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(Journal of Nutrition. 1999;129:1454S-1456S.)
© 1999 The American Society for Nutritional Sciences


Supplement

Petfood Applications of Inulin and Oligofructose1

Hussein S. Hussein, Elizabeth A. Flickinger* and George C. Fahey, Jr.*,2

School of Veterinary Medicine, University of Nevada-Reno, Reno, NV 89557 and * Department of Animal Sciences and Division of Nutritional Sciences, University of Illinois, Urbana, IL 61801

2To whom correspondence should be addressed.


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 Origin and health hazards...
 Dietary manipulation of colonic...
 Evidence from canine and...
 Oligofructose in petfood...
 SUMMARY
 REFERENCES
 
Published data on intestinal microbiota of dogs and cats are limited but suggest the presence of a complex and diverse colonic bacterial population (34 genera including 129 species) the majority of which are anaerobes. During the colonic fermentation of endogenous and undigested amino acids, several putrefactive compounds (i.e., ammonia, aliphatic amines, indoles, phenols and volatile sulfur-containing compounds) are produced and are responsible for the malodor of dog and cat feces. These fecal odor components also have been implicated as causes of colorectal cancer; therefore, dietary manipulation of gut microbiota towards a potentially more remedial community (Bifidobacterium and Lactobacillus) is gaining more attention. The health benefits derived from dietary supplementation of prebiotics (e.g., oligofructose and inulin) have been documented in humans. However, little is known of a potentially similar role in companion animals. Feeding another prebiotic (i.e., lactosucrose) to dogs or cats is reported to increase the numbers of bifidobacteria and decrease the numbers of pathogens and the concentration of fecal odor components. In our laboratory, oligofructose supplementation numerically decreased the concentrations of ammonia and amines and increased the numbers of bifidobacteria in dog feces.


KEY WORDS: • oligofructose • inulin • dogs • cats • petfood


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 Origin and health hazards...
 Dietary manipulation of colonic...
 Evidence from canine and...
 Oligofructose in petfood...
 SUMMARY
 REFERENCES
 
Unlike the case for other monogastric animals (e.g., rats, mice, and pigs) or humans, published data on intestinal microbiota of dogs or cats are limited (Balish et al. 1977Citation , Clapper 1970Citation , Davis et al. 1977Citation ) but suggest the presence of a complex colonic bacterial population. This microbial population was found to be diverse (34 genera including 129 species; Balish et al. 1977Citation ), to contain large numbers of anaerobic bacteria (i.e., 1010 organisms/g dry feces; Davis et al. 1977Citation ) and to promote significant colonic fermentation (Banta et al. 1979Citation ). These colonic bacterial species not only contribute to normal physiologic function but also participate significantly in the causation or prevention of various diseases by biotransforming a variety of ingested or endogenous compounds to beneficial or harmful derivatives. This biotransformation was suggested to influence drug efficacy, toxicity, carcinogenesis and aging (Mitsuoka 1990Citation ). There is evidence that the composition of colonic microbiota can be altered by dietary ingredients. For example, source and level of dietary protein were found to influence the occurrence of pathogens (e.g., Clostridium perfringens) in dog feces (Amtsberg et al. 1980Citation ). Therefore, the potential exists for dietary manipulation of colonic fermentation by changing the composition of microbiota in the colon toward a potentially more remedial community.


    Origin and health hazards of fecal odor components
 TOP
 ABSTRACT
 INTRODUCTION
 Origin and health hazards...
 Dietary manipulation of colonic...
 Evidence from canine and...
 Oligofructose in petfood...
 SUMMARY
 REFERENCES
 
During the colonic fermentation of endogenous and undigested amino acids, several putrefactive compounds are produced (Bakke 1969a and 1969bCitation Citation , Tabor and Tabor 1985Citation , Williams 1959Citation ) and are responsible for the malodor of the feces. These compounds include ammonia, aliphatic amines (agmatine, cadaverine, phenylethylamine, putrescine and tyramine), branched-chain fatty acids (isobutyrate and isovalerate), indoles (indole, 3-methylindole [skatole], 2-methylindole, 2,3-methylindole and 2,5-methylindole), phenols (phenol, p-cresol and 4-ethylphenol), and volatile sulfur-containing compounds (dimethyl disulfide, diethyl disulfide, di-n-propyl disulfide and di-n-butyl disulfide) (MacFarlane and Cummings 1991Citation ). These compounds are produced from amino acids by deamination (e.g., ammonia), deamination-decarboxylation (e.g., short-chain fatty acids) or decarboxylation (e.g., aliphatic amines) processes.

Many of these putrefactive compounds have adverse effects on colonic health. Some of these fecal odor components have been implicated as causes of colorectal cancer (Johnson 1977Citation , Silverman and Andrews 1977Citation ). Ammonia may promote tumorigenesis (Lin and Visek 1991Citation , Visek 1978Citation ). Phenol and p-cresol have been implicated in colonic cancer (Bingham 1988Citation ) and may exacerbate diseases such as ulcerative colitis (Ramakrishna et al. 1991Citation ). Despite the importance of the problem, no significant control measures have been taken because of the lack of knowledge of the relationship between diet and fecal odor components.


    Dietary manipulation of colonic fermentation
 TOP
 ABSTRACT
 INTRODUCTION
 Origin and health hazards...
 Dietary manipulation of colonic...
 Evidence from canine and...
 Oligofructose in petfood...
 SUMMARY
 REFERENCES
 
Because the gut microbiota can play a major role in host health, there is currently some interest in manipulation of the composition of the gut microbiota towards a potentially more remedial community. Prebiotics are nondigestible food ingredients that beneficially affect the host by selectively stimulating the growth and/or activity of one or a limited number of bacterial species already resident in the colon; the desired outcome is to improve host health (Gibson and Roberfroid 1995Citation ). Intake of prebiotics can significantly modulate the colonic microbiota by increasing the number of specific bacteria and thus changing the composition of the microbiota. In the early 1990s, Terada et al. (1992 and 1993)Citation Citation reported in the dog and cat, respectively, that feeding lactosucrose, a prebiotic, increased bifidobacteria while decreasing pathogenic organisms (i.e., C. perfringens).

Nondigestible oligosaccharides in general, and oligofructose in particular, are prebiotics. They have been shown to stimulate the growth of endogenous bifidobacteria, which, after a short feeding period, become predominant in human feces (Gibson and Roberfroid 1995Citation ). Oligofructose, for example, stimulated the growth of bifidobacteria at the expense of others that are pathogens or less desirable (i.e., bacteroides, clostridia and coliforms); these were reduced in number to very low levels (Wang and Gibson 1993Citation ). Bifidobacteria (a major group of saccharolytic bacteria) constitute up to 25% of the total bacterial population in the gut of adult humans (Kawase et al. 1981Citation ), and their positive biological activities have received much attention (Tamura 1983Citation ).


    Evidence from canine and feline species
 TOP
 ABSTRACT
 INTRODUCTION
 Origin and health hazards...
 Dietary manipulation of colonic...
 Evidence from canine and...
 Oligofructose in petfood...
 SUMMARY
 REFERENCES
 
Few published reports exist concerning the effects of oligofructose and inulin on canine or feline colonic bacterial populations. Willard et al. (1994)Citation reported on supplementation of dog diets with 1% oligofructose. This research dealt with small intestinal bacterial overgrowth, and the results indicated positive health responses to such supplementation. After an adaptation period (46–51 d), oligofructose decreased (P < 0.05) both aerobic and facultative anaerobic bacterial numbers in fluid from both the duodenum and proximal part of the jejunum, as well as in the duodenal mucosa.

In a study reviewed by Buddington and Sunvold (1998)Citation , adult beagles were fed diets containing cellulose or beet pulp plus oligofructose as the fiber source. Both groups had similar fecal concentrations of total anaerobes and total aerobes, but dogs fed oligofructose tended to have fewer Enterobacteriaceae and clostridia and greater numbers of lactobacilli. In addition, dogs fed oligofructose had longer and heavier small intestines, with more mucosa and greater absorptive surface area.

In a study reviewed by Gruffydd et al. (1998)Citation , cats fed diets containing 0 or 0.75% oligofructose had increased (P < 0.05) fecal concentrations of lactobacilli (7.9 x 107 vs. 5.0 x 105). The cats fed oligofructose also had decreased concentrations of C. perfringens (7.9 x 104 vs. 4.0 x 106) (P < 0.10) and Escherichia coli (3.2 x 107 vs. 2.0 x 106) (P < 0.05) compared with the controls. This may indicate that oligofructose supplementation elicits a more remedial colonic microbial population.

In a recent study from our laboratory (E. A. Flickinger, A. R. Patil, H. S. Hussein and G. C. Fahey, Jr., unpublished data), 16 adult male beagles were fed a corn-based diet without or with 0.3, 0.6 or 0.9% supplemental oligofructose for 18 d. Dietary supplementation increased (P < 0.05) fecal short-chain fatty acid concentrations. Fecal ammonia concentrations were numerically lower (P = 0.30) in the oligofructose-fed groups than in the control group (2.20 vs. 4.07 mg/g dry feces). Fecal concentrations of putrescine and cadaverine were numerically lower (P = 0.28) in all of the oligofructose-supplemented groups (putrescine = 0.54, 0.29, 0.30 and 0.20 and cadaverine = 0.20, 0.16, 0.06 and 0 mg/g dry feces for dogs fed 0, 0.3, 0.6 or 0.9% oligofructose, respectively). The dogs that were fed the highest level of oligofructose tended to have lower (P = 0.07) concentrations of total phenols (0.61 vs. 0.80 mg/g dry feces) and higher (P = 0.06) numbers of bifidobacteria (6.3 x 109 vs. 2.5 x 109 colony-forming units) in their feces compared with the control group.


    Oligofructose in petfood ingredients
 TOP
 ABSTRACT
 INTRODUCTION
 Origin and health hazards...
 Dietary manipulation of colonic...
 Evidence from canine and...
 Oligofructose in petfood...
 SUMMARY
 REFERENCES
 
The practice of dietary supplementation of oligofructose, inulin or other oligosaccharides will depend on the contribution of natural prebiotics in petfood ingredients. Because of the lack of a database on concentrations of oligofructose as well as other oligosaccharides in petfood ingredients, 25 common petfood ingredients were selected and analyzed for oligofructose concentration (Hussein et al. 1998Citation ). In this study, the concentrations of three major subcomponents of oligofructose (i.e., 1-kestose [GF2], nystose [GF3] and 1F-ß-fructofuranosylnystose [GF4]) in these ingredients were assayed. No oligofructose was detected in corn, corn distiller's solubles, hominy, milo, brown rice, white rice, brewer's rice, rice hulls, seaweed or soybean meal. On a dry matter basis, wheat co-products (bran, germ and middlings) contained the highest concentrations (0.40, 0.47 and 0.51%, respectively) of total oligofructose, followed by peanut hulls (0.24%), alfalfa meal (0.22%), barley (0.19%) and wheat (0.14%). The remaining ingredients (e.g., corn gluten meal, oats, rice bran, beet pulp, soybean hulls and canola meal) contained very low concentrations (<0.04%). This database should be expanded to include other petfood ingredients; in addition, the analyses should be expanded to include other oligosaccharide groups.


    SUMMARY
 TOP
 ABSTRACT
 INTRODUCTION
 Origin and health hazards...
 Dietary manipulation of colonic...
 Evidence from canine and...
 Oligofructose in petfood...
 SUMMARY
 REFERENCES
 
It is important to establish accurate relationships between dietary ingredients (especially protein) and the microbial ecology of the dog and cat colon. Such relationships should provide guidelines for formulation of diets that contain the optimal levels and sources of proteins to meet amino acid requirements and contain prebiotics that support dog and cat health. These guidelines would only result from future in vivo experiments that focus on examining dietary supplementation of oligofructose, inulin and other oligosaccharides under different dietary and physiologic conditions.


    FOOTNOTES
 
1 Presented at the conference Nutritional and Health Benefits of Inulin and Oligofructose held May 18–19, 1998 in Bethesda, MD. This symposium was supported in part by educational grants from the National Institutes of Health Office of Dietary Supplements, the U.S. Department of Agriculture and Orafti Technical Service. Published as a supplement to The Journal of Nutrition. Guest editors for the symposium publication were John A. Milner, The Pennsylvania State University, and Marcel Roberfroid, Louvain University, Brussels, Belgium. Back


    REFERENCES
 TOP
 ABSTRACT
 INTRODUCTION
 Origin and health hazards...
 Dietary manipulation of colonic...
 Evidence from canine and...
 Oligofructose in petfood...
 SUMMARY
 REFERENCES
 

1. Amtsberg G., Drochner W., Meyer H. Influence of food composition on the intestinal flora of the dog. Anderson R. S. eds. Nutrition of the Dog and Cat 1980:181-188 Pergamon Press Oxford, U.K.

2. Bakke O. M. Urinary simple phenols in rats fed purified and nonpurified diet. J. Nutr. 1969;98:209-216

3. Bakke O. M. Urinary simple phenols in rats fed diets containing different amounts of casein and 10% tyrosine. J. Nutr. 1969;98:217-221

4. Balish E., Cleven D., Brown J., Yale C. E. Nose, throat, and fecal flora of beagle dogs housed in "locked" or "open" environments. Appl. Environ. Microbiol. 1977;34:207-221[Abstract/Free Full Text]

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13. Hussein H. S., Campbell J. M., Bauer L. L., Fahey G. C., Jr, Hogarth A.J.C.L., Wolf B. W., Hunter D. E. Selected fructooligosaccharide composition of petfood ingredients. J. Nutr. 1998;128:2803S-2805S[Free Full Text]

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