Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-27T13:53:02.814Z Has data issue: false hasContentIssue false
  • English
  • Français

Current state of knowledge: the canine gastrointestinal microbiome

Published online by Cambridge University Press:  30 May 2012

Seema Hooda ,
Yasushi Minamoto ,
Jan S. Suchodolski  and
Kelly S. Swanson
Seema Hooda
Affiliation:
Department of Animal Sciences, University of Illinois, 1207 West Gregory Drive, Urbana, Illinoi 61801, USA
Yasushi Minamoto
Affiliation:
Gastrointestinal Laboratory, Department of Small Animal Clinical Sciences, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, Texas 77843, USA
Jan S. Suchodolski
Affiliation:
Gastrointestinal Laboratory, Department of Small Animal Clinical Sciences, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, Texas 77843, USA
Kelly S. Swanson*
Affiliation:
Department of Animal Sciences, University of Illinois, 1207 West Gregory Drive, Urbana, Illinoi 61801, USA
*
*Corresponding author. E-mail: ksswanso@illinois.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

Gastrointestinal (GI) microbes have important roles in the nutritional, immunological, and physiologic processes of the host. Traditional cultivation techniques have revealed bacterial density ranges from 104 to 105 colony forming units (CFU)/g in the stomach, from 105 to 107 CFU/g in the small intestine, and from 109 to 1011 CFU/g in the colon of healthy dogs. As a small number of bacterial species can be grown and studied in culture, however, progress was limited until the recent emergence of DNA-based techniques. In recent years, DNA sequencing technology and bioinformatics have allowed for better phylogenetic and functional/metabolic characterization of the canine gut microbiome. Predominant phyla include Firmicutes, Bacteroidetes, Fusobacteria, Proteobacteria, and Actinobacteria. Studies using 16S ribosomal RNA (rRNA) gene pyrosequencing have demonstrated spatial differences along the GI tract and among microbes adhered to the GI mucosa compared to those in intestinal contents or feces. Similar to humans, GI microbiome dysbiosis is common in canine GI diseases such as chronic diarrhea and inflammatory bowel diseases. DNA-based assays have also identified key pathogens contributing to such conditions, including various Clostridium, Campylobacter, Salmonella, and Escherichia spp. Moreover, nutritionists have applied DNA-based techniques to study the effects of dietary interventions such as dietary fiber, prebiotics, and probiotics on the canine GI microbiome and associated health indices. Despite recent advances in the field, the canine GI microbiome is far from being fully characterized and a deeper characterization of the phylogenetic and functional/metabolic capacity of the GI microbiome in health and disease is needed. This paper provides an overview of recent studies performed to characterize the canine GI microbiome.

Keywords

dietgastrointestinal healthpathogens
Type
Review Article
Information
Animal Health Research Reviews , Volume 13 , Issue 1 , June 2012 , pp. 78 - 88
Copyright
Copyright © Cambridge University Press 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Apanavicius, CJ, Powell, KL, Vester, BM, Karr-Lilienthal, LK, Pope, LL, Fastinger, ND, Wallig, MA, Tappenden, KA and Swanson, KS (2007). Fructan supplementation and infection affect food intake, fever, and epithelial sloughing from Salmonella challenge in weanling puppies. Journal of Nutrition 137: 1923–1930.CrossRefGoogle ScholarPubMed
Bell, JA, Kopper, JJ, Turnbull, JA, Barbu, NI, Murphy, AJ and Mansfield, LS (2008). Ecological characterization of the colonic microbiota of normal and diarrheic dogs. Interdisciplinary Perspectives on Infectious Diseases 2008: 149–694.CrossRefGoogle ScholarPubMed
Benno, Y, Nakao, H, Uchida, K and Mitsuoka, T (1992). Impact of the advances in age on the gastrointestinal microflora of beagle dogs. Journal of Veterinary Medical Science/The Japanese Society of Veterinary Science 54: 703–706.CrossRefGoogle ScholarPubMed
Beynen, AC, Baas, JC, Hoekemeijer, PE, Kappert, HJ, Bakker, MH, Koopman, JP and Lemmens, AG (2002). Fecal bacterial profile, nitrogen excretion and mineral absorption in healthy dogs fed supplemental oligofructose. Journal of Animal Physiology and Animal Nutrition 86: 298–305.CrossRefGoogle ScholarPubMed
Clarridge, JE (2004). Impact of 16S rRNA gene sequence analysis for the identification of bacteria on clinical microbiology and infectious diseases. Clinical Microbiology Review 17: 840–862.CrossRefGoogle ScholarPubMed
Davis, CP, Cleven, D, Balish, E and Yale, CE (1977). Bacterial association in the gastrointestinal tract of beagle dogs. Applied and Environmental Microbiology 34: 194–206.CrossRefGoogle ScholarPubMed
Eckburg, PB, Bik, EB, Bernstein, CN, Purdom, E, Dethlefsen, L, Sargent, M, Gill, SR, Nelson, KE and Relman, DA (2005). Diversity of the human intestinal microbial flora. Science 308: 1635–1638.CrossRefGoogle ScholarPubMed
Faber, TA, Hopkins, AC, Middelbos, IS, Price, NP and Fahey, GC Jr (2011). Galactoglucomannan oligosaccharide supplementation affects nutrient digestibility, fermentation end-product production, and large bowel microbiota of the dog. Journal of Animal Science 89: 103–112.CrossRefGoogle ScholarPubMed
Flint, HJ, Duncan, SH, Scott, KP and Louis, P (2007). Interactions and competition within the microbial community of the human colon: links between diet and health. Environmental Microbiology 9: 1101–1111.CrossRefGoogle ScholarPubMed
Fox, JG (1998). Enteric bacterial infections-gastric helicobacters. In: Greene, CE (ed.) Infectious Diseases of the Dog and Cat. Philadelphia, PA: WB Saunders Company, pp. 229–233.Google Scholar
Friswell, M, Campbell, B and Rhodes, J (2010). The role of bacteria in the pathogenesis of inflammatory bowel disease. Gut and Liver 4: 295–306.CrossRefGoogle ScholarPubMed
Garcia-Mazcorro, JF, Lanerie, DJ, Dowd, SE, Paddock, CG, Grutzner, N, Steiner, JM, Ivanek, R and Suchodolski, JS (2011). Effect of a multi-species synbiotic formulation on fecal bacterial microbiota of healthy cats and dogs as evaluated by pyrosequencing. FEMS Microbiology Ecology 78: 542–554.CrossRefGoogle ScholarPubMed
Garcia-Mazcorro, JF, Suchodolski, JS, Jones, KR, Clark-Price, SC, Dowd, SE, Minamoto, Y, Markel, M, Steiner, JM, Dossin, O and Marchesi, J. (2012). Effect of the proton-pump inhibitor omeprazole on the gastrointestinal bacterial microbiota of healthy dogs. FEMS Microbiology Ecology 80: 624–636 doi: 10.1111/j.1574-6941.2012.01331.CrossRefGoogle ScholarPubMed
German, AJ, Day, MJ, Ruaux, CG, Steiner, JM, Williams, DA and Hall, EJ (2003). Comparison of direct and indirect tests for small intestinal bacterial overgrowth and antibiotic-responsive diarrhea in dogs. Journal of Veterinary Internal Medicine 17: 33–43.Google ScholarPubMed
Greene, CE (1998). Infectious Diseases of Dog and Cat. 2nd edn. Philadelphia, PA: WB Saunders Company.Google Scholar
Grieshop, CM, Flickinger, EA, Bruce, KJ, Patil, AR, Czarnecki-Maulden, GL and Fahey, GC Jr (2004). Gastrointestinal and immunological responses of senior dogs to chicory and mannan-oligosaccharides. Archives of Animal Nutrition 58: 483–493.CrossRefGoogle ScholarPubMed
Hall, EJ (2011). Antibiotic-responsive diarrhea in small animals. Veterinary Clinics of North America: Small Animal Practice 41: 273–286.CrossRefGoogle ScholarPubMed
Handl, S, Dowd, SE, Garcia-Mazcorro, JF, Steiner, JM and Suchodolski, JS (2011). Massive parallel 16S rRNA gene pyrosequencing reveals highly diverse fecal bacterial and fungal communities in healthy dogs and cats. FEMS Microbiology Ecology 76: 301–310.CrossRefGoogle ScholarPubMed
Hermanns, W, Kregel, K, Breuer, W and Lechner, J (1995). Helicobacter-like organisms: histopathological examination of gastric biopsies from dogs and cats. Journal of Comparative Pathology 112: 307–318.CrossRefGoogle ScholarPubMed
Hooper, LV, Wong, MH, Thelin, A, Hansson, L, Falk, PG and Gordon, JI (2001). Molecular analysis of commensal host-microbial relationships in the intestine. Science 291: 881–884.CrossRefGoogle ScholarPubMed
Jia, J, Frantz, N, Khoo, C, Gibson, GR, Rastall, RA and McCartney, AL (2010). Investigation of the faecal microbiota associated with canine chronic diarrhea. FEMS Microbiology Ecology 71: 304–312.CrossRefGoogle Scholar
Johnston, KA (1999). Small intestinal bacterial overgrowth. Veterinary Clinics of North America: Small Animal Practice 29: 523–550.Google ScholarPubMed
Kanauchi, O, Matsumoto, Y, Matsumura, M, Fukuoka, M and Bamba, T (2005). The beneficial effects of microflora, especially obligate anaerobes, and their products on the colonic environment in inflammatory bowel disease. Current Pharmaceutical Design 11: 1047–1053.CrossRefGoogle ScholarPubMed
Khachatryan, ZA, Ktsoyan, ZA, Manukyan, GP, Kelly, D, Ghazaryan, KA and Aminov, RI (2008). Predominant role of host genetics in controlling the composition of gut microbiota. PLoS ONE 3: 3064.CrossRefGoogle ScholarPubMed
Ley, RE, Backhed, F, Turnbaugh, P, Lozupone, CA, Knight, RD and Gordon, JI (2005). Obesity alters gut microbial ecology. Proceedings of the National Academy of Sciences of the United States of America 102: 11070–11075.CrossRefGoogle ScholarPubMed
Louis, P, Scott, KP, Duncan, SH and Flint, HJ (2007). Understanding the effects of diet on bacterial metabolism in the large intestine. Journal of Applied Microbiology 102: 1197–1208.CrossRefGoogle ScholarPubMed
Mackie, RI, Sghir, A and Gaskins, HR (1999). Developmental microbial ecology of the neonatal gastrointestinal tract. American Journal of Clinical Nutrition 69: 1035S–1045S.CrossRefGoogle ScholarPubMed
Mariat, D, Firmesse, O, Levenez, F, Guimaraes, V, Sokol, H, Dore, J, Corthier, G and Furet, JP (2009). The Firmicutes/Bacteroidetes ratio of the human microbiota changes with age. BMC Microbiology 9: 123.CrossRefGoogle ScholarPubMed
Marks, SL and Kather, EJ (2003). Bacterial-associated diarrhea in the dog: a critical appraisal. The Veterinary clinics of North America: Small Animal Practice 33: 1029–1060.CrossRefGoogle ScholarPubMed
Marks, SL, Rankin, SC, Byrne, BA and Weese, JS (2011). Enteropathogenic bacteria in dogs and cats: diagnosis, epidemiology, treatment, and control. Journal of Veterinary Internal Medicine 25: 1195–1208.CrossRefGoogle ScholarPubMed
Mentula, S, Harmoinen, J, Heikkila, M, Westermarck, E, Rautio, M, Huovinen, P and Kononen, E (2005). Comparison between cultured small-intestinal and fecal microbiotas in beagle dogs. Applied and Environmental Microbiology 71: 4169–4175.CrossRefGoogle ScholarPubMed
Metzler-Zebeli, BU, Hooda, S, Mosenthin, R, Ganzle, MG and Zijlstra, RT (2010). Bacterial fermentation affects net mineral flux in the large intestine of pigs fed diets with viscous and fermentable nonstarch polysaccharides. Journal of Animal Science 88: 3351–3362.CrossRefGoogle ScholarPubMed
Middelbos, IS, Fastinger, ND and Fahey, GC Jr (2007). Evaluation of fermentable oligosaccharides in diets fed to dogs in comparison to fiber standards. Journal of Animal Science 85: 3033–3044.CrossRefGoogle ScholarPubMed
Middelbos, IS, Vester Boler, BM, Qu, A, White, BA, Swanson, KS and Fahey, GC Jr (2010). Phylogenetic characterization of fecal microbial communities of dogs fed diets with or without supplemental dietary fiber using 454 pyrosequencing. PLoS ONE 5: e9768.CrossRefGoogle ScholarPubMed
Momozawa, Y, Deffontaine, V, Louis, E and Medrano, JF (2011). Characterization of bacteria in biopsies of colon and stools by high throughput sequencing of the V2 region of bacterial 16S rRNA gene in human. PLoS ONE 6: e16952.CrossRefGoogle ScholarPubMed
Neiger, R and Simpson, KW (2000). Helicobacter infection in dogs and cats: facts and fiction. Journal of Veterinary Internal Medicine 14: 125–133.CrossRefGoogle Scholar
Peterson, J, Garges, S, Giovanni, M, McInnes, P, Wang, L, Schloss, JA, Bonazzi, V, McEwen, JE, Wetterstrand, KA, Deal, C, Baker, CC, Di Francesco, V, Howcroft, TK, Karp, RW, Lunsford, RD, Wellington, CR, Belachew, T, Wright, M, Giblin, C, David, H, Mills, M, Salomon, R, Mullins, C, Akolkar, B, Begg, L, Davis, C, Grandison, L, Humble, M, Khalsa, J, Little, AR, Peavy, H, Pontzer, C, Portnoy, M, Sayre, MH, Starke-Reed, P, Zakhari, S, Read, J, Watson, B and Guyer, M (2009). The NIH human microbiome project. Genome Research 19: 2317–2323.Google ScholarPubMed
Rowland, IR, Mallett, AK and Wise, A (1985). The effect of diet on the mammalian gut flora and its metabolic activities. Critical Reviews in Toxicology 16: 31–103.CrossRefGoogle ScholarPubMed
Russell, TJ (1998). The Effect of Natural Sources of Non-Digestible Oligosaccharides on the Fecal Microflora of the Dog and Effects on Digestion. Missouri: Friskies R&D centre, © Friskies-Europe.Google Scholar
Seksik, KP (2010). Gut microbiota and IBD. Gastroenterology Clinical Biology 34: S44–51.CrossRefGoogle ScholarPubMed
Simpson, KW, Dogan, B, Rishniw, M, Goldstein, RE, Klaessig, S, McDonough, PL, German, AJ, Yates, RM, Russell, DG, Johnson, SE, Berg, DE, Harel, J, Bruant, G, McDonough, SP and Schukken, YH (2006). Adherent and invasive Escherichia coli is associated with granulomatous colitis in boxer dogs. Infection and Immunity 74: 4778–4992.CrossRefGoogle ScholarPubMed
Spears, JK, Karr-Lilienthal, LK, Grieshop, CM, Flickinger, EA, Wolf, BW and Fahey, GC Jr (2005). Pullulans and gamma-cyclodextrin affect apparent digestibility and metabolism in healthy adult ileal cannulated dogs. The Journal of Nutrition 135: 1946–1952.CrossRefGoogle ScholarPubMed
Suchodolski, JS, Camacho, J and Steiner, JM (2008). Analysis of bacterial diversity in the canine duodenum, jejunum, ileum, and colon by comparative 16S rRNA gene analysis. FEMS Microbiology Ecology 66: 567–578.CrossRefGoogle ScholarPubMed
Suchodolski, JS, Dowd, SE, Westermarck, E, Steiner, JM, Wolcott, RD, Spillmann, T and Harmoinen, JA (2009). The effect of the macrolide antibiotic tylosin on microbial diversity in the canine small intestine as demonstrated by massive parallel 16S rRNA gene sequencing. BMC Microbiology 9: 210.CrossRefGoogle ScholarPubMed
Suchodolski, JS, Xenoulis, PG, Paddock, CG, Steiner, JM and Jergens, AE (2010). Molecular analysis of the bacterial microbiota in duodenal biopsies from dogs with idiopathic inflammatory bowel disease. Veterinary Microbiology 142: 394–400.CrossRefGoogle ScholarPubMed
Sunvold, GD, Fahey, GC Jr, Merchen, NR, Titgemeyer, EC, Bourquin, LD, Bauer, LL and Reinhart, GA (1995). Dietary fiber for dogs: IV. In vitro fermentation of selected fiber sources by dog fecal inoculum and in vivo digestion and metabolism of fiber-supplemented diets. Journal of Animal Science 73: 1099–1109.CrossRefGoogle ScholarPubMed
Swanson, KS, Dowd, SE, Suchodolski, JS, Middelbos, IS, Vester, BM, Barry, KA, Nelson, KE, Torralba, M, Henrissat, B, Coutinho, PM, Cann, IK, White, BA and Fahey, GC Jr (2011). Phylogenetic and gene-centric metagenomics of the canine intestinal microbiome reveals similarities with humans and mice. ISME Journal 5: 639–649.CrossRefGoogle ScholarPubMed
Swanson, KS, Grieshop, CM, Flickinger, EA, Healy, HP, Dawson, KA, Merchen, NR and Fahey, GC Jr (2002a). Effects of supplemental fructooligosaccharides plus mannanoligosaccharides on immune function and ileal and fecal microbial populations in adult dogs. Archiv fur Tierernahrung 56: 309–318.CrossRefGoogle ScholarPubMed
Swanson, KS, Grieshop, CM, Flickinger, EA, Bauer, LL, Healy, HP, Dawson, KA, Merchen, NR and Fahey, GC Jr (2002b). Supplemental fructooligosaccharides and mannanoligosaccharides influence immune function, ileal and total tract nutrient digestibilities, microbial populations and concentrations of protein catabolites in the large bowel of dogs. Journal of Nutrition 132: 980–989.CrossRefGoogle ScholarPubMed
Swanson, KS, Grieshop, CM, Flickinger, EA, Bauer, LL, Chow, J, Wolf, BW, Garleb, KA and Fahey, GC Jr (2002c). Fructooligosaccharides and Lactobacillus acidophilus modify gut microbial populations, total tract nutrient digestibilities, and fecal protein catabolites concentrations in healthy adult dogs. Journal of Nutrition 132: 3042–3050.CrossRefGoogle ScholarPubMed
Swanson, KS and Fahey, GC Jr (2006). Prebiotics impacts on companion animals. In: Gibson, GR and Rastall, RA (eds) Prebiotics Development and Application. Hoiboken, NJ: John Wiley and Sons, pp. 213–236.Google Scholar
Terada, A, Hara, H, Oishi, T, Matsui, S, Mitsuoka, T, Nakajyo, S, Fujimori, I and Hara, K (1992). Effect of dietary lactosucrose on faecal flora and faecal metabolites of dogs. Microbial Ecology in Health and Disease 5: 87–92.CrossRefGoogle Scholar
Turnbaugh, PJ, Backhed, F, Fulton, L and Gordon, JI (2008). Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host and Microbe 3: 213–223.CrossRefGoogle ScholarPubMed
Vernia, P, Annese, V, Bresci, G, d'Albasio, G, D'Inca, R, Giaccari, S, Ingrosso, M, Mansi, C, Riegler, G, Valpiani, D, Caprilli, R and Gruppo Italiano per lo Studio del Colon and del Retto (2003). Topical butyrate improves efficacy of 5-ASA in refractory distal ulcerative colitis: results of a multicentre trial. European Journal of Clinical Investigation 33: 244–248.CrossRefGoogle ScholarPubMed
Vester, BM and Fahey, GC Jr (2010). Prebiotics and probiotics in companion animal nutrition. In: Cho, SS and Finocchiaro, E (eds). Handbook of Prebiotics and Probiotics Ingredients: Health Benefits and Food Applications. Boca Raton, FL: CRC Press, pp. 355–380.Google Scholar
Vince, A, Killingley, M and Wrong, OM (1978). Effect of lactulose on ammonia production in a fecal incubation system. Gastroenterology 74: 544–549.CrossRefGoogle Scholar
Virgin, HW and Todd, JA (2011). Metagenomics and personalized medicine. Cell 147: 44–56.CrossRefGoogle ScholarPubMed
Viswanathan, VK, Hodges, K and Hecht, G (2009). Enteric infection meets intestinal function: how bacterial pathogens cause diarrhoea. Nature Review Microbiology 7: 110–119.CrossRefGoogle ScholarPubMed
Wen, L, Ley, RE, Volchkov, PY, Stranges, PB, Avanesyan, L, Stonebraker, AC, Hu, C, Wong, FS, Szot, GL, Bluestone, JA, Gordon, JI and Chervonsky, AV (2008). Innate immunity and intestinal microbiota in the development of Type 1 diabetes. Nature 455: 1109–1113.CrossRefGoogle ScholarPubMed
Wong, JM, de Souza, R, Kendall, CW, Emam, A and Jenkins, DJ (2006). Colonic health: fermentation and short chain fatty acids. Journal of Clinical Gastroenterology 40: 235–243.CrossRefGoogle ScholarPubMed
Xenoulis, PG, Palculict, B, Allenspach, K, Steiner, JM, Van House, AM and Suchodolski, JS (2008). Molecular-phylogenetic characterization of microbial communities imbalances in the small intestine of dogs with inflammatory bowel disease. FEMS Microbiology Ecology 66: 579–589.CrossRefGoogle ScholarPubMed