Randomized, controlled trial evaluating the effect of multi-strain probiotic on the mucosal microbiota in canine idiopathic inflammatory bowel disease

Gut Microbes

Volumn 8, Issue 5, 2017, Pages 451-466

  White, Robin ^a   Atherly, Todd ^b   Guard, Blake ^c   Rossi, Giacomo ^d   Wang, Chong ^a   Mosher, Curtis ^e   Webb, Craig ^f   Hill, Steve ^g   Ackermann, Mark ^a   Sciabarra, Peter ^a   Allenspach, Karin ^a   Suchodolski, Jan ^c   Jergens, Albert E ^a  

^a IOWA STATE UNIVERSITY   (United States)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

^c TEXAS A AND M UNIVERSITY   (United States)

^d UNIVERSITY OF CAMERINO   (Italy)

^e Iowa State University   (United States)

^f USA   (United States)

^g Veterinary Specialty Hospital   (United States)

Author keywords

CIBDAI; FISH; IBD; microbiota; probiotic; randomized controlled trial; tight junction protein

Indexed keywords

METRONIDAZOLE; PROBIOTIC AGENT;

ARTICLE; BACTERIAL FLORA; DISEASE SEVERITY; DOG; ECHOGRAPHY; FLUORESCENCE IN SITU HYBRIDIZATION; FOLLOW UP; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; INFLAMMATORY BOWEL DISEASE; INTESTINE BIOPSY; NONHUMAN; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; PROTEIN LOSING GASTROENTEROPATHY; ANIMAL; CONTROLLED STUDY; CYTOCHEMISTRY; DOG DISEASE; GASTROINTESTINAL TRACT; INTESTINE FLORA; PATHOLOGY; RANDOMIZED CONTROLLED TRIAL; TREATMENT OUTCOME; VETERINARY;

ANIMALS; DOG DISEASES; DOGS; GASTROINTESTINAL MICROBIOME; GASTROINTESTINAL TRACT; HISTOCYTOCHEMISTRY; INFLAMMATORY BOWEL DISEASES; PROBIOTICS; TREATMENT OUTCOME;

EID: 85023777660     PISSN: 19490976     EISSN: 19490984     Source Type: Journal    
DOI: 10.1080/19490976.2017.1334754     Document Type: Article

References (55)

1. Allenspach K. Clinical immunology and immunopathology of the canine and feline intestine. Vet Clin North Am Small Anim Pract 2011; 41:345-60; https://doi.org/10.1016/j.cvsm.2011.01.004
2. 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; https://doi.org/10.1016/j.cvsm.2011.02.003
3. Kathrani A, House A, Catchpole B, Murphy A, German A, Werling D, Allenspach K. Polymorphisms in the Tlr4 and Tlr5 gene are significantly associated with inflammatory bowel disease in German shepherd dogs. PLoS One 2010; 5:e15740; PMID:21203467; https://doi.org/10.1371/journal.pone.0015740
4. Baumgart M, Dogan B, Rishniw M, Weitzman G, Bosworth B, Yantiss R, Orsi RH, Wiedmann M, McDonough P, Kim SG, Berg D, Schukken Y, Scherl E, Simpson KW. Culture independent analysis of ileal mucosa reveals a selective increase in invasive Escherichia coli of novel phylogeny relative to depletion of Clostridiales in Crohn's disease involving the ileum. Isme J 2007; 1:403-18; PMID:18043660; https://doi.org/10.1038/ismej.2007.52
5. 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, Schukken YH. Adherent and invasive Escherichia coli is associated with granulomatous colitis in boxer dogs. Infect Immun 2006; 74:4778-92; PMID:16861666; https://doi.org/10.1128/IAI.00067-06
6. 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; https://doi.org/10.1371/journal.pone.0039333
7. Suchodolski JS, Xenoulis PG, Paddock CG, Steiner JM, Jergens AE. Molecular analysis of the bacterial microbiota in duodenal biopsies from dogs with idiopathic inflammatory bowel disease. Vet Microbiol 2010; 142:394-400; PMID:19959301; https://doi.org/10.1016/j.vetmic.2009.11.002
8. 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; https://doi.org/10.1111/j.1574-6941.2008.00556.x
9. Grzeskowiak L, Endo A, Beasley S, Salminen S. Microbiota and probiotics in canine and feline welfare. Anaerobe 2015; 34:14-23; PMID:25863311; https://doi.org/10.1016/j.anaerobe.2015.04.002
10. 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; https://doi.org/10.1371/journal.pone.0094699
11. Jergens AE, Crandell J, Morrison JA, 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 Int Med 2010; 24:269-77; PMID:20051005; https://doi.org/10.1111/j.1939-1676.2009.0447.x
12. Jergens AE, Schreiner CA, Frank DE, Niyo Y, Ahrens FE, Eckersall PD, Benson TJ, Evans R. A scoring index for disease activity in canine inflammatory bowel disease. J Vet Int Med 2003; 17:291-7; PMID:12774968; https://doi.org/10.1111/j.1939-1676.2003.tb02450.x
13. Jergens AE, Evans RB, Ackermann M, Hostetter J, Willard M, Mansell J, Bilzer T, Wilcock B, Washabau R, Hall EJ, Minami T, Wang C, Day MJ. Design of a simplified histopathologic model for gastrointestinal inflammation in dogs. Vet Pathol 2014; 51:946-50; PMID:24280943; https://doi.org/10.1177/0300985813511123
14. Guard BC, Barr JW, Reddivari L, Klemashevich C, Jayaraman A, Steiner JM, Vanamala J, Suchodolski JS. Characterization of microbial dysbiosis and metabolomic changes in dogs with acute diarrhea. PLoS One 2015; 10:e0127259; PMID:26000959; https://doi.org/10.1371/journal.pone.0127259
15. Janeczko S, Atwater D, Bogel E, Greiter-Wilke A, Gerold A, Baumgart M, Bender H, McDonough PL, McDonough SP, Goldstein RE, Simpson KW. The relationship of mucosal bacteria to duodenal histopathology, cytokine mRNA, and clinical disease activity in cats with inflammatory bowel disease. Vet Microbiol 2008; 128:178-93; PMID:18054447; https://doi.org/10.1016/j.vetmic.2007.10.014
16. Jergens AE, Pressel M, Crandell J, Morrison JA, Sorden SD, Haynes J, Craven M, Baumgart M, Simpson KW. Fluorescence in situ hybridization confirms clearance of visible Helicobacter spp. associated with gastritis in dogs and cats. J Vet Intern Med 2009; 23:16-23; PMID:19175715; https://doi.org/10.1111/j.1939-1676.2008.0211.x
17. Priestnall SL, Wiinberg B, Spohr A, Neuhaus B, Kuffer M, Wiedmann M, Simpson KW. Evaluation of “Helicobacter heilmannii” subtypes in the gastric mucosas of cats and dogs. J Clin Microbiol 2004; 42:2144-51; PMID:15131182; https://doi.org/10.1128/JCM.42.5.2144-2151.2004
18. Franks AH, Harmsen HJ, Raangs GC, Jansen GJ, Schut F, Welling GW. Variations of bacterial populations in human feces measured by fluorescent in situ hybridization with group-specific 16S rRNA-targeted oligonucleotide probes. Appl Environ Microbiol 1998; 64:3336-45; PMID:9726880
19. Poulsen LK, Lan F, Kristensen CS, Hobolth P, Molin S, Krogfelt KA. Spatial distribution of Escherichia coli in the mouse large intestine inferred from rRNA in situ hybridization. Infect Immun 1994; 62:5191-4; PMID:7927805
20. Harmsen HJ, Gibson GR, Elfferich P, Raangs GC, Wildeboer-Veloo AC, Argaiz A, Roberfroid MB, Welling GW. Comparison of viable cell counts and fluorescence in situ hybridization using specific rRNA-based probes for the quantification of human fecal bacteria. FEMS Microbiol Lett 2000; 183:125-9; PMID:10650214; https://doi.org/10.1111/j.1574-6968.2000.tb08945.x
21. Garcia-Mazcorro JF, Dowd SE, Poulsen J, Steiner JM, Suchodolski JS. Abundance and short-term temporal variability of fecal microbiota in healthy dogs. MicrobiologyOpen 2012; 1:340-7; PMID:23170232; https://doi.org/10.1002/mbo3.36
22. Amann RI, Binder BJ, Olson RJ, Chisholm SW, Devereux R, Stahl DA. Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl Environ Microbiol 1990; 56:1919-25; PMID:2200342
23. Cassmann E, White R, Atherly T, Wang C, Sun Y, Khoda S, Mosher C, Ackermann M, Jergens A. Alterations of the ileal and colonic mucosal microbiota in canine chronic enteropathies. PLoS One 2016; 11:e0147321; PMID:26840462; https://doi.org/10.1371/journal.pone.0147321
24. Ruaux CG. Cobalamin in companion animals: Diagnostic marker, deficiency states and therapeutic implications. Vet J 2013; 196:145-152; PMID:23518469; https://doi.org/10.1016/j.tvjl.2013.01.025
25. Jonkers D, Stockbrugger R. Probiotics and inflammatory bowel disease. J R Soc Med 2003; 96:167-71; PMID:12668702; https://doi.org/10.1258/jrsm.96.4.167
26. Marteau P, Seksik P, Shanahan F. Manipulation of the bacterial flora in inflammatory bowel disease. Best Pract Res Clin Gastroenterol 2003; 17:47-61; PMID:12617882; https://doi.org/10.1053/bega.2002.0344
27. Sartor RB. Therapeutic manipulation of the enteric microflora in inflammatory bowel diseases: antibiotics, probiotics, and prebiotics. Gastroenterology 2004; 126:1620-33; PMID:15168372; https://doi.org/10.1053/j.gastro.2004.03.024
28. Bassaganya-Riera J, Viladomiu M, Pedragosa M, De Simone C, Carbo A, Shaykhutdinov R, Jobin C, Arthur JC, Corl BA, Vogel H, Storr M, Hontecillas R. Probiotic bacteria produce conjugated linoleic acid locally in the gut that targets macrophage PPAR gamma to suppress colitis. PLoS One 2012; 7:e31238; PMID:22363592; https://doi.org/10.1371/journal.pone.0031238
29. Uronis JM, Arthur JC, Keku T, Fodor A, Carroll IM, Cruz ML, Appleyard CB, Jobin C. Gut microbial diversity is reduced by the probiotic VSL#3 and correlates with decreased TNBS-induced colitis. Inflamm Bowel Dis 2011; 17:289-97; PMID:20564535; https://doi.org/10.1002/ibd.21366
30. Reiff C, Delday M, Rucklidge G, Reid M, Duncan G, Wohlgemuth S, Hörmannsperger G, Loh G, Blaut M, Collie-Duguid E, Haller D, Kelly D. Balancing inflammatory, lipid, and xenobiotic signaling pathways by VSL#3, a biotherapeutic agent, in the treatment of inflammatory bowel disease. Inflamm Bowel Dis 2009; 15:1721-36; PMID:19639558; https://doi.org/10.1002/ibd.20999
31. Bibiloni R, Fedorak RN, Tannock GW, Madsen KL, Gionchetti P, Campieri M, De Simone C, Sartor RB. VSL#3 probiotic-mixture induces remission in patients with active ulcerative colitis. Am J Gastroenterol 2005; 100:1539-46; PMID:15984978; https://doi.org/10.1111/j.1572-0241.2005.41794.x
32. Tursi A, Brandimarte G, Giorgetti GM, Forti G, Modeo ME, Gigliobianco A. Low-dose balsalazide plus a high-potency probiotic preparation is more effective than balsalazide alone or mesalazine in the treatment of acute mild-to-moderate ulcerative colitis. Med Sci Monit 2004; 10:Pi126-31; PMID:15507864
33. Gionchetti P, Rizzello F, Helwig U, Venturi A, Lammers KM, Brigidi P, Vitali B, Poggioli G, Miglioli M, Campieri M. Prophylaxis of pouchitis onset with probiotic therapy: a double-blind, placebo-controlled trial. Gastroenterology 2003; 124:1202-9; PMID:12730861; https://doi.org/10.1016/S0016-5085(03)00171-9
34. Floch MH. Recommendations for probiotic use in humans-a 2014 update. Pharmaceuticals (Basel) 2014; 7:999-1007; PMID:25310351; https://doi.org/10.3390/ph7100999
35. Verbeke KA, Boesmans L, Boets E. Modulating the microbiota in inflammatory bowel diseases: prebiotics, probiotics or faecal transplantation? Proc Nutr Soc 2014; 73:490-7; PMID:24969143; https://doi.org/10.1017/S0029665114000639
36. Scaldaferri F, Gerardi V, Lopetuso LR, Del Zompo F, Mangiola F, Boškoski I, Bruno G, Petito V, Laterza L, Cammarota G, Gaetani E, Sgambato A, Gasbarrini A. Gut microbial flora, prebiotics, and probiotics in IBD: their current usage and utility. Biomed Res Int 2013; 2013:435268; PMID:23991417; https://doi.org/10.1155/2013/435268
37. Sauter SN, Allenspach K, Gaschen F, Gröne A, Ontsouka E, Blum JW. Cytokine expression in an ex vivo culture system of duodenal samples from dogs with chronic enteropathies: modulation by probiotic bacteria. Domest Anim Endocrinol 2005; 29:605-22; PMID:15941645; https://doi.org/10.1016/j.domaniend.2005.04.006
38. Sauter SN, Benyacoub J, Allenspach K, Gaschen F, Ontsouka E, Reuteler G, Cavadini C, Knorr R, Blum JW. Effects of probiotic bacteria in dogs with food responsive diarrhoea treated with an elimination diet. J Anim Physiol Anim Nutrition 2006; 90:269-77; PMID:16867072; https://doi.org/10.1111/j.1439-0396.2005.00595.x
39. Simpson KW, Rishniw M, Bellosa M, Liotta J, Lucio A, Baumgart M, Czarnecki-Maulden G, Benyacoub J, Bowman D. Influence of Enterococcus faecium SF68 probiotic on giardiasis in dogs. J Vet Intern Med 2009; 23:476-81; PMID:19298607; https://doi.org/10.1111/j.1939-1676.2009.0283.x
40. Herstad HK, Nesheim BB, L'Abee-Lund T, Larsen S, Skancke E. Effects of a probiotic intervention in acute canine gastroenteritis–a controlled clinical trial. J Small Anim Pract 2010; 51:34-8; PMID:20137007; https://doi.org/10.1111/j.1748-5827.2009.00853.x
41. Schmitz S, Glanemann B, Garden OA, Brooks H, Chang YM, Werling D, Allenspach K. A prospective, randomized, blinded, placebo-controlled pilot study on the effect of Enterococcus faecium on clinical activity and intestinal gene expression in canine food-responsive chronic enteropathy. J Vet Intern Med 2015; 29:533-43; PMID:25776251; https://doi.org/10.1111/jvim.12563
42. Madsen K, Cornish A, Soper P, McKaigney C, Jijon H, Yachimec C, Doyle J, Jewell L, De Simone C. Probiotic bacteria enhance murine and human intestinal epithelial barrier function. Gastroenterology 2001; 121:580-91; PMID:11522742; https://doi.org/10.1053/gast.2001.27224
43. Honneffer JB, Minamoto Y, Suchodolski JS. Microbiota alterations in acute and chronic gastrointestinal inflammation of cats and dogs. World J Gastroenterol 2014; 20:16489-97; PMID:25469017; https://doi.org/10.3748/wjg.v20.i44.16489
44. Suchodolski JS, Xenoulis PG, Paddock CG, Steiner JM, Jergens AE. Molecular analysis of the bacterial microbiota in duodenal biopsies from dogs with idiopathic inflammatory bowel disease. Vet Microbiol 2010; 142:394-400; PMID:19959301; https://doi.org/10.1016/j.vetmic.2009.11.002
45. Allenspach K, House A, Smith K, McNeill FM, Hendricks A, Elson-Riggins J, Riddle A, Steiner JM, Werling D, Garden OA, et al. Evaluation of mucosal bacteria and histopathology, clinical disease activity and expression of Toll-like receptors in German shepherd dogs with chronic enteropathies. Vet Microbiol 2010; 146:326-35; PMID:20615633; https://doi.org/10.1016/j.vetmic.2010.05.025
46. Suchodolski JS, Markel ME, Garcia-Mazcorro JF, Unterer S, Heilmann RM, Dowd SE, Kachroo P, Ivanov I, Minamoto Y, Dillman EM, Steiner JM, Cook AK, Toresson L. The fecal microbiome in dogs with acute diarrhea and idiopathic inflammatory bowel disease. PLoS One 2012; 7:e51907; PMID:23300577; https://doi.org/10.1371/journal.pone.0051907
47. Hostutler RA, Luria BJ, Johnson SE, Weisbrode SE, Sherding RG, Jaeger JQ, Guilford WG. Antibiotic-responsive histiocytic ulcerative colitis in 9 dogs. J Vet Intern Med 2004; 18:499-504; PMID:15320587; https://doi.org/10.1111/j.1939-1676.2004.tb02574.x
48. Mansfield CS, James FE, Craven M, Davies DR, O'Hara AJ, Nicholls PK, Dogan B, MacDonough SP, Simpson KW. Remission of histiocytic ulcerative colitis in Boxer dogs correlates with eradication of invasive intramucosal Escherichia coli. J Vet Int Med 2009; 23:964-9; PMID:19678891; https://doi.org/10.1111/j.1939-1676.2009.0363.x
49. Arthur JC, Gharaibeh RZ, Uronis JM, Perez-Chanona E, Sha W, Tomkovich S, Mühlbauer M, Fodor AA, Jobin C. VSL#3 probiotic modifies mucosal microbial composition but does not reduce colitis-associated colorectal cancer. Sci Rep 2013; 3:2868; PMID:24100376; https://doi.org/10.1038/srep02868
50. Mennigen R, Nolte K, Rijcken E, Utech M, Loeffler B, Senninger N, Bruewer M. Probiotic mixture VSL#3 protects the epithelial barrier by maintaining tight junction protein expression and preventing apoptosis in a murine model of colitis. Am J Physiol Gastrointest Liver Physiol 2009; 296:G1140-9; PMID:19221015; https://doi.org/10.1152/ajpgi.90534.2008
51. Corridoni D, Pastorelli L, Mattioli B, Locovei S, Ishikawa D, Arseneau KO, Chieppa M, Cominelli F, Pizarro TT. Probiotic bacteria regulate intestinal epithelial permeability in experimental ileitis by a TNF-dependent mechanism. PLoS One 2012; 7:e42067; PMID:22848704; https://doi.org/10.1371/journal.pone.0042067
52. Jergens AE, Simpson KW. Inflammatory bowel disease in veterinary medicine. Front Biosci (Elite edition) 2012; 4:1404-19; PMID:22201965; https://doi.org/10.2741/e470
53. Harrell L, Wang Y, Antonopoulos D, Young V, Lichtenstein L, Huang Y, Hanauer S, Chang E. Standard colonic lavage alters the natural state of mucosal-associated microbiota in the human colon. PLoS One 2012; 7:e32545; PMID:22389708; https://doi.org/10.1371/journal.pone.0032545
54. Swidsinski A, Loening-Baucke V, Theissig F, Engelhardt H, Bengmark S, Koch S, Lochs H, Dörffel Y. Comparative study of the intestinal mucus barrier in normal and inflamed colon. Gut 2007; 56:343-50; PMID:16908512; https://doi.org/10.1136/gut.2006.098160
55. Minamoto Y, Otoni CC, Steelman SM, Büyükleblebici O, Steiner JM, Jergens AE, Suchodolski JS. Alteration of the fecal microbiota and serum metabolite profiles in dogs with idiopathic inflammatory bowel disease. Gut Microbes 2015; 6:33-47; PMID:25531678; https://doi.org/10.1080/19490976.2014.997612