Skip to main content Accessibility help
×
Home

Effects of prebiotic inulin-type fructans on blood metabolite and hormone concentrations and faecal microbiota and metabolites in overweight dogs

  • Celeste Alexander (a1), Tzu-Wen L. Cross (a1), Saravanan Devendran (a2), Franka Neumer (a3), Stephan Theis (a3), Jason M. Ridlon (a1) (a2), Jan S. Suchodolski (a4), Maria R. C. de Godoy (a1) (a2) and Kelly S. Swanson (a1) (a2)...

Abstract

Because obesity is associated with many co-morbidities, including diabetes mellitus, this study evaluated the second-meal effect of a commercial prebiotic, inulin-type fructans, and the effects of the prebiotic on faecal microbiota, metabolites and bile acids (BA). Nine overweight beagles were used in a replicated 3×3 Latin square design to test a non-prebiotic control (cellulose) against a low (equivalent to 0·5 % diet) and high dose (equivalent to 1·0 % diet) of prebiotic over 14-d treatments. All dogs were fed the same diet twice daily, with treatments provided orally via gelatin capsules before meals. On days 13 or 14 of each period, fresh faecal samples were collected, dogs were fed at 08.00 hours and then challenged with 1 g/kg body weight of maltodextrin in place of the 16.00 hours meal. Repeated blood samples were analysed for glucose and hormone concentrations to determine postprandial incremental AUC (IAUC) data. Baseline glucose, insulin and active glucagon-like peptide-1 levels were similar between all groups (P>0·10). Glucose and insulin IAUC after glucose challenge appeared lower following the high dose, but did not reach statistical relevance. Prebiotic intervention resulted in an increase in relative abundance of some Firmicutes and a decrease in the relative abundance of some Proteobacteria. Individual and total faecal SCFA were significantly increased (P<0·05) following prebiotic supplementation. Total concentration of excreted faecal BA tended to increase in dogs fed the prebiotic (P=0·06). Our results indicate that higher doses of inulin-type prebiotics may serve as modulators of gut microbiota, metabolites and BA pool in overweight dogs.

Copyright

Corresponding author

*Corresponding author: K. S. Swanson, fax +1 217 333 5044, email ksswanso@illinois.edu

References

Hide All
1. Kaneko, JJ, Mattheeuws, D, Rottiers, RP, et al. (1977) Glucose tolerance and insulin response in diabetes mellitus of dogs. J Small Anim Pract 18, 8594.
2. Chikamune, T, Katamoto, H, Ohashi, F, et al. (1995) Serum lipid and lipoprotein concentrations in obese dogs. J Vet Med Sci 57, 595598.
3. Chandler, M, Cunningham, S, Lund, EM, et al. (2017) Obesity and associated comorbidities in people and companion animals: a one health perspective. J Comp Pathol 156, 296309.
4. Massimino, SP, McBurney, MI, Field, CJ, et al. (1998) Fermentable dietary fiber increases GLP-1 secretion and improves glucose homeostasis despite increased intestinal glucose transport capacity in healthy dogs. J Nutr 128, 17861793.
5. Chandalia, M, Garg, A, Lutjohann, D, et al. (2000) Beneficial effects of high dietary fiber intake in patients with type 2 diabetes mellitus. N Engl J Med 342, 13921398.
6. Respondek, F, Swanson, KS, Belsito, KR, et al. (2008) Short-chain fructooligosaccharides influence insulin sensitivity and gene expression of fat tissue in obese dogs. J Nutr 138, 17121718.
7. Weickert, M, Möhlig, M, Schöfl, C, et al. (2006) Cereal fiber improves whole-body insulin. Diabetes Care 29, 773780.
8. Reimer, R & McBurney, M (1996) Dietary fiber modulates intestinal proglucagon messenger ribonucleic acid and postprandial secretion of glucagon-like peptide-l and insulin in rats. Endocrinology 137, 39483956.
9. Delzenne, NM & Cani, PD (2005) A place for dietary fibre in the management of the metabolic syndrome. Curr Opin Clin Nutr Metab Care 8, 636640.
10. Staub, H (1921) Untersuchungen uber den Zuckerstoffwechsel des Munchen (Studies on the sugar metabolism of the munich). Z Klin Med 91, 4448.
11. Traugott, K (1922) Über das Verhalten des Blutzucherspiegels bei wiederholter und verschiedener Art enteraler Zuckerzufuhr und dessen Bedeutung für die Leberfunktion (On the behaviour of blood sugar levels with repeated and various types of enteral sugar intake and its importance for liver function). Klin Woch 1, 892894.
12. Deng, P, Beloshapka, AN, Vester Boler, BM, et al. (2013) Dietary fibre fermentability but not viscosity elicited the ‘second-meal effect’ in healthy adult dogs. Br J Nutr 110, 960968.
13. Brighenti, F, Benini, L, Del Rio, D, et al. (2006) Colonic fermentation of indigestible carbohydrates contributes to the second-meal effect. Am J Clin Nutr 83, 817822.
14. Nilsson, AC, Ostman, EM, Holst, JJ, et al. (2008) Including indigestible carbohydrates in the evening meal of healthy subjects improves glucose tolerance, lowers inflammatory markers, and increases satiety after a subsequent standardized breakfast. J Nutr 138, 732739.
15. Priebe, MG, Wang, H, Weening, D, et al. (2010) Factors related to colonic fermentation of nondigestible carbohydrates of a previous evening meal increase tissue glucose uptake and moderate glucose-associated inflammation. Am J Clin Nutr 91, 9097.
16. de Carvalho, CM, de Paula, TP, Viana, LV, et al. (2017) Plasma glucose and insulin responses after consumption of breakfasts with different sources of soluble fiber in type 2 diabetes patients: a randomized crossover clinical trial. Am J Clin Nutr 106, 12381245.
17. Ropert, A, Cherbut, C, Roze, C, et al. (1996) Colonic fermentation and proximal gastric tone in humans. Gastroenterology 111, 289296.
18. Robertson, MD (2007) Metabolic cross talk between the colon and the periphery: implications for insulin sensitivity. Proc Nutr Soc 66, 351361.
19. Anderson, JW & Bridges, SR (1984) Short-chain fatty acid fermentation products of plant fiber affect glucose metabolism of isolated rat hepatocytes. Proc Soc Exp Biol Med 177, 372376.
20. Middelbos, IS, Boler, BMV, Qu, A, et al. (2010) Phylogenetic characterization of fecal microbial communities of dogs fed diets with or without supplemental dietary fiber using 454 pyrosequencing. PLoS ONE 5, e9768.
21. Beloshapka, AN, Dowd, SE, Suchodolski, JS, et al. (2013) Fecal microbial communities of healthy adult dogs fed raw meat-based diets with or without inulin or yeast cell wall extracts as assessed by 454 pyrosequencing. FEMS Microbiol Ecol 84, 532541.
22. Garcia-Mazcorro, JF, Barcenas-Walls, JR, Suchodolski, JS, et al. (2017) Molecular assessment of the fecal microbiota in healthy cats and dogs before and during supplementation with fructo-oligosaccharides (FOS) and inulin using high-throughput 454-pyrosequencing. PeerJ 5, e3184.
23. Holscher, HD, Bauer, LL, Gourineni, V, et al. (2015) Agave inulin supplementation affects the fecal microbiota of healthy adults participating in a randomized, double-blind, placebo-controlled, crossover trial. J Nutr 145, 20252032.
24. Holscher, HD, Caporaso, JG, Hooda, S, et al. (2015) Fiber supplementation influences phylogenetic structure and functional capacity of the human intestinal microbiome: follow-up of a randomized controlled trial. Am J Clin Nutr 101, 5564.
25. Dominianni, C, Sinha, R, Goedert, JJ, et al. (2015) Sex, body mass index, and dietary fiber intake influence the human gut microbiome. PLOS ONE 10, e0124599.
26. Ridlon, JM, Harris, SC, Bhowmik, S, et al. (2016) Consequences of bile salt biotransformations by intestinal bacteria. Gut Microbes 7, 2239.
27. Joyce, SA & Gahan, CGM (2016) Bile acid modifications at the microbe-host interface: potential for nutraceutical and pharmaceutical interventions in host health. Annu Rev Food Sci Technol 7, 313333.
28. National Research Council (2006) Nutrient Requirements of Dogs and Cats. Washington, DC: National Research Council of the National Academies.
29. Barry, KA, Hernot, DC, Middelbos, IS, et al. (2009) Low-level fructan supplementation of dogs enhances nutrient digestion and modifies stool metabolite concentrations, but does not alter fecal microbiota populations. J Anim Sci 87, 32443252.
30. Apanavicius, CJ, Powell, KL, Vester, BM, et al. (2007) Fructan supplementation and infection affect food intake, fever, and epithelial sloughing from Salmonella challenge in weanling puppies. J Nutr 137, 19231930.
31. Association of Official Analytical Chemists (2006) Official Methods of Analysis. Arlington, VA: AOAC.
32. American Association of Cereal Chemists (1983) Approved Methods. St Paul, MN: AACC.
33. Budde, EF (1952) The determination of fat in baked biscuit type of dog foods. J Assoc Off Agric Chem 35, 799805.
34. Prosky, L, Asp, N-G, Schweizer, TF, et al. (1992) Determination of soluble and insoluble dietary fiber in foods and food products: collaborative study. J AOAC 75, 360367.
35. Knapp, BK, Parsons, CM, Swanson, KS, et al. (2008) Physiological responses to novel carbohydrates as assessed using canine and avian models. J Agric Food Chem 56, 79998006.
36. Lubbs, DC, Vester Boler, BM, Ridge, TK, et al. (2010) Dietary macronutrients and feeding frequency affect fasting and postprandial concentrations of hormones involved in appetite regulation in adult dogs. J Anim Sci 88, 39453953.
37. Erwin, ES, Marco, GJ & Emery, EM (1961) Volatile fatty acid analyses of blood and rumen fluid by gas chromatography. J Dairy Sci 44, 17681771.
38. Chaney, AL & Marbach, EP (1962) Modified reagents for determination of urea and ammonia. Clin Chem 8, 130132.
39. Flickinger, EA, Schreijen, EMWC, Patil, AR, et al. (2003) Nutrient digestibilities, microbial populations, and protein catabolites as affected by fructan supplementation of dog diets. J Anim Sci 81, 20082018.
40. Kakiyama, G, Muto, A, Takei, H, et al. (2014) A simple and accurate HPLC method for fecal bile acid profile in healthy and cirrhotic subjects: validation by GC-MS and LC-MS. J Lipid Res 55, 978990.
41. McInnes, P & Cutting, M (2010) Manual of Procedures for Human Microbiome Project – Core Microbiome Sampling Protocol A #07-001, vol. 9. Bethesda, MD: National Institutes of Health.
42. Caporaso, JG, Lauber, CL, Walters, WA, et al. (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6, 16211624.
43. Malinen, E, Rinttilä, T, Kajander, K, et al. (2005) Analysis of the fecal microbiota of irritable bowel syndrome patients and healthy controls with real-time PCR. Am J Gastroenterol 100, 373382.
44. Rossi, G, Pengo, G, Caldin, M, et al. (2014) Comparison of microbiological, histological, and immunomodulatory parameters in response to treatment with either combination therapy with prednisone and metronidazole or probiotic VSL#3 strains in dogs with idiopathic inflammatory bowel disease. PLOS ONE 9, e94699.
45. Suchodolski, JS, Markel, ME, Garcia-Mazcorro, JF, et al. (2012) The fecal microbiome in dogs with acute diarrhea and idiopathic inflammatory bowel disease. PLOS ONE 7, e51907.
46. Caporaso, JG, Kuczynski, J, Stombaugh, J, et al. (2010) QIIME allows analysis of high-throughput community sequencing data intensity normalization improves color calling in SOLiD sequencing. Nat Publ Gr 7, 335336.
47. Edgar, RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 24602461.
48. DeSantis, TZ, Hugenholtz, P, Larsen, N, et al. (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72, 50695072.
49. Lozupone, C & Knight, R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71, 82288235.
50. Deng, P, Jones, JC & Swanson, KS (2014) Effects of dietary macronutrient composition on the fasted plasma metabolome of healthy adult cats. Metabolomics 10, 638650.
51. Parks, DH, Tyson, GW, Hugenholtz, P, et al. (2014) STAMP: Statistical analysis of taxonomic and functional profiles. Bioinformatics 30, 31233124.
52. Mollard, RC, Wong, CL, Luhovyy, BL, et al. (2014) Second-meal effects of pulses on blood glucose and subjective appetite following a standardized meal 2 h later. Appl Physiol Nutr Metab 39, 849851.
53. Clark, C, Gardiner, J, McBurney, M, et al. (2006) Effects of breakfast meal composition on second meal metabolic responses in adults with type 2 diabetes mellitus. Eur J Clin Nutr 60, 11221129.
54. Roediger, WEW (1982) Utilization of nutrients by isolated epithelial cells of the rat colon. Gastroenterology 83, 424429.
55. Liong, M-TT (2007) Probiotics: a critical review of their potential role as antihypertensives, immune modulators, hypocholesterolemics, and perimenopausal treatments. Nutr Rev 65, 316328.
56. Topping, DL & Clifton, PM (2001) Short-chain fatty acids and human colonic function: roles of resistant starch and nonstarch polysaccharides. Physiol Rev 81, 10311064.
57. Cummings, J & Macfarlane, G (1991) The control and consequences of bacterial fermenation in the human colon. J Appl Bacteriol, 443459.
58. Macfarlane, GT & Allison, C (1986) Utilisation of protein by human gut bacteria. FEMS Microbiol Ecol 38, 1924.
59. Ridlon, JM, Kang, D-J & Hylemon, PB (2006) Bile salt biotransformations by human intestinal bacteria. J Lipid Res 47, 241259.
60. Suchodolski, JS (2016) Diagnosis and interpretation of intestinal dysbiosis in dogs and cats. Vet J 215, 3037.
61. Washizu, T, Ikenaga, H, Washizu, M, et al. (1990) Bile acid composition of dog and cat gall-bladder bile. Jpn J Vet Sci 52, 423425.
62. Honneffer, J, Guard, B, Steiner, JM, et al. (2015) Untargeted metabolomics reveals disruption within bile acid, cholesterol, and tryptophan metabolic pathways in dogs with idiopathic inflammatory bowel disease. Gastroenterology 148, S715.
63. Rémésy, C, Levrat, M, Gamet, L, et al. (1993) Cecal fermentations in rats fed oligosaccharides (inulin) are modulated by dietary calcium level. Am J Physiol 264, G855G862.
64. Labbe, A, Ganopolsky, JG, Martoni, CJ, et al. (2014) Bacterial bile metabolising gene abundance in Crohn’s, ulcerative colitis and type 2 diabetes metagenomes. PLOS ONE 9, e115175.
65. AlShawaqfeh, M, Wajid, B, Minamoto, Y, et al. (2017) A dysbiosis index to assess microbial changes in fecal samples of dogs with chronic inflammatory enteropathy. FEMS Microbiol Ecol 93, fix136.
66. Igarashi, H, Ohno, K, Horigome, A, et al. (2016) Fecal dysbiosis in miniature dachshunds with inflammatory colorectal polyps. Res Vet Sci 105, 4146.

Keywords

Type Description Title
WORD
Supplementary materials

Alexander et al. supplementary material
Table S1 and Figures S1-S2

 Word (130 KB)
130 KB

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed