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© 2002 The American Society for Nutritional Sciences J. Nutr. 132:1682S-1684S, June 2002

Supplement: Waltham International Symposium

Intestinal Effects of Mannanoligosaccharides, Transgalactooligosaccharides, Lactose and Lactulose in Dogs

Jürgen Zentek2, Bettina Marquart and Tanja Pietrzak

Institute of Animal Nutrition, School of Veterinary Medicine Hannover, Hannover, Germany

2To whom correspondence should be addressed. E-mail: juergen.zentek{at}vu-wien.ac.at.

KEY WORDS: • dogs • mannanoligosaccharides • transgalactooligosaccharides • lactose • lactulose

EXPANDED ABSTRACT

Carbohydrates that are indigestible by mammalian enzymes can influence the composition and metabolic activity of the intestinal microflora and are therefore of interest for the formulation of pet food and specific veterinary diets. Mannanoligosaccharides are isolated from yeast cell walls (1). They are not hydrolyzed by digestive enzymes but by different lactobacilli and some bifidobacteria (2,3) and seem to be less fermentable by intestinal bacteria than are fructooligosaccharides (4–7). Galactooligosaccharides consist of ß-1,6-linked galactopyranosyl units and an {alpha}-glycosidic bonding to a terminal glycopyranosyl residue and have been shown to be fermentable by canine intestinal microflora (6). Transgalactooligosaccharides are produced by the ß-galactosidase from Aspergillus oryzae (8). Lactose can be regarded as a facultative fermentable carbohydrate in dogs. The activity of intestinal lactase decreases age dependently with concomitant compensatory fermentation by small intestinal and colonic bacteria (9). Lactulose is an isomeric form of lactose with one galactose molecule linked to fructose by ß-1,4-linkage. In vitro investigations demonstrated that lactulose is readily fermented by bifidobacteria and lactobacilli, but also by Clostridium perfringens, Escherichia coli and Bacteroides sp. (10–12). A decrease of colonic pH and blood ammonia concentrations in dogs was found after ingestion of lactulose (13,14).

In the present study mannanoligosaccharides, transgalactooligosaccharides, lactose and lactulose were added to a mixed diet for dogs and investigated for their effects on the fecal quality, nutrient and mineral digestibilities and on some products of intestinal microbial metabolism.


   MATERIALS AND METHODS
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 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 LITERATURE CITED
 
Animals

Four adult female beagles with an average body weight of 11.7 ± 2.2 kg. Care and treatment of the animals was approved by governmental commission according to the procedures of the animals’ protection law. The dogs were vaccinated and dewormed as usual and housed individually.

Diet

The basal diet (17 g/kg BW/d) was fed without added carbohydrates in the control periods I and II. Mannanoligosaccharides (MOS, Bio Mos; Alltech, Bad Segeberg, Germany), transgalactooligosaccharides (TGOS, Lactifit; Borculo Whey Products, Borculo, The Netherlands), lactose (Variolac 99; Biolac GmbH, Harbarnsen, Germany) or lactulose (Lactuverlan; Verla-Pharm, Tutzing, Germany) were dosed individually for each dog (1 g/kg BW/d) and mixed with the basal diet during four supplementation periods. The experiment was designed as a 4 x 4 Latin square and the dogs received the basal diet without additives before and after the four diets were supplemented with the fermentable carbohydrates. The adaptation periods lasted at least 10 d before collection of the samples.

Variables

The apparent digestibility of crude nutrients [methods in Naumann and Bassler (15) and macrominerals, by wet ashing in a mixture of perchloric and nitric acid, atomic absorption spectrophotometry for calcium and magnesium (16), flame photometry for sodium and potassium (17), vanadate molybdate method for phosphorus (18)] was measured after 5-d collection periods in a metabolism cage. Additional variables were a daily scoring of fecal consistency, determination of fecal dry matter (oven drying to weight constancy) and of unbound water by centrifugation (weight of fluid after centrifugation of 2 g of feces for 30 min, 30,000 x g; Sorvall Superspeed RC2-B, DuPont, Bad Homburg, Germany), and of pH (Knick-pH-Meter; Knick, Berlin, Germany). Dietary effects on the metabolism of the intestinal microflora were assessed by the fecal concentrations of ammonia (ammonia-Electrode, Model IS 570 NH3; Philips, Kassel, Germany) and volatile fatty acids (VFA) (capillary chromatograph PU 4550; Pye Unicam, Offenbach, Germany; glass column, 2 m length x 2 mm ID, packed with GP 10%/SP 1000/1% H3PO4 on 100/120 Chromosorb WAW; Supelco, Deisenhofen, Germany) and urinary nitrogen, indican (19) and urea excretion (Urea Kit, bio Merieux, Nürtingen, Germany). Fecal suspensions (1:10 in prereduced physiological saline) were incubated under nitrogen atmosphere for 24 h with measurement of total gas formation and production of VFA.

Statistics

Data were processed by EXCEL 5.0 and SAS 6.04 (20). ANOVA and Tukey test were used for comparison of the Latin square with the supplemented diets. Comparison of supplemented and basal diets I and II was done by t-test. Probability values of <0.05 were taken as significant.


   RESULTS AND DISCUSSION
TOP
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
LITERATURE CITED
 
The apparent digestibilities of dry matter, crude protein and N-free extracts were lower with the mannanoligosaccharides (Table 1) than those with the other dietary periods.


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  		TABLE 1 Apparent digestibilities (means ± SD) of dry matter and crude nutrients (% of intake; n = 4)1

 
Apparent absorption rates of calcium (5–15%), phosphorus (31–46%), magnesium (9–29%), sodium (93–97%) and potassium (90–95%) were not influenced by the type of diet. Fecal consistency tended to get looser during the lactulose period than during the basal period, whereas the other carbohydrates had no negative effects on stool quality. The lowest unbound water (5.5%) was found with mannanoligosaccharides (Table 2), accompanied by a lower fecal pH (6.6). Fecal ammonia concentration and excretion were higher with basal diet I than with basal diet II. The ammonia concentrations were lower after the addition of mannanoligosaccharides than that in basal diet I and the lactulose period.


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  		TABLE 2 Fecal consistency, dry matter, unbound water, pH and ammonia (means ± SD; n = 4)1

 
The fecal VFA concentrations ranged from 139 to 209 mmol/L with no differences attributed to diet (data not shown). Dietary alterations did not influence the renal nitrogen (45–60 mmol/kg BW/d), urea (18–27 mmol/kg) or indican (10–16 µmol/kg) excretion. Ammonia yield from anaerobic in vitro incubation of fecal suspensions for 24 h in dogs fed lactulose was higher than that when either basal diet was fed. There was a similar trend when the other three supplemented diets were fed (Table 3).


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  		TABLE 3 pH, ammonia, gas volume and volatile fatty acids after 24-h incubation of fecal suspensions (means ± SD; n = 4)1

 
Total gas production was lowest in the initial control period (basal diet I) compared with that of the other experimental diets. The concentrations of VFA (Table 3), mainly of acetic acid, increased during the incubation, whereas the proportion of propionic acid and n-butyric acid decreased. There were no obvious dietary influences on in vitro fermentation.

In conclusion, lactose, lactulose or transgalactooligosaccharides did not alter the measures of microbial metabolism, compared to those of the control periods. Higher intakes might have induced clearer changes, but according to our own preliminary experiments a dosage of 2 g lactulose/kg BW/d induced diarrhea, which shows comparatively narrow limits between tolerance and intolerance in dogs. Mannanoligosaccharides resulted in a lower fecal pH, ammonia excretion and apparent digestibilities of crude protein, nitrogen-free extracts and dry matter, compared to those of the control periods and the other carbohydrates. The percentage of total fecal water increased and the unbound water decreased substantially during this period, which can be interpreted as a change in the physical properties of the intestinal chyme. This higher water binding could have influenced the solubility of nutrients, which might explain the lower digestibilities and also the activity of the intestinal microflora. Further studies are warranted to confirm these effects and the underlying mechanisms.


   FOOTNOTES
 
1 Presented as part of the Waltham International Symposium: Pet Nutrition Coming of Age held in Vancouver, Canada, August 6–7, 2001. This symposium and the publication of symposium proceedings were sponsored by the Waltham Centre for Pet Nutrition. Guest editors for this supplement were James G. Morris, University of California, Davis, Ivan H. Burger, consultant to Mars UK Limited, Carl L. Keen, University of California, Davis, and D’Ann Finley, University of California, Davis. Back

3 Abbreviations used: BW, body weight; IU, international units; MOS, basal diet with mannanoligosaccharides; TGOS, basal diet with transgalactooligosaccharides. Back

4 Ingredients: dry greaves (35%), pressure-cooked rice (35%), fish meal (5%), soya oil (20%), cellulose 3%, and vitamin and mineral supplement (2%; Vitakalk: 21% calcium, 8% phosphorus, 6% sodium, 1% magnesium; per kg: 500,000 IU vitamin A, 40,000 IU vitamin D3, 1000 mg vitamin E, 700 mg copper; Marienfelde GmbH, Roth, Germany). Composition of the mixed diet (g/kg): dry matter, 945; crude ash, 39.8; crude protein, 366; crude fat, 244; crude fiber, 49.5; calcium, 6.76; magnesium, 0.53; phosphorus, 5.06; sodium, 4.23; potassium, 3.06; chloride, 5.31. Back


   LITERATURE CITED
TOP
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 LITERATURE CITED
 

1. Newman, K. (1994) Lyons, T. P. Jacques, K. A. eds. Mannan-oligosaccharides: natural polymers with significant impact on the gastrointestinal microflora and the immune system 1994:167-174 Nottingham University Press Nottingham, UK .

2. Lyons, T. P. (1994) Biotechnology in the feed industry: 1994 and beyond. A panorama of techniques, processes and products to address animal production problems today and tomorrow.. Lyons, T. P. eds. Biotechnology in Feed Industry 1994:1-48 Nottingham University Press Nottingham, UK .

3. Miles, R. D. (1993) Manipulation of the microflora of the gastrointestinal tract: natural ways to prevent colonization by pathogens. Lyons, T. P. eds. Biotechnology in Feed Industry 1993:133-150 Nottingham University Press Nottingham, UK .

4. Flickinger, E. A., Wolf, B. W., Garleb, K. A., Chow, J., Leyer, G. J., Johns, P. W. & Fahey, G. C., Jr (2000) Glucose-based oligosaccharides exhibit different in vitro fermentation patterns and affect in vivo apparent nutrient digestibility and microbial populations in dogs. J. Nutr. 130:1267-1273.[Abstract/Free Full Text]

5. Ohtsuka, R., Iwasa, A., Iwahashi, M., Moriyama, H., Jeong, E. S., Hayashi, T., Fujii, T., Okamoto, Y., Teshima, H. & Sakurai, T. (1995) Effects of administration of galactooligosaccharides on faecal character in dogs and cats. Bull. Fac. Agric. Tottori Univ. 48:145-149.

6. Sumihara, Y. (1987) The function of galactooligosaccharides and their application for food. Food Chem 6:87-94.

7. Vickers, R. J., Sunvold, G. D., Kelley, R. L. & Reinhart, G. A. (2001) Comparison of fermentation of selected fructooligosaccharides and other fiber substrates by canine colonic microflora. Am. J. Vet. Res. 62:609-615.[Medline]

8. Matsumoto, K., Kobayashi, Y., Ueyama, S., Watanabe, T., Tanaka, R., Kan, T., Kuroda, A. & Sumihara, Y. (1993) Galactooligosaccharides. Nakakuki, T. eds. Oligosaccharides: Production, Properties and Applications 3:90-106 Gordon and Breach Science Publishers Tokyo, Japan .

9. Meyer, H. (1992) Laktosefütterung bei Fleischfressern. Wien. Tierärztl. Msschr. 79:236-241.

10. Hidaka, H., Eida, T., Takizawa, T., Tokunaga, T. & Tashiro, Y. (1986) Effects of fructooligosaccharides on intestinal flora and human health. Bifidobacteria Microflora 5:37-50.

11. Mitsuoka, T., Hidaka, A. & Eida, T. (1987) Effect of fructo-oligosaccharides on intestinal microflora. Nahrung 31:427-436.[Medline]

12. Smart, J. B., Pillidge, C. J. & Garman, J. H. (1993) Growth of lactic acid bacteria and bifidobacteria on lactose and lactose-related mono-, di- and trisaccharides and correlation with distribution of beta-galactosidase and phospho-beta-galactosidase. J. Dairy Res. 60:557-568.

13. Bircher, J., Haemmerli, U. P., Trabert, E., Largiader, F. & Mocetti, T. (1971) The mechanism of action of lactulose in portal-systemic encephalopathy. Non-ionic diffusion of ammonia in the canine colon. Rev. Eur. Etud. Clin. Biol. 16:352-357.[Medline]

14. Matsuoka, Y., Uruno, T., Yamada, M., Mizukami, A., Kanetake, Y., Sunagane, N. & Kubota, K. (1990) Effects of lactulose on blood ammonia levels in beagles with end-to-side portacaval shunt. Nippon Yakurigaku Zasshi 96:97-101.[Medline]

15. Naumann, K. & Bassler, R. (1993) Die chemische Untersuchung von Futtermitteln 1993 Verlag Neumann Darmstadt, Germany .

16. Slavin, W. (1968) Atomic absorption spectroscopy. Chem. Anal. 25:87-90.

17. Schuhknecht, A. & Schinkel, H. (1963) Universalvorschrift für die Bestimmung von Natrium, Kalium und Lithium nebeneinander. Z. Anal. Chem. 194:176-183.

18. Gericke, S. & Kurmies, B. (1952) Die kolorimetrische Phosphorbestimmung mit Ammonium-Vanadat-Molybdat und ihre Anwendung in der Pflanzenanalyse. Z. Pflanz. Ernährg. Düng. Bdkde. 59:235-247.

19. Curzon, G. & Walsh, J. (1967) A method for determination of urinary indoxylsulphate (indican). Clin. Chim. Acta 7:657-663.

20. SAS Institute (1991) SAS/STAT User’s guide release 6.04 ed. 1991 SAS Institute Inc. Cary, NC .




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