Alteration of the fecal microbiota and serum metabolite profiles in dogs with idiopathic inflammatory bowel disease

Gut Microbes

Volumn 6, Issue 1, 2015, Pages 33-47

  Minamoto, Yasushi ^a   Otoni, Cristiane C ^b   Steelman, Samantha M ^a   Büyükleblebici, Olga ^c   Steiner, Jörg M ^a   Jergens, Albert E ^b   Suchodolski, Jan S ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

^b IOWA STATE UNIVERSITY   (United States)

^c AKSARAY UNIVERSITY   (Turkey)

Author keywords

Dog; Dysbiosis; Faecalibacterium; Feces; IBD; Metabolomics; Microbiome

Indexed keywords

3 HYDROXYBUTYRIC ACID; BIOLOGICAL MARKER; BUDESONIDE; CYCLOSPORIN; GLUCONIC ACID; HEXURONIC ACID; METRONIDAZOLE; PREDNISOLONE; PREDNISONE; RIBOSE; RNA 16S; TRANSCRIPTION FACTOR;

AGE; AMINO ACID METABOLISM; ANIMAL EXPERIMENT; ANIMAL TISSUE; AREA UNDER THE CURVE; ARTICLE; BACTERIAL SECRETION SYSTEM; BACTEROIDETES; BIFIDOBACTERIUM; BLAUTIA; BODY WEIGHT; CANINE INFLAMMATORY BOWEL DISEASE ACTIVITY INDEX; CARBOHYDRATE METABOLISM; CLINICAL EXAMINATION; CONTROLLED STUDY; CORRELATION ANALYSIS; DIAGNOSTIC TEST ACCURACY STUDY; DISEASE ASSESSMENT; DNA EXTRACTION; DOG; ESCHERICHIA COLI; FAECALIBACTERIUM; FECES ANALYSIS; FECES MICROFLORA; FEMALE; FUSOBACTERIA; GAMMAPROTEOBACTERIA; GAS CHROMATOGRAPHY; GENE SEQUENCE; HISTOGRAM; HISTOLOGY; INFLAMMATORY BOWEL DISEASE; LACTOBACILLUS; MALE; MASS SPECTROMETRY; METABOLOMICS; MICROBIAL COMMUNITY; NONHUMAN; OXIDATIVE STRESS; PENTOSE PHOSPHATE CYCLE; PYROSEQUENCING; REAL TIME POLYMERASE CHAIN REACTION; RECEIVER OPERATING CHARACTERISTIC; RUMINOCOCCACEAE; SEQUENCE ANALYSIS; ANIMAL; BIOTA; CHEMISTRY; DNA SEQUENCE; DOG DISEASES; FECES; INFLAMMATORY BOWEL DISEASES; METABOLOME; METAGENOMICS; MICROBIOLOGY; PATHOLOGY; SERUM; VETERINARY;

BACTERIA (MICROORGANISMS); CANIS FAMILIARIS; CLOSTRIDIA; FAECALIBACTERIUM; GAMMAPROTEOBACTERIA;

ANIMALS; BIOTA; DOG DISEASES; DOGS; FECES; INFLAMMATORY BOWEL DISEASES; METABOLOME; METABOLOMICS; METAGENOMICS; SEQUENCE ANALYSIS, DNA; SERUM;

EID: 84924700052     PISSN: 19490976     EISSN: 19490984     Source Type: Journal    
DOI: 10.1080/19490976.2014.997612     Document Type: Article

References (50)

1. DuPont AW, DuPont HL. The intestinal microbiota and chronic disorders of the gut. Nat Rev Gastroenterol Hepatol 2011; 8:523-31.PMID:21844910; http://dx.doi.org/10.1038/nrgastro.2011.133.
2. Packey C, Sartor R. Commensal bacteria, traditional and opportunistic pathogens, dysbiosis and bacterial killing in inflammatory bowel diseases. Curr Opin Infect Dis 2009; 22:292-301.PMID:19352175; http://dx.doi.org/10.1097/QCO.0b013e32832a8a5d.
3. Suchodolski JS, Dowd SE, Wilke V, Steiner JM, Jergens AE. 16S rRNA gene pyrosequencing reveals bacterial dysbiosis in the duodenum of dogs with idiopathic inflammatory bowel disease. PLoS One 2012; 7:e39333.PMID:22720094; http://dx.doi.org/10.1371/journal.pone.0039333.
4. Suchodolski JS, Markel ME, Garcia-Mazcorro JF, Unterer S, Heilmann RM, Dowd SE, Kachroo P, Ivanov I, Minamoto Y, Dillman EM, et al. The fecal microbiome in dogs with acute diarrhea and idiopathic inflammatory bowel disease. PLoS One 2012; 7: e51907.PMID:23300577; http://dx.doi.org/10.1371/journal.pone.0051907.
5. Suchodolski JS, Xenoulis PG, Paddock CG, Steiner JM, Jergens AE, Steiner JM. Molecular analysis of the bacterial microbiota in duodenal biopsies from dogs with idiopathic inflammatory bowel disease. Vet Microbiol 2010; 142:394-400.PMID:19959301; http://dx.doi.org/10.1016/j.vetmic.2009.11.002.
6. Xenoulis PG, Palculict B, Allenspach K, Steiner JM, Van House AM, Suchodolski JS. Molecular-phylogenetic characterization of microbial communities imbalances in the small intestine of dogs with inflammatory bowel disease. FEMS Microbiol Ecol 2008; 66:579-89.PMID:18647355; http://dx.doi.org/10.1111/j.1574-6941.2008.00556.x.
7. Simpson KW, Jergens AE. Pitfalls and progress in the diagnosis and management of canine inflammatory bowel disease. Vet Clin North Am Small Anim Pract 2011; 41:381-98.PMID:21486642; http://dx.doi.org/10.1016/j.cvsm.2011.02.003.
8. Overstreet A, Ramer-Tait A. The Role of the Micro-biota in Gastrointestinal Health and Disease. In: Szabo I, editor. Inflammatory Bowel Disease. InTech Published; 2012.
9. Washabau R, Day M. Endoscopic, biopsy, and histopathologic guidelines for the evaluation of gastrointestinal inflammation in companion animals. J Vet Intern Med 2010; 24:10-26.PMID:20391635; http://dx.doi.org/10.1111/j.1939-1676.2010.0520.x.
10. Jergens a E, Crandell J, Morrison J A, Deitz K, Pressel M, Ackermann M, Suchodolski JS, Steiner JM, Evans R. Comparison of oral prednisone and prednisone combined with metronidazole for induction therapy of canine inflammatory bowel disease: a randomized-controlled trial. J Vet Intern Med 2010; 24:269-77.PMID:20051005; http://dx.doi.org/10.1111/j.1939-1676.2009.0447.x.
11. Brestoff JR, Artis D. Commensal bacteria at the interface of host metabolism and the immune system. Nat Immunol 2013; 14:676-84.PMID:23778795; http://dx.doi.org/10.1038/ni.2640.
12. Nicholson JK, Lindon JC. Systems biology: Metabonomics. Nature 2008; 455:1054-6.PMID:18948945; http://dx.doi.org/10.1038/4551054a.
13. Marchesi J, Holmes E, Khan F, Kochhar S, Scanlan P, Shanahan F, Wilson I, Wang Y. Rapid and noninvasive metabonomic characterization of inflammatory bowel disease. J Proteome Res 2007; 6:546-51.PMID:17269711; http://dx.doi.org/10.1021/pr060470d.
14. Lin H-M, Helsby N, Rowan D, Ferguson L. Using metabolomic analysis to understand inflammatory bowel diseases. Inflamm Bowel Dis 2011; 17:1021-9.PMID:20629098; http://dx.doi.org/10.1002/ibd.21426.
15. De Preter V, Verbeke K. Metabolomics as a diagnostictool in gastroenterology. World J Gastrointest Pharmacol Ther 2013; 4:97-107.PMID:24199025.
16. Patti GJ, Yanes O, Siuzdak G. Innovation: Metabolomics: the apogee of the omics trilogy. Nat Rev MolCell Biol 2012; 13:263-9.PMID:22436749; http://dx.doi.org/10.1038/nrm3314.
17. Steelman SM, Johnson P, Jackson A, Schulze J, Chowdhary BP. Serum metabolomics identifies citrulline as a predictor of adverse outcomes in an equine model of gut-derived sepsis. Physiol Genomics 2014; 46:339-47.PMID:24619519; http://dx.doi.org/10.1152/physiolgenomics.00180.2013.
18. Zhang J, Wei S, Liu L, Nagana Gowda G A, Bonney P, Stewart J, Knapp DW, Raftery D. NMR-based metabolomics study of canine bladder cancer. Biochim Biophys Acta 2012; 1822:1807-14.PMID:22967815; http://dx.doi.org/10.1016/j.bbadis.2012.08.001.
19. Ritchie L, Burke K, Garcia-Mazcorro J, Steiner J, Suchodolski J. Characterization of fecal microbiota in cats using universal 16S rRNA gene and group-specific primers for Lactobacillus and Bifidobacterium spp. Vet Microbiol 2010; 144:140-146.PMID:20092970; http://dx.doi.org/10.1016/j.vetmic.2009.12.04520.
20. Handl S, Dowd SE, Garcia-Mazcorro JF, Steiner JM, Suchodolski JS. Massive parallel 16S rRNA gene pyrosequencing reveals highly diverse fecal bacterial and fungal communities in healthy dogs and cats. FEMS Microbiol Ecol 201; 76:301-10; http://dx.doi.org/10.1111/j.1574-6941.2011.01058.x.
21. Ritchie L, Steiner J, Suchodolski J. Assessment of microbial diversity along the feline intestinal tract using16S rRNA gene analysis. FEMS Microbiol Ecol 2008; 66:590-598.PMID:19049654; http://dx.doi.org/10.1111/j.1574-6941.2008.00609.x.
22. Fiehn O, Wohlgemuth G, Scholz M. Setup and annotation of metabolomic experiments by integrating biological and mass spectrometric metadata. Data Integr life Sci 2005;224-39; http://dx.doi.org/10.1007/11530084_18.
23. Xia J, Broadhurst DI, Wilson M, Wishart DS. Translational biomarker discovery in clinical metabolomics: an introductory tutorial. Metabolomics 2013; 9:280-99.PMID:23543913; http://dx.doi.org/10.1007/s11306-012-0482-9.
24. Barupal DK, Haldiya PK, Wohlgemuth G, Kind T, Kothari SL, Pinkerton KE, Fiehn O. MetaMapp: mapping and visualizing metabolomic data by integrating information from biochemical pathways and chemical and mass spectral similarity. BMC Bioinformatics 2012; 13:99.PMID:22591066; http://dx.doi.org/10.1186/1471-2105-13-99.
25. Kabeerdoss J, Sankaran V, Pugazhendhi S, Ramakrishna BS. Clostridium leptum group bacteria abundance and diversity in the fecal microbiota of patients with inflammatory bowel disease: a case-control study in India. BMC Gastroenterol 2013; 13:20.PMID:23351032; http://dx.doi.org/10.1186/1471-230X-13-20.
26. Gophna U, Sommerfeld K, Gophna S, Doolittle WF, Veldhuyzen van Zanten SJO. Differences between tis-sue-associated intestinal microfloras of patients with Crohn’s disease and ulcerative colitis. J Clin Microbiol 2006; 44:4136-41.PMID:16988016; http://dx.doi.org/10.1128/JCM.01004-06.
27. Manichanh C, Rigottier-Gois L, Bonnaud E, Gloux K, Pelletier E, Frangeul L, Nalin R, Jarrin C, Chardon P, Marteau P, et al. Reduced diversity of faecal microbiota in Crohn’s disease revealed by a metagenomic approach. Gut 2006; 55:205-11.PMID:16188921; http://dx.doi.org/10.1136/gut.2005.073817.
28. Frank DN, St Amand AL, Feldman R A, Boedeker EC, Harpaz N, Pace NR. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci U S A 2007; 104:13780-5.PMID:17699621; http://dx.doi.org/10.1073/pnas.0706625104.
29. De la Fuente M, Franchi L, Araya D, Dıaz-Jimenez D, Olivares M, Alvarez-Lobos M, Golenbock D, Gonzalez M-J, Lopez-Kostner F, Quera R, et al. Escherichia coliisolates from inflammatory bowel diseases patients survive in macrophages and activate NLRP3 inflammasome. Int J Med Microbiol 2014; :1-9.PMID:24183099; http://dx.doi.org/10.1155/2014/489569.
30. Kotlowski R, Bernstein CN, Sepehri S, Krause DO. High prevalence of Escherichia coli belonging to the B2CD phylogenetic group in inflammatory bowel disease. Gut 2007; 56:669-75.PMID:17028128; http://dx.doi.org/10.1136/gut.2006.099796.
31. Simpson KW, Dogan B, Rishniw M, Goldstein RE, Klaessig S, McDonough PL, German AJ, Yates RM, Russell DG, Johnson SE, et al. Adherent and invasive Escherichia coli is associated with granulomatous colitis in boxer dogs. Infect Immun 2006; 74:4778-92.PMID:16861666; http://dx.doi.org/10.1128/IAI.00067-06.
32. Suchodolski JS, Camacho J, Steiner JM. Analysis of bacterial diversity in the canine duodenum, jejunum, ileum, and colon by comparative 16S rRNA gene analysis. FEMS Microbiol Ecol 2008; 66:567-78.PMID:18557939; http://dx.doi.org/10.1111/j.1574-6941.2008.00521.x.
33. Rossi G, Pengo G, Caldin M, Palumbo Piccionello A, Steiner JM, Cohen ND, Jergens AE, Suchodolski JS. 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 2014; 9:e94699.PMID:24722235; http://dx.doi.org/10.1371/journal.pone.0094699.
34. Blachier F, Mariotti F, Huneau JF, Tome D. Effects ofamino acid-derived luminal metabolites on the colonicepithelium and physiopathological consequences. Amino Acids 2007; 33:547-62.PMID:17146590; http://dx.doi.org/10.1007/s00726-006-0477-9.
35. Smith MI, Yatsunenko T, Manary MJ, Trehan I, Mkakosya R, Cheng J, Kau AL, Rich SS, Concannon P, Mychaleckyj JC, et al. Gut microbiomes of Malawian twin pairs discordant for kwashiorkor. Science 2013; 339:548-54.PMID:23363771; http://dx.doi.org/10.1126/science.1229000.
36. Duncan SH, Hold GL, Harmsen HJM, Stewart CS, Flint HJ. Growth requirements and fermentation products of Fusobacterium prausnitzii, and a proposal to reclassify it as Faecalibacterium prausnitzii gen. nov., comb. nov. Int J Syst Evol 2002; 52:2141-6; http://dx.doi.org/10.1099/ijs.0.02241-0.
37. Garcia-Mazcorro JF, Dowd SE, Poulsen J, Steiner JM, Suchodolski JS. Abundance and short-term temporalvariability of fecal microbiota in healthy dogs. Microbiologyopen 2012;1:340-7.PMID:23170232; http://dx.doi.org/10.1002/mbo3.36.
38. Riganti C, Gazzano E, Polimeni M, Aldieri E, Ghigo D. The pentose phosphate pathway: an antioxidantdefense and a crossroad in tumor cell fate. Free Radic Biol Med 2012; 53:421-36.PMID:22580150; http://dx.doi.org/10.1016/j.freeradbiomed.2012.05.006.
39. Bertin Y, Girardeau JP, Chaucheyras-Durand F, Lyan B, Pujos-Guillot E, Harel J, Martin C. Enterohaemorrhagic Escherichia coli gains a competitive advantage by using ethanolamine as a nitrogen source in the bovine intestinal content. Environ Microbiol 2011; 13:365-77.PMID:20849446; http://dx.doi.org/10.1111/j.1462-2920.2010.02334.x.
40. Morgan XC, Tickle TL, Sokol H, Gevers D, Devaney KL, Ward D V, Reyes J A, Shah S A, LeLeiko N, Snapper SB, et al. Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment. Genome Biol 2012; 13:R79PMID:23013615; http://dx.doi.org/10.1186/gb-2012-13-9-r79.
41. Gevers D, Kugathasan S, Denson L A, Vazquez-Baeza Y, Van Treuren W, Ren B, Schwager E, Knights D, Song SJ, Yassour M, et al. The treatment-naive microbiome in new-onset Crohn’s disease. Cell Host Microbe 2014; 15:382-92.PMID:24629344; http://dx.doi.org/10.1016/j.chom.2014.02.005.
42. Rooks MG, Veiga P, Wardwell-Scott LH, Tickle T, Segata N, Michaud M, Gallini CA, Beal C, van Hylckama-Vlieg JE, Ballal S a, et al. Gut microbiome composition and function in experimental colitis during active disease and treatment-induced remission. ISME J 2014; 1-15.PMID:24152717.
43. Moubareck C, Gavini F, Vaugien L, Butel MJ, Doucet-Populaire F. Antimicrobial susceptibility of bifidobacte-ria. J Antimicrob Chemother 2005; 55:38-44.PMID:15574479; http://dx.doi.org/10.1093/jac/dkh495.
44. Theriot CM, Koenigsknecht MJ, Carlson PE, Hatton GE, Nelson AM, Li B, Huffnagle GB, Z Li J, Young VB. Antibiotic-induced shifts in the mouse gut micro- biome and metabolome increase susceptibility to Clostridium difficile infection. Nat Commun 2014; 5:3114.PMID:24445449; http://dx.doi.org/10.1038/ncomms4114.
45. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, et al. correspondEnce QIIMEallows analysis of high- throughput communitysequencing data Intensity normalization improves colorcalling in SOLiD sequencing. Nat Publ Gr 2010;7:335-6.
46. Garcia-Mazcorro JF, Suchodolski JS, Jones KR, Clark-Price SC, Dowd SE, Minamoto Y, Markel M, Steiner JM, Dossin O. Effect of the proton pump inhibitor omeprazole on the gastrointestinal bacterial microbiota of healthy dogs. Fems Micriobiology Ecol 2012;80:642-636.
47. Fiehn O, Garvey WT, Newman JW, Lok KH, Hoppel CL, Adams SH. Plasma metabolomic profiles reflective of glucose homeostasis in non-diabetic and type 2 diabeticobese African-American women. PLoS One 2010;5:e15234.PMID:21170321; http://dx.doi.org/10.1371/journal.pone.0015234.
48. Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C. Metagenomic biomarker discovery and explanation. Genome Biol 2011; 12:R60.PMID:21702898; http://dx.doi.org/10.1186/gb-2011-12-6-r60.
49. Xia J, Wishart DS. Web-based inference of biological patterns, functions and pathways from metabolomic data using MetaboAnalyst. Nat Protoc 2011; 6:743-60.PMID:21637195; http://dx.doi.org/10.1038/nprot.2011.319.
50. Saito R, Smoot ME, Ono K, Ruscheinski J, Wang P, Lotia S, Pico AR, Bader GD, Ideker T. A travel guide to Cytoscape plugins. 2012; 9:1069-76.PMID:23132118.