mechanisms for these benefits of supplemental inulin to mineral bioavailability (2,7). The popular notion is that actions of inulin are mediated by its fermentation in the large intestine (8). However, data on the sites of inulin degradation in the gastrointestinal (GI)6 tracts of humans and pigs are conflicting (9–15).

Comparisons of inulin concentrations between feces and effluents of ileostomy patients indicate virtually no degradation (9–13) or absorption (16,17) of inulin superior to large intestines of humans. In contrast, Branner et al. (14) and Houdijk et al. (15) reported that >90% of inulin digestion occurs before the cecum in pigs, and questioned pigs as a proper animal model for humans in this regard. However, these pig studies had technical limitations for precisely identifying the location of inulin degradation. In both studies, digesta samples for inulin analysis were taken from only a single site in the GI tract without determination of the sequential flow or change of digesta inulin in other segments. In the study by Branner et al. (14), inulin disappearance was based on digesta samples collected from the anus of ileostomy patient-mimicked pigs that underwent a surgical procedure to connect the terminal ileum to the proximal section of 20–25 cm of intact rectum. Evidently, the hydrolysis of inulin in the rectum was neglected. In the study by Houdijk et al. (15), a T-cannula was placed in the cecum of pigs and, therefore, collections of true digesta from the ileum was impossible. In addition, they derived inulin content by simply subtracting the proximate nutrient components (ash, crude protein, ether extract, and crude fiber) from the dry matter (15). That particular method does not yield as consistent or accurate results as the HPLC method (18) or provide profiles of carbohydrate that are different in their nature (i.e. chain length). Understanding the profiles of oligosaccharides such as raffinose and stachyose is important, because supplementation of these substances from soybean meal have been shown to affect nutrient digestibility in the ileum (19).

Therefore, our objectives were to determine the following: 1) inulin concentrations and carbohydrate profiles in digesta collected from 7 consecutive GI segments between the stomach and the distal colon in pigs fed diets containing 0 or 4% supplemental inulin; and 2) whether feeding inulin induced the inulin-degrading activity in digesta collected from 6 segments from the stomach to mid-colon.


   Materials and Methods
TOP
 ABSTRACT
 Introduction
 Materials and Methods
Results
 Discussion
 LITERATURE CITED
 
    Animals, diets, and feeding experiments. Two experiments were conducted with a total of 24 weanling Yorkshire x Hampshire x Landrace crossbred pigs (barrows and gilts) from the Cornell University Swine Farm. Our animal protocols were approved by the University Institutional Animal Care and Use Committee. In Expt. 1, 12 weanling pigs weighing 7.7 ± 0.2 kg were divided into 2 groups (n = 6) and were fed a corn-soybean meal basal diet (BD) (7) or the BD + 4% inulin (Synergy 1, Orafti) for 6 wk. The BD contained 14.1 MJ/kg, 18.5% crude protein, and 4.3% crude fiber, with no supplemental inorganic iron (7). The supplemental inulin source, Synergy 1, was added to the experimental diet to replace 4% corn starch in the BD and this product was a mixture of {alpha}-D-glucopyranosyl-(ß-D-fructofuranosyl)n-1-ß-D-fructofuranosides (n = 10–60, mean of 25), and oligofructose, {alpha}-D-fructopyranosyl-(ß-D-fructofuranosyl)n-1-ß-D-fructofuranosides (n = 2–7, mean of 4). In Expt. 2, 12 weanling pigs weighing 11.2 ± 1.1 kg were fed the same dietary treatments as in Expt.1 except the BD was added with 60 mg of iron and the feeding trial lasted for 8 wk. The BD and the inulin-supplemented diets contained 0.6 and 3.2% inulin by analysis, respectively. Pigs were housed in an environmentally controlled barn (22–25°C; a light:dark cycle of 12:12 h), given free access to feed and water, and checked daily. We measured body weight gain and feed consumption weekly, which did not differ between dietary treatments in either experiment.

    Digesta sample collection. At the end of both experiments, pigs were food deprived for 8 h and then consumed feed ad libitum for 10 h before they were killed to collect digesta samples (7). In Expt. 1, digesta samples were collected from the entire contents of stomach after thorough mixing with a blender and from 6 intestinal segments with 12-cm length each. The excisions were as follows: upper jejunum, 2 m distal to the pylorus; lower jejunum, 2 m proximal to the ileocaecal junction; cecum, ~20 g of digesta contents were squeezed out from a small incision that was made at the apex; proximal colon, immediately after the ileocaecal junction; mid-colon, equal length up and down the mid-transverse colon; and distal colon, immediately prior to the rectum. In Expt. 2, digesta samples were collected from all segments as designated in Expt.1 except the upper jejunum. In addition, digesta samples were also collected from the ileum at 12 cm proximal to the ileal-caecal junction. The collected digesta samples were frozen in liquid nitrogen immediately and stored in a –80°C freezer. Before analysis, digesta samples were freeze-dried (20 SRC-X, Virtis) for 48 h and were ground with a coffee grinder at 4°C.

    HPLC analyses of digesta carbohydrates. The concentrations of inulin, glucose, fructose, lactose, sucrose, raffinose, stachyose, and verbascose in digesta and diet samples were measured using the method described by Quemer et al. (20). Digesta samples were mixed with distilled water and sterilized in an autoclave (121°C, 20 min) before proceeding to the standard method. Preliminary experiments were conducted to confirm no significant effect of autoclaving on concentrations of inulin and other sugars in digesta samples. Before and after enzymatic hydrolysis, the sample supernatant fraction was subjected to high performance anion-exchange chromatography (Dionex). The system consisted of a gradient pump and programmable pulsed electrochemical detector (ED50 electrochemical detector, Dionex). Separations were performed using a Carbopac PA100 column (4 x 250 mm) that was preceded by a Dionex GM-4 gradient mixer. The isocratic point of the chromatographic mobile phase was consisted with a gradient of 150 mmol/L NaOH for 0–5 min and 300 mmol/L NaOH for 5–12 min.

    In vitro incubation of added inulin in digesta samples. To determine the potential inulin-degrading capacity in digesta from the ileum, cecum, and proximal colon, we weighed 0.2 g of freeze-dried digesta samples from each of the segments in Expt. 2 and suspended the samples in disposable glass tubes (16 x 100 mm, Fisher Scientific) containing 1.8 mL of ice-cold water. A duplicate set of samples was prepared and autoclaved (121°C for 20 min) to serve as baseline controls. Exogenous inulin (Synergy 1) (0.2 mL, containing 8 mg inulin) was added to the tubes to make a final inulin concentration of 4% (wt:wt on dry matter basis). Samples were then incubated under aerobic conditions in a water bath at 37°C for 0, 1, and 4 h with agitation every 30 min. At each time point, samples were taken and placed in a –80°C freezer. All samples were freeze-dried and stored in a –20°C freezer until analysis. The inulin concentrations of these samples were measured using the same method described above for the digesta.

    Inulin degrading activity assay. Freeze-dried digesta samples (1 g) of the stomach, lower jejunum, ileum, cecum, and proximal and mid-colon were suspended in 10 mL of 55 mmol/L 2 N-morpholino-ethanesulphonic acid buffer (pH 5.5), sonicated at 40 watts for 3 intervals of 10 s (VC130 ultrasonic processor, Sonics & Materials), and extracted by constant stirring (magnetic stir bar) at 4°C for 30 min. The mixture was centrifuged at 15,000 x g; 20 min at 4°C (GA-20 rotor, GS-6KR Centrifuge, Beckman Instruments). After the supernatant fraction was transferred to a conical tube, a spin column method (molecular weight cutoff 30,000 kDa; Millipore) was used to remove free sugars following the manufacturer's instructions (the typical size of inulinase produced by microorganisms is larger than 53,000 kDa) (21). Inulin-degrading activity was determined by measuring the concentration of free fructose in the final volume of ~200-µL samples following incubation. We measured fructose concentrations using an enzyme-coupled assay described by Beutler et al. (22). The amount of NADPH formed was measured at 340 nm using a Microplate Scanning Spectrophotometer (KC-4 version 2.6, BIO-TEK Instruments).

    Statistical analyses. Data were analyzed as a randomized block design using the Proc General Linear Models procedure of SAS (version 6.12, SAS Institute). The main effects of supplemental dietary inulin and in vitro incubation time or autoclaving on various measures were analyzed using Student's t test and the significance level was set at P ≤ 0.05 (23). Due to the relatively large variation, data on sucrose, stachyose, and raffinose were log transformed prior to the t test. Values are expressed as means ± SEM.


   Results
TOP
 ABSTRACT
 Introduction
 Materials and Methods
 Results
Discussion
 LITERATURE CITED
 
    Expt. 1. Compared with pigs fed the BD, pigs fed 4% inulin had 84, 99, and 97% higher (P < 0.05) digesta inulin concentrations in the stomach, upper jejunum, and lower jejunum, respectively (Fig. 1A). Inulin was, however, undetectable in digesta samples from cecum or proximal, mid-, and distal colon in either group. Compared with pigs fed the BD, pigs fed 4% inulin had 60, 61, and 97% higher (P < 0.05) fructose concentrations in the stomach, upper jejunum, and lower jejunum (Table 1) and had 74% higher (P < 0.05) concentration of raffinose and 99% higher (P < 0.05) concentration of stachyose in the lower jejunum.


Figure 1
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  		FIGURE 1  Effect of supplemental dietary inulin on inulin concentrations of digesta (on dry matter basis) from various segments of GI tracts of pigs in Expt. 1 (A) and Expt. 2 (B). Values are means ± SEM, n = 6. *Different from BD, P < 0.05.

 

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  		TABLE 1 Effects of supplemental dietary inulin on digesta sugar concentrations in pigs in Expt. 11

 
Low concentrations of fructose (0.2 ± 0.08 µmol/g) and sucrose (0.3 ± 0.03 µmol/g) were detected in cecum digesta of both groups, but glucose, fructose, sucrose, raffinose, stachyose, and verbascose were not detectable in the 3 parts of colon of either group.

    Expt. 2. The mean daily intakes of pigs fed the BD and the BD + 4% inulin were 8.2 and 42.9 g, respectively. Compared with pigs fed the BD, pigs fed 4% inulin had higher (P < 0.05) digesta inulin concentrations in stomach, lower jejunum, and ileum (Fig. 1B). Inulin was not detected in digesta samples from the cecum or any part of the colon of either group. Compared with pigs fed the BD, pigs fed 4% inulin had 80–88% higher (P < 0.05) fructose concentrations in digesta of stomach, lower jejunum, and cecum, and 89% higher (P < 0.05) sucrose concentrations in digest of ileum (Fig. 2). In contrast, these pigs had 61 and 88% lower glucose concentrations in digesta of stomach and cecum than those of pigs fed the BD, respectively. Although low concentrations of sucrose and raffinose were detected in the digesta of cecum, virtually no sugars were detected in digesta collected from any part of colon of pigs in either group. Inulin-degrading activities (mmol/h fructose liberated) in digesta (1 g dry matter) of pigs fed BD and BD + 4% inulin were as follows: ileum, 8.1 vs. 4.8 (SEM = 2.4); cecum, 13.2 vs. 64.8 (SEM = 12.1), P < 0.05; and proximal colon, 5.7 vs. 14.5 (SEM = 4.0). No activity was detected in digesta from the stomach, lower jejunum, and mid-colon.


Figure 2
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  		FIGURE 2  Effect of supplemental dietary inulin on concentrations of glucose (A), fructose (B), and sucrose (C) in digesta (on dry matter basis) collected from various segments of GI tracts of pigs in Expt. 2. Values are means ± SEM, n = 3–6. *Different from BD, P < 0.05.

 
Adding 4% inulin in the digesta of ileum resulted in much higher (P < 0.05) inulin concentrations in pigs fed BD + 4% inulin than those fed BD at all time points (Fig. 3A,B). However, the in vitro incubation up to 4 h, regardless of prior sample autoclaving, caused no decrease in inulin concentrations in either group. The addition of 4% inulin in digesta of the cecum and proximal colon resulted in similar inulin concentrations in the 2 dietary groups (Fig. 3C–F). The in vitro incubation caused substantial (P < 0.05) disappearance of inulin in both groups at 4 h. Comparatively, the disappearance was faster and/or greater in digesta from pigs fed 4% inulin than that from pigs fed the BD. Inulin concentrations of the cecum or colon digesta samples that underwent prior autoclaving were unchanged by the in vitro incubation.


Figure 3
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  		FIGURE 3  Time course of inulin disappearance in digesta collected from the ileum (A and B), cecum (C and D) and proximal colon (E and F) of pigs fed the BD (A, C, and E) or BD + 4% inulin (B, D, and F) in Expt. 2. Before the in vitro incubation, all digesta samples were added with 4% inulin (on dry matter basis). The control samples shown by the broken line were autoclaved before the incubation. Values are means ± SEM, n = 3. *Different from 0 h of the treatment and the autoclaved samples at the same time point, P < 0.05.

 

   Discussion
TOP
 ABSTRACT
 Introduction
 Materials and Methods
 Results
 Discussion
LITERATURE CITED
 
Three lines of evidence suggest that the cecum was the major degradation site of ingested inulin in the GI tracts of young pigs. Whereas higher inulin concentrations were found in digesta of the stomach, jejunum, and ileum from pigs fed 4% inulin than pigs fed the BD, no inulin was detectable in digesta of cecum or colon in either group. In the 6 measured segments, digesta from the cecum displayed the highest inulin-degrading enzyme activity. Moreover, the activity was induced by inulin feeding in pigs. Furthermore, cecum digesta, but not ileum digesta, was able to degrade the added inulin in in vitro incubations. To our knowledge, this is the first systematic characterization of the hydrolysis profile of ingested inulin in the entire GI tract of pigs or other experimental simple-stomached animals. The lack of substantial inulin degradation in the upper GI tract (small intestine) of pigs is in agreement with results from human studies. Kundsen et al. (9) demonstrated an 87% recovery of the ingested short-chain inulin [68%, degree of polymerization (DP) < 10] in the effluent of ileostomy subjects. Another study using ileostomy subjects showed 88% recovery of inulin (DP = 10) and 89% recovery of oligosaccharides (DP = 4) in the effluent (12). Thus, our findings argue against the previous notion that pigs are not a proper model for humans to study inulin and oligosaccharides because these compounds are nearly completely digested in the upper part of the GI tract (14,15). The discrepancy between the previous pig trials and the present study may be explained by differences in the methodology and nature of the test materials. In the study by Branner et al. (17), inulin (DP = 23) disappearance was based on digesta samples collected from the anus of ileostomy patient-mimicked pigs and hydrolysis of inulin in the 20- to 25-cm intact rectum was neglected. Using the same procedure, Bohmer et al. (24) observed only 57% instead of >90% inulin digestion in the upper gut before cecum. Apparently, the procedure did not yield consistent results. In the study by Houdijk et al. (18), only cecum digesta was collected from the T-cannula placed in the cecum of pigs. Actual digesta from the ileum could not be collected to compare the inter-segment changes of oligosaccharide (DP = 4) concentrations between ileum and cecum. Because cecum digesta had the highest inulin-degrading activity and a strong ability to degrade added inulin in vitro, the presumed digestion of inulin proximal to the cecum by Houdijk et al. (18) most likely occurred in the cecum. In comparison, our study has demonstrated the consecutive changes of digesta inulin from the stomach to the distal colon. The distribution of ingested inulin in the digesta of different segments was consistent with their particular inulin-degrading activities. However, our experimental design did not allow us to determine the actual rates of flow or disappearance of inulin in individual GI segments. Reference digestibility markers such as Cr2O3 may be added in the test diets for that purpose in future studies.

The application of HPLC analysis of digesta inulin has given us not only a more accurate quantification of inulin over the simple subtraction method of proximate nutrient analysis (18), but it also provides an opportunity to explore the effect of supplemental inulin on digesta carbohydrate profiles. In both experiments, pigs fed 4% inulin had higher concentrations of fructose in digesta from stomach and jejunum than pigs fed the BD. Although it is not clear whether this moderate release of fructose from the ingested inulin was due to acid hydrolysis in the stomach (25) or to altered microbial fermentation by inulin (26), the elevated free fructose concentration might be beneficial to iron absorption (7). It has been reported that fructose forms a stable ferric fructose chelate to enhance iron bioavailability (27,28). Presumably, fructose liberated from inulin in the upper GI tract may form a stable complex with iron (III) atoms, which may partially explain the improved hemoglobin repletion efficiency in pigs fed inulin in Expt.1 (7). Although high concentrations of fructose uptake can be a risk factor for obesity and other metabolic abnormalities (29,30), the very limited amount (µmol/g) of fructose from the slow hydrolysis of inulin in the small intestine may not present a major health concern. In fact, the elevated fructose concentrations in the digesta of stomach and jejunum in pigs fed inulin account for only 0.01% of digesta inulin concentrations in those segments. Thus, the changes in digesta fructose concentration did not seem to suggest appreciable hydrolysis of inulin in the stomach or the small intestine. In addition, supplemental dietary inulin elevated ileum digesta concentrations of stachyose and raffinose in Expt. 1 and sucrose in Expt. 2. These changes might be the results of, but not limited to, altered viscosity of digesta (31), reduced activity of sucrase, and reduced hydrolysis of stachyose or raffinose (32) by inulin feeding. Because soybean meal in our BD contained raffinose and stachyose that may affect colonic fermentation (33), it would be interesting to correlate alterations of these polysaccharides with growth/activity of beneficial bacteria induced by inulin (8).

Interestingly, inulin-degrading enzyme activity was induced by inulin feeding in the cecum digesta of pigs but not as much in proximal colon digesta. A number of studies have shown that inulin stimulates the proliferation of Bifidobacteria in the colon (34,35) and there is a strong correlation between the number of Bifidobacteria and inulin-degrading enzyme activity (36–39). Future research needs to determine which bacterial strains in the cecum are responsible for the induced inulin-degrading activity in pigs fed inulin.

In conclusion, we have provided 3 lines of solid evidences to suggest cecum as the major degradation site of ingested inulin in the GI tract of young pigs. This helps clarify the confusion on the site of inulin disappearance created by previous experiments with technical drawbacks (14,15) and supports the continued use of pigs as a model of humans for inulin studies. The rapid degradation of inulin in the cecum, the inducible inulin-degrading activity in cecum digesta, and the responses of digesta fructose, raffinose, stachyose, and sucrose concentrations in the upper GI tract to inulin feeding may lead to new directions for exploring the mechanisms of inulin in improving mineral nutrition and gut health.


   ACKNOWLEDGMENTS
 
We thank Larry Heller and Dr. Mike Rutzke for their technical support, Karl Roneker for his help with animal care, and Dr. Douwina Bosscher of Orafti Active Food Ingredients (Tienen, Belgium) for providing inulin.


   FOOTNOTES
 
1 Supported by a grant from Harvest-Plus, International Food Policy Research Institute (IFPRI) and Centro International Agriculture Tropical (CIAT). Mention of a trademark, proprietary product or vendor does not constitute a guarantee or warranty of the product by the USDA and does not imply its approval to the exclusion of other products or vendors that may also be suitable. Back

2 Author disclosures: K. Yasuda, R. Maiorano, R. M. Welch, D. D. Miller, and X. G. Lei, no conflicts of interest. Back

6 Abbreviations used: BD, basal diet; DP, degree of polymerization; GI, gastrointestinal. Back

Manuscript received 28 June 2007. Initial review completed 31 July 2007. Revision accepted 5 September 2007.


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 Introduction
 Materials and Methods
 Results
 Discussion
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K. Yasuda, H. D. Dawson, E. V. Wasmuth, C. A. Roneker, C. Chen, J. F. Urban, R. M. Welch, D. D. Miller, and X. G. Lei
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