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Article

Glucose-Based Oligosaccharides Exhibit Different In Vitro Fermentation Patterns and Affect In Vivo Apparent Nutrient Digestibility and Microbial Populations in Dogs

Division of Nutritional Sciences and Department of Animal Sciences, University of Illinois, Urbana, IL 61801 ^* Ross Products Division, Abbott Laboratories, Columbus, OH 43215

¹To whom correspondence should be addressed.

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION REFERENCES

 
To evaluate the potential of indigestible oligosaccharides (OS) to serve as "dietary fiber-like" ingredients, it is necessary to determine their extent of indigestibility. In vitro fermentation characteristics of two novel OS, -glucooligosaccharides (GOS) and a maltodextrin-like OS (MD), were compared to those of fructooligosaccharides (FOS), gum arabic (GA), guar gum (GG) and guar hydrolysate (GH). Total short-chain fatty acid (SCFA) production (µmol/g dry matter) as a result of MD fermentation was higher initially compared with GA (P < 0.01), but GA was more extensively fermented at 24 h (P < 0.01). Total SCFA production for GOS was similar to that for FOS, GG, GH and GA. In the second experiment, GOS and MD were added at 6% to an enteral formula control diet (Control) and fed to ileal-cannulated dogs in a 3 x 3 replicated Latin-square design. Ileal digestibility of glucose was lower (P < 0.05) and carbohydrate (CHO) numerically lower (P = 0.08) for both GOS and MD compared with the Control. Total tract digestibility of CHO and glucose was lower only for MD (P < 0.01) compared with the Control. Total fecal weights were higher (P < 0.01) for both GOS and MD treatments. Fecal concentration of bifidobacteria was numerically increased by GOS and MD supplementation (P = 0.13 and 0.23, respectively). Thus, GOS and MD are indigestible yet fermentable OS, and may act as "dietary fiber-like" ingredients.

KEY WORDS: • oligosaccharides • fermentation • intestinal microbiota • short-chain fatty acids • dogs

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION REFERENCES

 
Many oligosaccharides (OS)² are not hydrolyzed in the small intestine but are fermented rapidly in the lower gastrointestinal tract of humans and nonruminant animals. Gibson and Roberfroid (1995) used the term "prebiotics" for certain nondigestible OS because they selectively stimulate favorable endogenous bacterial populations when supplemented in the diet at low levels. Both the fermentation process and the proliferation of favorable bacteria caused by OS ingestion can benefit the host animal. Oligosaccharides are fermented rapidly to yield short-chain fatty acids (SCFA), including butyrate, which is a fuel for colonocytes (Sakata 1987 ). Favorable bacterial populations, such as bifidobacteria, can promote health by inhibiting pathogenic bacteria such as Clostridium perfringens and Escherichia coli (Araya-Kojima et al. 1995 , Gibson and Wang 1994 ).

An -glucooligosaccharide (GOS) was obtained through enzymatic synthesis from sucrose and maltose to yield a branched-chain (-1,2, -1,4 and -1,6 linkages) glucose polymer with an average degree of polymerization of 5. Maltodextrin-like glucose-based oligosaccharides (MD) were produced by heat and enzymatic treatment of cornstarch, creating a random distribution of - and ß- (1,4), (1,6), (1,2) and (1,3) linkages. It has an average molecular weight of 2000.

The objectives of this study were as follows: 1) to determine the in vitro fermentation characteristics of GOS and MD in reference to other fermentable oligosaccharides; 2) to determine the small intestinal digestibility of GOS and MD in ileal-cannulated dogs; and 3) to determine the effects of GOS and MD on fecal microbial populations in dogs.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION REFERENCES

 
In vitro experiment

    Substrates and donors. Substrates used in this study were GOS (Bioecolians, Solabia, Pantin Cedex, France), MD (Fibersol 2E, Matsutani Chemical Industry, Hyogo, Japan), fructooligosaccharides (FOS) (NutraFlora, Golden Technologies, Westminister, CO), gum arabic (GA), guar gum (GG) (TIC Gums, Belcamp, MD), and hydrolyzed guar gum with 24,000 MW (GH) (Fiberon S, Dainippon, Japan). Three healthy adult male human donors (average age 30 y; average weight 78 kg) served as sources of fecal material from which the inoculum was prepared. The donors consumed a "Western" diet and no antibiotics in the 3 mo preceding the experiment.

    Design. Substrates were fermented in vitro for 24 h with fresh human fecal microflora obtained from each of three donors. The experiment was designed as a randomized complete block with the three fecal donors serving as blocks. Treatments were allotted in a 6 x 7 factorial arrangement with six substrates and seven incubation lengths. Each block by treatment combination was assayed using duplicate fermentation tubes. Duplicate tubes containing no substrate also were fermented with each inoculum source and time point to correct for SCFA not arising from the substrates.

    Fermentation. Aliquots (9 mL) of sterile anaerobic buffer (95% CO₂/5% H₂, pH 6.8) were aseptically transferred into tubes containing 75 mg substrate. Buffer composition is presented in Table 1 . To maintain anaerobic conditions, the tubes were sealed with butyl rubber stoppers in an anaerobic (95% CO₂/5% H₂) chamber. Substrates were hydrated for ~2 h before incubation.

    Chemical analyses. A 1-mL aliquot was removed for immediate pH determination before centrifuging at 13,000 x g at 22°C for 3 min. The supernatant was stored at -70°C. Acetate, propionate, butyrate and lactate concentrations in cell-free supernatant were analyzed by ion exclusion chromatography using a Hewlett Packard Model HP1090 Liquid Chromatograph equipped with an ION-300 ion exclusion column (30 cm x 7.8 mm i.d.) (Interaction Chemicals, Mountain View, CA). The mobile phase consisted of 0.005 mol/L H₂SO₄ with a flow rate of 0.3 mL/min and 40°C column temperature.

    Statistical analyses. Data were analyzed as a randomized complete block with fecal donor serving as the block. The model statement included donor, substrate, time and substrate x time. All analyses were performed according to the General Linear Models (GLM) procedure of SAS (1994) . Arithmetic means are reported along with the SEM for all treatments. When treatment differences were detected (P < 0.05), means were compared by the least significant difference method (Carmer and Swanson 1973 ).

In vivo experiment

    Animals and diets. Six purpose-bred adult female dogs (Butler Farms USA, Clyde, NY) with hound bloodlines and an average weight of 25.3 ± 4.6 kg and age of 3 ± 1.5 y were surgically prepared with ileal cannulas. Ileal cannulation was conducted according to Walker et al. (1994) . Dogs were housed individually in clean floor pens (1.2 x 3.1 m) in a temperature-controlled room at the animal facility of the Edward R. Madigan Laboratory on the University of Illinois campus. All dogs were allowed free access to water. The surgical and animal care procedures were approved by the Campus Laboratory Animal Care Advisory Committee, University of Illinois at Urbana-Champaign.

Two OS treatments were tested against a control: Enteral Control, Enteral Control + GOS (GOS), and Enteral Control + MD (MD). An enteral diet was selected as the control because it provided very highly digestible nutrients for the dogs, allowing a more exact test of the less digestible OS. The OS were added at the 6% level [dry matter (DM) basis] to the Control diet, such that they did not replace any individual dietary component. Diets were reconstituted before feeding by adding 235 g of Enteral Control powder to 835 mL H₂O, or 249 g of the GOS or MD diets to 825 mL H₂O.

The chemical composition of the experimental diets is reported in Table 2 . Dietary protein was provided as sodium caseinate, calcium caseinate and soy protein isolate. Corn oil was used as the sole lipid source, whereas corn syrup and sucrose comprised the carbohydrate portion of the diet. On an energy basis, the enteral diets supplied ~14% of kJ as protein, 31.5% as fat and 54.5% as carbohydrate.

    Sampling procedures. During the collection phase, ileal effluent and feces were collected for 4 d. Ileal effluent was collected 3 times per day, with an interval of 4 h between collections. Individual ileal collections were 1 h in duration. Sampling times on the remaining 3 d were rotated 1 h from the previous day’s collection time. For example, on d 1, sampling took place at 0800, 1200 and 1600 h; on d 2, samples were collected at 0900, 1300 and 1700 h. Ileal samples were obtained by attaching a Whirlpak bag (Pioneer Container, Cedarburg, WI) to the cannula barrel and around the cannula hose clamp with a rubber band. Before attachment of the bag, the interior of the cannula was scraped clean with a spatula and initial digesta discarded. During collection of ileal effluent, dogs were encouraged to move around freely. The use of Elizabethan collars was necessary for some dogs to deter them from pulling the collection bag from their cannula. Total feces excreted during the collection phase of each period were collected from the floor of the pen, weighed, composited and frozen at -4°C.

    Sample handling. Ileal samples were frozen at -4°C in their individual bags. At the end of the experiment, all ileal effluent samples were composited for each dog for each period, and then refrozen at -4°C. Ileal effluent then was freeze-dried in a Tri-Philizer MP microprocessor-controlled lyophilizer (FTS Systems, Stone Ridge, NY). Feces were dried at 55°C in a forced-air oven. After drying, both feces and ileal samples were ground through a 2-mm screen in a Wiley mill (model 4, Thomas Scientific, Swedesboro, NJ). Diets were analyzed in the unhydrated powdered form.

Freshly voided feces were collected within 15 min of defecation; individual aliquots were immediately transferred to preweighed Carey-Blair transport media containers (Meridian Diagnostics, Cincinnati, OH) for subsequent bacterial enumeration. Feces were scored for each dog during each period according to the following system: 1 = hard, dry pellets, small, hard mass; 2 = hard, formed, dry stool, remains firm and soft; 3 = soft, formed, moist, softer than stool that retains shape; 4 = soft, unformed, stool assumes shape of container, pudding-like; 5 = watery; liquid that can be poured.

    Chemical analyses. Diets, feces and ileal effluent were analyzed for DM, organic matter (OM) and ash using AOAC (1984) methods. Crude protein (CP) was calculated from Kjeldahl N values (AOAC 1984 ). Total lipid content was determined by acid hydrolysis followed by ether extraction according to the American Association of Cereal Chemists (1983) and Budde (1952) . Chromium was analyzed according to Williams et al. (1962) using an atomic absorption spectrophotometer (Model 2380, Perkin-Elmer, Norwalk, CT). Carbohydrate (CHO) content was calculated as the difference between OM content and the sum of crude protein and lipid contents. Glucose content was determined by monosaccharide analysis according to Bourquin et al. (1990) . Monosaccharides were hydrolyzed with H₂SO₄ and quantified by anion exchange HPLC with pulsed electrochemical detection. Briefly, 50 µL of each neutralized, hydrolyzed sample was injected into an HPLC fitted with a Dionex Carbo-Pac PA-1 column (250 x 4 mm) (Dionex, Sunnyvale, CA). Individual monosaccharides were eluted with degassed water (1.0 mL/min, ambient temperature) and 300 mmol/L NaOH was added postcolumn. For all laboratory analyses, samples were analyzed in duplicate, and analyses were repeated if a deviation > 5% between duplicates occurred.

Total anaerobes, total aerobes, bifidobacteria, lactobacilli and bacteroides spp. were determined by serial dilution of fecal samples in anaerobic diluent (Bryant and Burkey 1953 ) before inoculation onto respective petri dishes of sterile agar. Total anaerobe and total aerobe agars were prepared according to Bryant and Robinson (1961) and Mackie et al. (1978) . The selective medium for bifidobacteria (BIM-25) was prepared using reinforced clostridial agar (BBL Microbiology Systems, Cockeyville, MD) according to the method described by Muñoa and Pares (1988) . Lactobacilli were cultured on Rogosa SL agar (Difco Laboratories, Detroit, MI). Bacteroides spp. were cultured on a trypticase yeast extract glucose agar listed in Table 3 . Plates were incubated anaerobically (95% CO₂/5% H₂) at 38°C. Colony forming units were defined as being distinct colonies measuring at least 1 mm in diameter.

    Statistical analysis. Data were analyzed by the General Linear Models procedure of SAS (1994) . The experimental design was a replicated 3 x 3 Latin square. Six sequences of the diets (one sequence per dog) were used (ABC, CAB, BCA, ACB, BAC, CBA), where A was Enteral Control, B was Enteral Control + GOS, and C was Enteral Control + MD. Model sums of squares were separated into treatment, period and animal effects. When significant (P < 0.05) differences were detected, treatment means were compared by the least significant difference method of SAS (Carmer and Swanson 1973 ).

	RESULTS AND DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION REFERENCES

 
In vitro experiment

    pH values. In general, pH decreased as time of fermentation increased (Fig. 1 ). All substrates had similar pH values (6.9) at 0 h. Fructooligosaccharide fermentation resulted in the most rapid decline in pH and the lowest pH values (P < 0.05) at 3 and 6 h. Conversely, GA had the slowest decline in pH and the highest pH values (P < 0.05) at 1.5, 3, 6 and 11 h of fermentation. The pH values for GOS, GH, GG and MD generally were intermediate to that of FOS and GA between 0 and 6 h. However, at 24 h, GOS had a numerically lower pH (P = 0.18) than FOS and a lower pH (P < 0.05) than all other substrates. The pH decline for MD was rapid from 0 to 3 h, but then was relatively stable. At 24 h, the highest (P < 0.05) pH value was noted for MD (6.31) compared with all other substrates. Overall, the pH declines for GOS, FOS, GH and GG were not different (P = 0.35) from those of MD and GA.

View larger version (23K): [in this window] [in a new window]   Figure 1. The pH values of substrates after different times of in vitro fermentation. Values are means, n = 6. Asterisks indicate a significant difference from all other means at that time, P < 0.05. FOS, fructooliogsaccharide; GOS, -glucooligosaccharide; GH, hydrolyzed guar gum; GG, guar gum; MD, maltodextrin-like glucose-based oligosaccharide; GA, gum arabic.

(Table 4

In contrast to the 11-h observation, after 24 h of fermentation, the concentration of acetate for GA was greater than FOS (P < 0.05) and numerically greater than GOS (P = 0.10) (Table 4) . The concentration of acetate produced by GOS remained greater (P < 0.05) than that of MD, which was similar to the values for GG, GH and FOS. After 24 h of incubation, propionate concentration was numerically lowest (P = 0.15) for FOS (Table 4) . Butyrate accumulation was greater (P < 0.05) for FOS, GOS, GH and GG, than for MD and GA (Table 4) after 18 and 24 h of incubation. The highest butyrate-producing substrates resulted in ~5–35 times greater values compared with the lowest butyrate-producing substrates after 11–24 h of fermentation. Relatively little lactate accumulated, and none was detected after 6 h of fermentation (data not shown). Fructooligosaccharides had the highest (P < 0.05) concentrations of lactate at 3 and 6 h of fermentation. No lactate accumulated as a result of the fermentation of GG or GA.

The more rapid pH decline and organic acid production as a result of FOS and GOS fermentation indicated that these two OS were fermented more rapidly than the other substrates tested in this study. Maltodextrin-like oligosaccharides resulted in the lowest in vitro production of organic acids and the highest pH at 24 h, indicating some resistance to fermentation. Short-chain fatty acid profiles, in addition to concentrations, varied among substrates. Butyrate production was highest and similar for FOS, GOS, GH and GG. Butyrate is a major fuel for colonocytes (Roediger 1980 ) and has been demonstrated to stimulate epithelial cell proliferation (Sakata 1987 ). Therefore, substrates that produce high levels of butyrate, such as FOS, GOS, GG and GH, may provide similar beneficial effects when included in diets. The rapid in vitro accumulation of butyrate with FOS fermentation at 6 h indicates that FOS would serve as an excellent source of butyrate in vivo. On the other hand, the slower rate of fermentation of GA and MD indicates that they would perhaps provide a source of fermentable CHO to the more distal part of the large intestine. A blend of rapidly and slowly fermented carbohydrates should result in production of SCFA throughout the large intestine.

In vivo experiment

    Chemical composition. The chemical composition of the diets is reported in Table 2 . Dry matter, OM, CP, fat, glucose and CHO content did not differ among diets.

    Nutrient intake and apparent digestibility. Intakes of DM, OM and CP did not differ (Table 5). Fat intake was lower (P < 0.05) for the Control treatment than for either the GOS or MD treatments due to lower DM intakes. Dogs consuming either the GOS- or MD-containing diets had greater (P < 0.05) glucose and numerically greater (P = 0.09) CHO intakes compared with the Control diet. This was expected because GOS and MD were added at 6% "on top" of the control diet.

View this table: [in this window] [in a new window]   Table 5. Nutrient intakes and apparent digestibility data for ileal-cannulated dogs fed diets supplemented with -glucooligosaccharide (GOS) or maltodextrin-like glucose-based oligosaccharide (MD)

Total tract digestibilities of DM and fat did not differ among treatments. Crude protein digestibility was lower (P < 0.05) for dogs consuming the GOS and MD treatments. The lower values for total tract digestibility of the GOS and MD diets may be attributed to an increased fecal excretion of microbial protein. Wolf et al. (1998) proposed that as the percentage of fermentable carbohydrate increases in the diet, the amount of microbial mass increases in the feces. This would result in an increase in fecal N excretion and an apparent decrease in crude protein digestibility. Organic matter, carbohydrate and glucose digestibilities were lower (P < 0.05) for the MD treatment compared with either the Enteral Control or the GOS treatments. This may indicate that MD was not completely fermented in the large intestine as suggested by our in vitro study. Incomplete fermentation also was reported by Tsuji and Gordon (1998) , who recovered 38% of orally dosed MD in the feces of adult rats. There was a trend for carbohydrate and glucose digestibility to be slightly lower for the GOS diet compared with the Control. This suggests that GOS was extensively fermented. These findings agree with those of Djouzi et al. (1995) who demonstrated that GOS was fermented extensively by human intestinal bacterial strains in vitro and in vivo by trixenic rats associated with Bacteroides thetaiotaomicron, Bifidobacterium breve and Clostridium butyricum.

    Fecal weight, fecal score, and body weight changes. There were no differences among treatments in body weight changes of dogs (data not shown). Fecal weights for dogs consuming the GOS diet were greater (P < 0.05) than those of the Control on an as-is basis and tended (P = 0.07) to be greater on a DM basis (Table 6). Fecal weight, on both an as-is and DM basis, was greater (P < 0.05) for dogs consuming the MD treatment compared with the Control. On a DM basis, the fecal weight for MD was greater (P < 0.05) than that of GOS. These data, along with the high 24-h pH value for MD after 24 h of in vitro fermentation, indicate that it is not completely fermented by the colonic microflora of dogs or humans. Increased fecal weight is a common outcome of dietary fiber consumption. Depending on its individual characteristics, dietary fiber can increase fecal bulk by increasing bacterial cell mass, undegraded fiber residue, fecal water or a combination of these effects (Fahey et al. 1990 , Roberfroid 1993 , Schneeman, 1987 ). Fecal scores were higher (P < 0.05) for dogs consuming the GOS and MD treatments compared with the Control, indicating a higher fecal moisture content. Overall, the fecal scores were relatively high. The loosely formed stools were caused in part by consumption of an enteral formula. Increased fecal moisture content is a common effect attributed to dietary fiber. Fecal water content can be increased by the physical water-holding properties of fibers, and possibly by the osmotic action of SCFA produced by fermentation (Roberfroid 1993 , Schneeman 1987 ).

View this table: [in this window] [in a new window]   Table 6. Fecal characteristics of ileal-cannulated dogs fed diets supplemented with -glucooligosaccharide (GOS) or maltodextrin-like glucose-based oligosaccharide (MD)

View this table: [in this window] [in a new window]   Table 7. Fecal bacterial concentrations for cannulated dogs fed diets supplemented with -glucooligosaccharide (GOS) or maltodextrin-like glucose-based oligosaccharide (MD)1

Bacteroides are the predominant colonic bacterial genera, comprising ~30% of the total culturable microflora (Macfarlane and Macfarlane 1995 ). Most bacteroides are considered neither beneficial nor detrimental to host health. They readily utilize resistant starch as well as nonstarch polysaccharides (Hudson and Marsh, 1995 ). In our experiment, GOS and MD led to a numerical increase in fecal concentrations of bacteroides.

Ileal-cannulated dogs were chosen as the animal model for this study for the many similarities they share with humans. Both dogs and humans are omnivorous monogastrics. Like humans, dogs have numerous species of endogenous bacteria in their lower gastrointestinal tract (Balish et al. 1977 , Davis et al. 1977 ) that contribute to significant amounts of colonic fermentation (Banta et al. 1979 ). The microflora of both dogs and humans contains bacteroides, bifidobacteria and lactobacilli as predominant species (Davis et al. 1977 , Gibson and Roberfroid 1995 ). Dogs have been employed in numerous studies pertaining to human nutrition (Diez et al. 1997 and 1998 , Willard et al. 1994 ). The ileal-cannulated dog model has been widely used to evaluate ileal digestibility of nutrients in many types of ingredients (Muir et al. 1996 ; Murray et al. 1997 and 1998 , Zuo et al. 1996 ). Therefore, the ileal-cannulated dog is an appropriate model to utilize in evaluating oligosaccharides with potential human applications.

The in vitro and in vivo studies provided complementary data regarding the fermentation of the novel OS, GOS and MD. In vitro, the fermentation of GOS resulted in rapid production of high concentrations of SCFA, whereas MD fermentation resulted in a more gradual and overall lower SCFA production. In vivo, GOS and MD resisted hydrolytic digestion and were present at the terminal ileum. -Glucooligosaccharide appears to be extensively fermented because very little was recovered in feces. However, MD was fermented only partially, resulting in significantly lower total tract CHO and glucose digestibility values.

In conclusion, both GOS and MD appear to be indigestible in the small intestine, supplying CHO to the large intestine for bacterial fermentation. Both in vitro and in vivo digestibility data suggest that GOS was fermented more extensively than MD. Dietary supplementation of these OS at the 6% level in an enteral formula did not greatly alter the digestibility of macronutrients. Both GOS and MD increased the volume of feces excreted and the moisture content of the feces. These OS also tended to increase fecal concentrations of beneficial bacteria, including bifidobacteria. These findings indicate that GOS and MD are indigestible in the upper intestinal tract. However, these OS may serve as fermentable dietary fiber-like substrates and positively affect gastrointestinal tract health.

	FOOTNOTES

 
² Abbreviations used: CHO, carbohydrate; CP, crude protein; DM, dry matter; FOS, fructooligosaccharide; GA, gum arabic; GG, guar gum; GH, hydrolyzed guar gum; GOS; -glucooligosaccharide; MD, maltodextrin-like glucose-based oligosaccharide; OM, organic matter; OS, oligosaccharide; SCFA, short-chain fatty acids.

Manuscript received October 14, 1999. Initial review completed December 9, 1999. Revision accepted February 1, 2000.

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