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Prebiotics in companion animal nutrition |
 
Who saw this article? New!
Author: KELLY S. SWANSON and GEORGE C. FAHEY, JR.- University of Illinois (Courtesy of Alltech Inc.)
Publication date: 02/27/2007
The colonic microbiota play an important role in the health of the gastrointestinal tract and of the host animal. Diet, in turn, plays an important role in determining the composition of the gut microflora. Prebiotics are dietary constituents that may be used to beneficially alter microbial populations in the gut, thereby preventing pathogenic invasion and improving host health. A prebiotic is a nondigestible food ingredient that beneficially affects the host by selectively stimulating the growth and/or activity of a limited number of bacteria already inhabiting the colon (Gibson and Roberfroid, 1995).
The most common prebiotics studied are fructans, which reach the colon and are highly digestible substrates for bacteria. More specifically, ingestion of fructans selectively stimulates the population of bifidobacteria in the colon. Bifidobacteria are one of the beneficial microbial species in the colon. By producing bacteriocins, acetate, and lactate, bifidobacteria decrease luminal pH and create an unfavorable environment for several pathogens.
Fructans also effectively relieve the symptoms of constipation in humans (Kleesen et al., 1997) and improve mineral absorption in rats (Binder and Mehta, 1989). In addition to manipulating colonic microflora populations, fructan supplementation also may decrease concentrations of protein catabolites produced in the colon by providing gut microflora with an additional energy supply. Mannanoligosaccharides (MOS) are another type of oligosaccharide that may positively influence gut microbial populations and immune capacity.
Mannanoligosaccharides are moderately fermentable and serve as a substrate for lactic acid bacteria (Bolduan, 1999), but their role in pathogen resistance and modulation of the immune system are most often studied. Mannans aid in the resistance of pathogenic colonization by acting as receptor analogues for Type-1 fimbriae present on E. coli and Salmonella species (Oyofo et al., 1989b). Mannans also have been reported to modulate the immune system, increasing immunoglobulin (Ig) A concentration in cecal contents of rats (Kudoh et al., 1999) and increasing neutrophil activity in dogs (O’Carra, 1997). Finally, there is some evidence that mannans may be a promising natural protective agent due to their antimutagenic and antioxidative activity (Chorvatovičová et al., 1999; Križková et al., 2001). Other oligosaccharides have prebiotic activity and will be mentioned later in this review.
Importance of microbial populations in the gastrointestinal tract
The hindgut of most animals contains a complex and dense population of microbial species. Depending on the composition of the microflora, their presence may be beneficial or harmful to the host. Although the microbiota may be a burden in some respects, this is heavily outweighed by the crucial role they play in the development of the immune system, resistance to pathogenic colonization, short-chain fatty acid (SCFA) production, and gene expression in the gut.
The intestine is the largest immune organ of the body (Jalkanen, 1990) with the gut-associated lymphoid tissues (GALT) possessing approximately 80% of the body’s immunological secreting cells (Brandtzaeg et al., 1989) and more than 50% of the immune effector cells (McKay and Perdue, 1993).
The development of GALT is highly dependent on the colonization of bacterial populations in the gut. This may be demonstrated by studying gnotobiotic (germ-free) animals, which have abnormal intestinal morphology and underdeveloped local immune systems, including decreases in total lymphocyte numbers, skewed intestinal lymphocyte and antibody profiles and underdeveloped Peyer’s patches (Thorbecke, 1959; McCracken and Gaskins, 1999).
Indigenous bacterial populations aid in pathogenic resistance by competing for nutrients and binding sites and producing antimicrobial compounds. Lactate produced from Lactobacillus and Bifidobacterium decreases luminal pH, creating an unfavorable environment for many pathogenic strains. Many indigenous microbes also produce bacteriocins that have a bactericidal mode of action against other bacterial strains, but not against themselves (Tagg et al., 1976).
Acetate, propionate and butyrate are the main SCFA end products of bacterial fermentation of organic matter (OM) in the large intestine. Shortchain fatty acids are the main energy source for colonocytes, in particular, butyrate, which is the preferred energy substrate of colonic epithelium (Roediger, 1982) and may account for up to 70% of its total energy consumption (Roediger, 1980).
Similar to lactate, these organic acids decrease luminal pH and assist in pathogen resistance. Recent reports also suggest that commensal bacteria modulate expression of genes involved with several important intestinal functions including nutrient absorption, mucosal barrier fortification, xenobiotic metabolism, angiogenesis and postnatal intestinal maturation (Hooper et al., 2001).
Therefore, gut physiology can be affected by changes in the composition of the indigenous microflora. It is apparent that over time, mammals have adapted and become quite dependent on microbes and their activities in the gastrointestinal tract.
Although the indigenous microflora may play many important roles in the gut, it also can be a burden on the body. Examples include an increased turnover of mucus and epithelial cells and the constant production of inflammatory and immune cells. Several pathogenic strains of bacteria produce protein toxins that disrupt the normal processes of host cells. Two research groups have recently shown that Campylobacter jejuni (Lara-Tejero and Galán, 2000) and Esherichia coli (Elwell and Dreyfus, 2000) are able to produce a family of bacterial toxins called the cytolethal distending toxins (CDTs) that result in marked swelling and eventual death of cultured mammalian cells. The CDTs result in arrest of host cells in the G2 phase of the cell cycle, eventually leading to cell destruction (Coburn and Leong, 2000). Some bacterial pathogens also are able to control NF-kB activation, which is now believed to be a major player in the inflammatory response of the gut (Karin and Ben-Neriah, 2000).
Diet has a dramatic impact on the bacterial populations inhabiting the colon. Both source and level of dietary protein influence the occurrence of pathogens in feces (Amtsberg et al., 1980). The typical Western diet of humans, many dog foods, and most cat foods commonly contain high concentrations of protein, which can lead to an increased colonic presence of undigested amino acids (AA) and fecal putrefactive compounds (Hobbs et al., 1996). Increasing the protein flow to the colon provides more substrates for pathogenic species such as Clostridium perfringens, which is known for its ability to degrade AA and produce fecal odor. Protein entering the colon may originate from several sources including dietary proteins escaping small intestinal breakdown, endogenous proteins (e.g., pancreatic and small intestinal secretions, sloughed epithelial cells), digestive mucins and blood urea diffusing into digestive contents (Mason, 1984; Moran and Jackson, 1990; Macfarlane and Macfarlane, 1997). The colonic microbiota metabolize nitrogenous compounds to putrefactive catabolites such as ammonia, biogenic amines, and phenols that are implicated as the major odor components of feces (Spoelstra, 1980; O’Neill and Phillips, 1992). More importantly, many of these protein catabolites may have negative influences on gut health. Ammonia is produced by the deamination of AA in the colon. High concentrations of ammonia are suspected to disturb the mucosa cell cycle and contribute to colon carcinogenesis (Visek, 1978; Thornton, 1981; Lin and Visek, 1991). Indoles and phenols are breakdown products of the aromatic AA in the gut.
Indoles originate from tryptophan while phenols are produced from tyrosine. Phenol has been reported to promote skin cancer (Boutwell and Bosch, 1959) and exacerbate ulcerative colitis (Ramakrishna et al., 1991). Phenols are usually excreted in urine after glucuronide or sulfate conjugation, which occurs in the large intestinal mucosa or liver (Tamm and Villako, 1971). However, little is known about phenol metabolism in the colon. Biogenic amines originate from AA and are primarily produced by decarboxylation reactions that occur in the colon.
Johnson (1977) reported increased decarboxylase activity and the number of bacterial species with high decarboxylase production in the colon of cancer patients vs normal subjects. Although amine concentrations were not measured in this study, the potential for producing greater amounts of amines would be higher in the presence of high decarboxylase levels. Therefore, biogenic amines also may play a role in the development of colon cancer. Although there is some evidence that amines may promote malignancy, polyamines stimulate DNA, RNA, and protein synthesis (McCormack and Johnson, 1991) and are important in the maturation of the intestinal mucosa (Capano et al., 1994). Because of their rapid absorption by the small intestine (Bardocz et al., 1993), microbial production of polyamines is probably very important for providing available polyamines for the large intestinal mucosa (Noack et al., 1998).
Manipulation of microbial populations by prebiotics
Classes of food-grade oligosaccharides include cyclodextrins, fructooligosaccharides (FOS), galactooligosaccharides, gentiooligosaccharides, glucosyl sucrose, isomaltooligosaccharides, lactosucrose, lactulose, maltooligosaccharides, palintose oligosaccharides, soybean oligosaccharides, and xylooligosaccharides (XOS) (Crittenden and Playne, 1996). Although some of these compounds are digested in the stomach and small intestine, many reach the colon intact and act as prebiotics. The most common prebiotics studied are fructans. The general term ‘FOS’ may include all nondigestible oligosaccharides composed of fructose and glucose units. Specifically, FOS refers to short chains of fructose units bound by ß(2-1) linkages and attached to a terminal glucose unit. Although FOS is found naturally in several plant sources (e.g., chicory, wheat, garlic, onions), it is produced commercially from sucrose via ßfructofuranosidase from Aspergillus niger or from inulin hydrolysis.
The ß(2-1) linkages present in fructans have been shown to be resistant to mammalian enzymes. Therefore, fructans reach the colon and are highly digestible substrates for bacteria. Oku et al. (1984) reported that <0.5% of short-chain FOS (scFOS) was hydrolyzed by rat intestinal mucosa. Hidaka et al. (1986) reported similar results, observing little scFOS hydrolysis when incubated in vitro with human salivary enzymes, rat pancreatic homogenate, or rat small intestinal mucosa homogenate. When scFOS was fed to human subjects, Hidaka et al. (1986) reported no differences in blood glucose or insulin responses, suggesting little or no digestion and absorption in the small intestine. Furthermore, in vitro work performed by Nilsson et al. (1988) reported that at pH >1.8, <1% oligofructose (OF) was hydrolyzed by human gastric juice. The recovery of OF from the small intestine of rats was similar to that of polyethylene glycol, a nondigestible marker, proving that it is nondigestible by mammalian enzymes. Tokunaga et al. (1989) proved that scFOS was degraded by microbial populations by incubating 14C-labelled scFOS in cecal contents of rats. After incubation, approximately 90% of the 14C was detected in fermentative end-products, namely SCFA (66%), CO2 (12%), and fecal biomass (6 to 10%).
Supplementation of fructans has been shown to enhance gut health in many ways. Their consumption may result in dramatic changes in the composition of gut microflora. Ingestion of fructans selectively stimulates the population of bifidobacteria, usually at the expense of clostridia and bacteroides species. Bifidobacterium species are selectively enhanced because of their ßfructosidase activity, which is selective for the ß(2-1) glycosidic linkages (de Vries and Stouthamer, 1967). Bifidobacteria are considered beneficial species as they have low xenobiotic metabolizing enzymes relative to E. coli and clostridia and decrease colonic pathogen concentrations (Chadwick et al., 1992). Some species of bifidobacteria are able to exert antimicrobial effects on various gram-positive and gram-negative intestinal pathogens including salmonellae, Campylobacter, and E. coli (Gibson and Wang, 1994). In addition to the production of bacteriocins, acetate and lactate produced from bifidobacteria decrease luminal pH, creating an unfavorable environment for many pathogens.
Fructans also effectively prevent and treat constipation. Inulin, a long-chain FOS, has been reported to increase stool frequency and moisture content in constipated humans (Kleesen et al., 1997; Hond et al., 2000). Short-chain fructooligosaccharides have been shown to improve the symptoms of constipation as well (Hidaka et al., 1986). In addition, SCFA produced from colonic fermentation have been shown to stimulate intestinal peristalsis (Kamath et al., 1988). Finally, fructan supplementation has been shown to improve mineral absorption. This effect is believed to be due to SCFA, which improves colonic absorption of Na+, Ca++, and Cl- (Binder and Mehta, 1989; Lutz and Scharrer, 1991). The increased absorption is thought to be due to exchange mechanisms (e.g., Na+-H+ exchange) present in the colon.
In addition to manipulating colonic microflora populations, fructan supplementation also may decrease concentrations of protein catabolites produced in the colon by providing gut microflora with an additional energy supply. The metabolism of nitrogen (N) in the colon by microflora may be modified by the availability of substrate, particularly by dietary carbohydrate (Rémésy and Demigné, 1989; Younes et al., 1995). Fermentable carbohydrates, including fructans, may decrease the concentration of putrefactive compounds by providing gut microflora with an additional energy supply. In the colon, bacteria act as N sinks utilizing the undigested protein and its metabolites in the presence of energy for protein synthesis (Cummings et al., 1979). Bacteria use ammonia as a major source of N, and other forms of protein or AA are deaminated to ammonia before being used metabolically (Jackson, 1995). Carbohydrates (e.g., fructans, resistant starch, dietary fiber) serve as the energy sources needed to produce microbial protein.
When energy (carbohydrate) supplies are limited, bacteria ferment AA to SCFA and ammonia in order to obtain energy (Russell et al., 1991). However, if a sufficient energy source is provided, the luminal concentrations of nitrogenous compounds decrease and the concentrations of fecal nitrogen (bacterial mass) increase (Cummings et al., 1979; Cummings and Bingham, 1987).
Fructan supplementation may also decrease the production of protein catabolites implicated as fecal odor components by modulating microbial populations, consequently affecting fecal enzyme activities. In general, species of Bifidobacterium and Lactobacillus possess low activities of xenobioticmetabolizing enzymes (azoreductase, nitroreductase, nitrate reductase, and ß-glucuronidase) in comparison to other major anaerobes in the gut such as bacteroides, eubacteria, and clostridia (Cole et al., 1985; Saito et al., 1992).
These fecal enzymes interact with various compounds found in intestinal digesta to produce putrefactive compounds, which produce fecal odor and may be highly carcinogenic. One example is ß-glucuronidase, which is responsible for the hydrolysis of the conjugated forms of phenols in urine into their free forms upon contact of urine and feces (Spoelstra, 1977). Hidaka et al. (1986) supplemented rat diets with 0.4, 2.0, or 10.0% scFOS.
Although no significant differences were observed in rats fed 0.4 or 2.0%, rats fed 10% scFOS had increased fecal total SCFA (approximately 3,000 μg/g feces increased to over 8,000 μg/g), decreased fecal pH (7.8 vs 7.1), and decreased concentrations of phenols in fecal (approximately 25 μg/d vs < 5 μg/d) and urine (approximately 400 μg/d vs < 100 μg/d) samples. No changes were observed in urinary indican concentrations. Aberrant crypt foci, pre-neoplastic lesions in the colon, often are measured and used as an indicator of a compound’s effectiveness to inhibit colon cancer in animal cancer models. Reddy et al. (1997) reported that OF (10%) or inulin (10%) supplementation significantly inhibited aberrant crypt formation and crypt multiplicity in the colon of rats, with inulin having a more pronounced effect. In this experiment, rats fed the control diet averaged 120 aberrant crypts/ colon while rats fed OF and inulin averaged 92 and 78 aberrant crypts/colon, respectively. Crypt multiplicity was examined by counting number of crypts for each aberrant focus. While there were no differences among groups in foci containing 1 or 4 crypts, control rats had significantly more foci with 2 or 3 crypts. Hughes and Rowland (2001) reported increased apoptotic indices, but no changes in ßglucuronidase activity, in rats fed OF (5%) or inulin (5%). Apoptotic Index (AI) is the number of positive cells expressed per crypt counted. Rats fed the basal diet had an AI of approximately 4, while rats fed OF and inulin had AIs of approximately 12 and 14, respectively. Oligofructose and inulin tended (P = 0.11) to decrease colonic ammonia concentrations as well. Ammonia concentrations were decreased from approximately 81 μmol/g in rats fed the basal diet to approximately 49 μmol/g (OFfed rats) and 47 μmol/g (inulin-fed rats). By increasing apoptotic indices and inhibiting aberrant crypt foci formation and multiplicity, these initial animal experiments suggest a protective effect of prebiotics against colon cancer.
Mannanoligosaccharides (MOS) are another type of oligosaccharide, and the mechanism by which they act is different from that of fructans. Several researchers have studied mannans/MOS and their ability to agglutinate and interfere with intestinal binding and colonization of harmful species such as E. coli and Salmonella (Oyofo et al.,1989a, b, c; Finucane et al., 1999b; Spring et al., 2000). These studies have shown that numerous E. coli and Salmonella strains possess mannose-specific fimbriae, agglutinate MOS in vitro, and colonize in lower concentrations in animals supplemented with MOS. Fimbrial adhesins specific for mannan residues are referred to as ‘Type-1’ adhesins.
Mannans aid in the resistance of pathogenic colonization by acting as receptor analogues for Type-1 fimbriae and decrease the number of available binding sites (Oyofo et al., 1989b).
Mannans also have been reported to modulate the immune system, increasing IgA concentration in cecal contents of rats (Kudoh et al.,1999), increasing bile IgA (P<0.007) and systemic IgG (P<0.0001) in turkeys (Savage et al., 1996), and increasing neutrophil activity in dogs (O’Carra, 1997). In the experiment of Kudoh et al. (1999), IgA concentrations increased from approximately 15 μg/g (20 μg/total cecal contents) in cellulosefed rats to approximately 60 μg/g (240 μg/total contents) in glucomannan-fed rats. Although significant differences were not observed in the study of O’Carra (1997), peak concentrations of activated neutrophils at 14 days post-vaccination were numerically higher in dogs fed MOS (approximately 18 NBT+ cells/slide) compared with control dogs (approximately 14 NBT+ cells/slide).
Mannanoligosaccharide supplementation of turkey poults reportedly decreased (P<0.05) populations of Clostridium spp. (2.98 vs 4.22 log CFU/g) (Finucane et al., 1999a), microbes that do not possess mannose-specific fimbriae. Supplementation of MOS in turkeys has been reported to increase (P<0.05) goblet cell numbers as well (Savage et al., 1997). Mucus-secreting goblet cells play a crucial role in intestinal homeostasis (Neutra and Forstner, 1987). Therefore, MOS also may strengthen the defense barrier in the gut by mechanisms that are not completely understood at this time.
Finally, there is some evidence that mannans may be a promising natural protective agent due to their antimutagenic and antioxidative activity. Chorvatovičová et al. (1999) reported that glucomannans isolated from Candida utilis had a protective effect against cyclophosphamide-induced mutagenicity in mice. In vitro work done by these researchers suggested that the antimutagenic effect of glucomannans may be based on their ability to scavenge reactive oxygen radicals (Križková et al., 2001). If additional research supports the results of the experiments above, mannan supplementation could be used in the future to help prevent colon cancer.
Canine prebiotic experiments
Although a large body of literature exists regarding the effects of prebiotics on human health, only a handful of experiments using the canine have been reported. The focus of most experiments using dogs has been narrow, with most groups focusing on microbial populations and fecal consistency. The effects of lactosucrose on microbial populations and fecal metabolites was examined in dogs by Terada et al. (1992). Lactosucrose is a trisaccharide produced from lactose and sucrose by a ß-fructofuranosidase enzyme and has been shown to enhance bifidobacteria populations in humans (Fujita et al., 1991). Adult dogs were given 1.5 g lactosucrose/day for 2 weeks. Fecal and microbial characteristics were measured before lactosucrose administration, on day 7 and day 14 of lactosucrose administration, and 7 days after administration had ceased. Bifidobacteria populations were increased (P<0.05) from 8.9 CFU log10/g (baseline) to 9.4 and 9.4 CFU log10/g after 7 and 14 days of lactosucrose feeding, respectively. Bifidobacteria populations decreased to baseline levels (8.8 CFU log10/g) 7 days after feeding had stopped. Lecithinase-positive clostridia populations, which include C. perfringens, decreased after 7 days (P<0.05; 4.4 vs 6.0 CFU log10/g) and 14 days (P<0.01; 3.1 vs 6.0 CFU log10/g) of lactosucrose feeding. Lecithinasenegative clostridia concentrations, however, were unaffected. Lactosucrose feeding also increased (P<0.05) fecal water content (74.3% at baseline vs 77.8 and 76.9% after 7 and 14 days) and decreased fecal concentrations of ammonia (172.5 vs 427.4 μg/g wet feces), phenol (25.9 vs 49.2 μg/g wet feces), ethylphenol (0.0 vs 8.5 μg/g wet feces), indole (18.9 vs 34.4 μg/g wet feces), and skatole (1.3 vs 3.0 μg/g wet feces) after 14 days of supplementation.
The increased bifidobacteria populations in combination with the decreased clostridia populations and putrefactive compound concentrations suggest enhanced colonic health as a result of lactosucrose supplementation. It appears that the negative correlation between fecal bifidobacteria populations and indole concentrations observed by Hayakawa et al. (1990) in humans occurred in this study as well.
Similar to the experiment performed in dogs, Terada et al. (1993) fed 175 mg lactosucrose/day to cats for 14 days. As in the dog study, fecal and microbial characteristics were measured before lactosucrose administration, on day 7 and day 14 of lactosucrose administration, and 7 days after administration had ceased. Lactosucrose decreased fecal ammonia, indole, and ethylphenol concentrations after 7 and 14 days of supplementation.
Urinary ammonia concentrations were decreased (P<0.05) after 14 days, but not 7 days, of lactosucrose supplementation. Similar to the experiment performed with dogs, all fecal and urinary compounds measured in this study returned to concentrations similar to that of baseline 7 days after supplementation ceased. Lactosucrose supplementation decreased (P<0.05) fecal lecithinase-positive clostridia and enterobacteriaceae concentrations and increased (P<0.05) lactobacilli concentrations after 7 and 14 days. Fecal fusobacteria, lecithinase-negative clostridia and staphylococci concentrations were lower (P<0.05) after 7, but not 14, days of lactosucrose supplementation compared to baseline. Seven days after supplementation had ceased, all microbial populations were similar to baseline values.
In an attempt to ameliorate small intestinal bacterial overgrowth (SIBO), scFOS was given to IgA-deficient German Shepherd dogs (Willard et al., 1994). Given the health status of these dogs, the main concern and outcome variable of this experiment was the concentration of small intestinal microbes. Chicken-based kibble diets, containing either no scFOS (control) or 1% scFOS, were fed. All dogs (n=16) were fed the control diet for 3 months and then randomized into two groups.
Intestinal fluid and tissue were collected at, before, and 46 to 51 days after scFOS administration. It was reported that scFOS was beneficial, as scFOSsupplemented dogs had decreased (P<0.05) aerobic and anaerobic bacteria in tissue samples and aerobic bacteria in the duodenal/jejunal fluid samples. In control dogs, aerobic/facultative anaerobic microbes increased from baseline in intestinal fluid (5,713,600 vs 618,875 cells) and tissue (99,475 vs 11,875 cells) samples. In control dogs, anaerobic microbes also increased in intestinal fluid (378,150 vs 87,000 cells) and tissue (41,350 vs 33,500 cells) samples. However, in dogs fed scFOS, aerobic/ facultative anaerobic microbes decreased in intestinal fluid (1,388,750 vs 2,171,275 cells), but increased in tissue (16,450 vs 6,250 cells) samples.
In addition, scFOS-supplemented dogs had decreased anaerobic populations in tissue samples (2,600 vs 15,000 cells), but not in intestinal fluid samples. Results of this experiment suggest that scFOS supplementation may be helpful in the prevention or treatment of SIBO in dogs.
Diez et al. (1997) evaluated the effects of a blend of scFOS and sugar beet fiber (4:1) on nutrient digestibility and plasma metabolite concentrations in healthy Beagles. The basal diet (composed mainly of minced meat, flaked maize, maize oil) was compared with diets containing either 5 or 10% of the fermentable fiber blend. Wet feces excreted increased (P<0.05) linearly with increasing amounts of fermentable fiber in the diet (139, 180, and 222 g wet feces/day in dogs fed the basal, 5% fermentable fiber and 10% fermentable fiber diets, respectively). No differences were observed in dry weight of feces excreted/day among treatments.
However, % DM of feces decreased (P<0.05) linearly with increasing amount of fermentable fiber in the diet. These results can be explained by the capability of fermentable fibers, such as scFOS, to bind water and increase wet fecal weight without influencing dry fecal weight. Apparent CP digestibility decreased (P<0.05) with increasing amounts of the fiber blend (87.8, 86.3, and 83.8% digestibility for dogs fed the basal diet, the diet containing 5% fermentable fiber, and the diet containing 10% fermentable fiber, respectively). No differences in apparent DM, OM, fat, or ash digestibilities were observed in this experiment.
O’Carra (1997) performed two experiments examining MOS and its effects on immune function in dogs. In the first experiment, adult Beagles were randomized into four treatment groups. A control diet was compared with diets containing 1, 2, or 4 g MOS/kg diet. Blood samples were collected at baseline (pretreatment) and on days 15 and 31 of treatment for plasma protein and IgG measurements. No changes were observed among groups. In the second experiment, Border Collie pups were assigned to 1) a control diet (no MOS) or 2) a diet containing 2 g MOS/kg. After a 7-day adaptation period, a vaccination protocol was initiated. All dogs were vaccinated against parvovirus, leptospirosis, adenovirus, and distemper. Vaccine boosters were applied on day 21 for leptospirosis and on day 35 for parvovirus. Blood characteristics were measured over a 9-week period. No changes were observed in weight gain, lysozyme activity, plasma protein concentration, or plasma IgG concentration. Neutrophil activity was numerically increased in pups fed the diet containing MOS after vaccination [approximately 18 vs 14 Nitroblue tetrazolium (NBT)+ cells/slide]. However, due to low animal numbers (n = 3/group), statistical significance was not reached.
Three experiments by Russell (1998) examined the effects of soy or chicory as a natural source of inulin, and scFOS on bifidobacteria and clostridia populations, fecal pH, fecal moisture, fecal SCFA concentrations, and total tract nutrient digestibility. In the first experiment, three diets were used: 1) 12% soy (control); 2) 12% soy + 1% scFOS; and 3) 12% soy + 3% chicory. Chicory or scFOS did not influence apparent digestibility. Dogs fed scFOS and chicory had decreased (P<0.05) clostridia and increased (P<0.05) bifidobacteria populations compared to dogs fed the control diet.
Clostridia concentrations were lower in dogs fed 1% scFOS (1.3 × 1010 CFU/g) and 3% chicory (4.2 × 1010 CFU/g) compared to those consuming 12% soy (1.6 × 1011 CFU/g). In contrast, bifidobacteria concentrations increased in dogs fed 1% scFOS (8.2 ×1010 CFU/g) and 3% chicory (4.5 × 1010 CFU/g) compared with those fed 12% soy (1 ×109 CFU/g).
The inclusion of 3% chicory significantly increased fecal volume (data were not shown) indicating that a lower concentration should be examined. The second experiment compared a control diet vs diets containing 1.5, 3.0, or 5.0% chicory. All inclusion levels of chicory increased (P<0.05) bifidobacteria (1.27 × 106 CFU/g in dogs fed control vs 7.88 × 107, 1.23 × 108, and 4.83 × 107 CFU/ g in dogs fed 1.5, 3.0, and 5.0% chicory), but failed to change clostridia concentrations. No differences were observed in apparent DM, N, or GE digestibility. In the third experiment, 10 diets containing different concentrations of chicory and soy were examined. Chicory was added at 0, 0.5, 2.0, or 4.0% in combination with three soy levels (0, 6.0, or 12.0%). Chicory again increased (P<0.05) bifidobacteria populations (approximately 4.98, 8.53, 7.89, and 8.01 CFU log10/g with 0, 0.5, 2.0, and 4.0% chicory), independent of soy inclusion level. Inclusion rates greater than 2% chicory reduced digestibility and increased fecal volume.
From these studies, the author concluded that chicory was effective in increasing bifidobacteria populations and had the potential to decrease pathogenic strains such as clostridia. The author suggested a maximal inclusion rate of 2% chicory to attain a desirable fecal consistency and avoid decreases in digestibility and increases in fecal volume.
Sparkes et al. (1998) were the first to examine the effects of FOS (0.75% of diet) on fecal microbial concentrations in cats. After consuming a basal diet for 8 weeks, a fresh fecal sample was collected.
Cats were then fed an FOS-containing diet for 12 weeks. Another fecal sample was collected at this time. After cats were fed FOS, greater (P<0.05) lactobacilli (7.9 vs 5.7 log10 CFU/g) and bacteroides (9.5 vs 8.0 log10 CFU/g) concentrations and lower E. coli (6.3 vs 7.5 log10 CFU/g) concentrations were measured compared to the basal diet.
Fructooligosaccharide supplementation also tended to decrease C. perfringens (4.9 vs 6.6 log10 CFU/g) concentrations compared to the basal diet. The authors stated that they were unable to evaluate the effects of FOS on bifidobacteria populations because this microbe was only detectable in one of the 12 cats on the experiment, which may have been due to their housing and environmental conditions.
Because bifidobacteria concentrations in the cats on this experiment were much lower than are commonly found in humans and dogs, it is unknown whether the same beneficial effects of FOS supplementation observed in humans and dogs also apply to cats.
Using adult ileal cannulated dogs, Strickling et al. (2000) compared a control diet vs diets containing 5 g oligosaccharide/kg. Oligosaccharides tested included: OF, MOS, and XOS. A 4 × 7 incomplete Latin square design was used with each period lasting 21 days. Researchers measured ileal and total tract nutrient digestibilities, microbial populations, ileal pH, ammonia and SCFA concentrations, blood glucose and fecal consistency. Besides minor changes in SCFA concentrations, the only relevant finding was a decrease (P=0.07) in C. perfringens populations in dogs fed MOS (4.48 CFU log10/g) vs dogs fed XOS (5.16 CFU logs10/g) or OF (4.74 CFU log10/g). Because clostridia species do not possess mannose-specific fimbriae, another mechanism is likely. The lack of any significant findings may be due to the low dose of prebiotics consumed (only ~1.3 g/d) or the basal diet used in the study.
The basal diet contained 150 g soybean meal/kg, which was not a good choice for an experiment examining prebiotics. Using calculations of Zuo et al. (1996), the authors estimated that the diet contained approximately 10 g/kg of naturally occurring oligosaccharides, potentially masking any beneficial effects originating from prebiotic supplementation.
Diets differing in type and amount of fiber were fed to evaluate the effects on N and energy metabolism and microflora populations in female Beagles (Howard et al., 2000). The following fiber sources were compared: cellulose (6% of diet), beet pulp (6% of diet), scFOS (1.5% of diet), and a fiber blend consisting of beet pulp (6% of diet), gum talha (2% of diet), and scFOS (1.5% of diet). In this experiment, DM intake expressed as a percent of BW was reduced with diets containing fermentable fiber sources, especially with the scFOS diet. Apparent DM digestibility was greater (P<0.05) for dogs fed the scFOS diet than for those fed the diet containing cellulose. The authors hypothesized that the decreased food intake by dogs fed scFOS may be in response to SCFA, which are potent stimulators of peptide YY (Pappas et al., 1986).
Peptide YY has been shown to slow gastric emptying and intestinal transit (Allen et al., 1986), which may lead to the increased satiety and nutrient digestibility observed in this experiment. Total coliform populations from the duodenum, ileum, proximal colon, and distal colon were not different among treatments. Dogs supplemented with scFOS had greater (P<0.10) numbers of aerobic species in the distal colon, but not in the duodenum, ileum, or proximal colon, compared to dogs consuming the other treatments.
Patil et al. (2001) examined the effects of chicory supplementation on fecal microflora and odor components in cats. Cats were fed a control diet from day 0 to 15 and then fed diets containing chicory (control + 1, 2, or 3%) from day 16 to 30. Unlike Sparkes et al. (1998), high concentrations of bifidobacteria were measured in this experiment.
Although no differences (P>0.05) were observed in fecal C. perfringens concentrations, cats fed 2% chicory had greater (P<0.05) fecal bifidobacteria concentrations compared to control. Cats fed 3% chicory had increased fecal lactobacilli compared to control. Fecal bifidobacteria and lactobacilli concentrations were unaffected by diets containing 1% chicory. When cats were fed 2% chicory, fecal benzothiazole, methyl sulfide, methanethiol, dimethyl sulfide, dimethyl disulfide, and dimethyl trisulfide concentrations were lower (P<0.05) than when fed the control diet. Inclusion of chicory to the diet did not affect food intake, apparent DM and protein digestibilities, or fecal characteristics.
To determine the fermentability of several nondigestible oligosaccharides and fibers by colonic microbes, Vickers et al. (2001) performed an in vitro experiment using canine fecal inoculum. Substrates were fermented at 39oC for 6, 12, and 24 h. Short chain fatty acid (acetate, propionate, butyrate) and lactate concentrations were determined and used as a measure of fermentability. Blanks were used at each time point to account for SCFA originating from the fecal inoculum. It was unclear whether 0 h (baseline) blank and sample tubes were used for correcting values at 6, 12, and 24 h.
Mannanoligosaccharide fermentation produced moderate levels of total SCFA after 6 (0.49 mmol/ g of OM), 12 (1.45 mmol), and 24 h (2.40 mmol/g) of in vitro fermentation. In comparison, scFOS produced high levels of SCFA (0.97, 3.60, and 4.60 mmol/g). Beet pulp, a common fiber source in pet foods, produced similar SCFA concentrations (0.85, 0.92, and 2.60 mmol/g) to MOS after 6, 12, and 24 h of fermentation. Very low levels of lactate were produced as a result of MOS fermentation. The microbial species responsible for MOS breakdown were not determined in this experiment. In a similar experiment, Hussein and Healy (2001) performed an in vitro experiment using canine and feline fecal inoculum to determine the fermentability of MOS. Substrates were incubated at 39oC for 6, 12, 18, and 24 h. Although blanks were used at each of these times, blank and sample tubes at 0 h (baseline) were not used. Dry matter and OM disappearance, SCFA concentrations, and lactate concentrations were determined and used as indices of fermentability. No differences were observed in fermentability between dog and cat fecal inoculum. By examining DM and OM disappearance, it would appear that MOS was highly fermented. Dry matter disappearance after 6, 12, 18, and 24 h of in vitro fermentation was 54.3, 57.9, 60.7, and 61.3%, respectively. Organic matter disappearance was similar to that of DM (56.8, 60.7, 63.7, and 64.1% after 6, 12, 18, and 24 h of fermentation). Dry matter and OM disappearance do not always reflect microbial fermentation due to the disappearance of soluble carbohydrates present in the substrates and not retained during filtering. Although soluble carbohydrates are available for fermentation, gravimetric methods cannot determine the proportion used by the microbes as an energy source. Therefore, the measurement of DM and OM disappearance is not as accurate as the measurement of the fermentation products (i.e., SCFA and gas), which is a direct measurement of fermentation.
Blank and sample tubes at 0 h (baseline) can be used to correct DM and OM disappearance, but were not used in this experiment. Concentrations of total SCFA, acetate, and propionate increased linearly over time. Moderate levels of total SCFA (10.1, 26.8, 36.7, and 49.7 mM) were produced after 6, 12, 18, and 24 hr. In comparison to total SCFA, lactate concentrations were fairly high (7.7, 8.7, 7.6, and 5.9 mM), suggesting fermentation by a lactateproducing species (e.g., lactobacilli, bifidobacteria).
In agreement with the work of Vickers et al. (2001), these data suggest that MOS is moderately fermentable by canine and feline microflora. The lactate produced during fermentation suggests that lactate-producing species are able to utilize MOS, possibly by acting as a prebiotic for these species.
Zentek et al. (2001) used four dogs in a 4 × 4 Latin square design to determine the effects of MOS, transgalactosylated oligosaccharides, lactose, and lactulose on fecal characteristics, total tract digestibility, and concentrations of microbial endproducts in feces and urine. Dogs were fed an experimental diet containing 35% dry greaves, 35% rice, 20% soya oil, 5% fish meal, 3% cellulose, and 2% vitamin/mineral supplement. Carbohydrate supplements were administered at a rate of 1 g/kg BW/day. A total of 6 periods were used in this experiment (period 1 = basal diet to all dogs; periods 2 to 5 = carbohydrate supplements given in the 4 × 4 Latin square design; period 6 = basal diet to all dogs). Mannanoligosaccharide supplementation decreased fecal DM, fecal pH, fecal ammonia excretion, and apparent DM, OM, crude protein, and N-free extract digestibilities. By decreasing fecal pH and ammonia, MOS supplementation appeared to improve indices of colonic health.
However, a decrease in fecal DM may result in undesirable stool quality. In addition, the decreases observed in apparent nutrient digestibilities resulting from MOS supplementation would increase fecal quantity and the cost of feeding the animal. The dose of carbohydrate supplements fed in this experiment (1 g/kg BW/d) was very high. Smaller doses of MOS may not have such negative effects on nutrient digestibility.
A 4 × 4 Latin square design with 14-day periods was used by Swanson et al. (2002) to examine the effects of scFOS and (or) MOS on indices of gut health in ileal cannulated dogs. Dogs were dosed with one of the following treatments twice daily: 1) control (no scFOS or MOS); 2) 1 g scFOS; 3) 1 g MOS; or 4) 1 g scFOS + 1 g MOS. Blood, ileal, and fecal samples were collected during the last 4 days of each period to measure protein catabolite concentrations, microbial populations, immune characteristics, and nutrient digestibilities. Dogs supplemented with MOS had lower (P=0.05) fecal total aerobes and tended (P=0.13) to have greater fecal Lactobacillus concentrations compared to control. Dogs fed MOS also had greater (P<0.05) plasma lymphocytes (% of total white blood cells) and tended (P=0.13) to have greater serum IgA concentrations vs control. Ileal IgA concentrations were greater (P=0.05) in dogs supplemented with scFOS + MOS vs control. Dogs fed scFOS and scFOS + MOS had lower (P<0.05) fecal total indole and phenol concentrations. Finally, dogs fed MOS tended to have higher fecal pH (P=0.09) and lower ileal DM (P=0.15) and OM (P=0.15) digestibilities vs control. Short-chain fructooligosaccharide supplementation did not influence fecal microbial, SCFA, or ammonia concentrations in this experiment.
To follow up on results of the previous experiment, Swanson (unpublished data) performed another study to evaluate the effects of MOS + scFOS on immune function and ileal and fecal microbial populations in dogs. This experiment used a crossover design to evaluate the combination of MOS + scFOS (1 g MOS + 2 g scFOS twice daily) vs a placebo (1 g sucrose twice daily). In this experiment, supplementation of MOS + scFOS increased (P<0.05) fecal total aerobes, Bifidobacterium, and Lactobacillus concentrations. Interestingly, supplementation of MOS + scFOS also increased (P<0.05) ileal Lactobacillus concentrations compared to placebo. Similar to Swanson et al. (2002), dogs supplemented with MOS + scFOS tended to have a shift in plasma immune cells, having lower (P=0.08) blood neutrophils (% of total white blood cells) and greater (P=0.06) blood lymphocytes (% of total white blood cells) compared to dogs given the placebo.
Conclusions
There is strong evidence that prebiotics are nondigestible by mammalian enzymes, are a highly digestible energy source for the colonic microflora, positively influence microbial populations, and relieve the symptoms of constipation. However, their effects on fecal protein catabolite concentrations and cancer prevention have not been studied enough for any strong conclusions to be made. A few studies have reported beneficial effects of MOS on microbial populations and immune capacity. More research is needed to support the work reported in these initial experiments, determine the mechanisms involved, and identify any other beneficial effects of ingesting these oligosaccharides.
Experiments with fructans have focused on the prevention and treatment of constipation, manipulating colonic microbial species, determining the optimal dose, and examining effects on nutrient digestibility. Few in vitro and in vivo canine experiments have examined these effects using other oligosaccharides. It appears that prebiotics may play an important role in the development or maintenance of a healthy gut. However, researchers must take the next step and perform more molecular and mechanistic research and measure specific indices associated with a healthy gut.
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Authors: KELLY S. SWANSON1 and GEORGE C. FAHEY, JR.1, 2
Division of Nutritional Sciences1 and Department of Animal Sciences2, University of Illinois, Urbana, IL, USA
Author: KELLY S. SWANSON and GEORGE C. FAHEY, JR.- University of Illinois (Courtesy of Alltech Inc.)
Publication date: 02/27/2007
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