861
Views
0
CrossRef citations to date
0
Altmetric
Research Article

Large intestinal nutritional and physicochemical parameters from different dog sizes reshape canine microbiota structure and functions in vitro

ORCID Icon, , , , ORCID Icon, & ORCID Icon show all
Article: 2325713 | Received 07 Dec 2023, Accepted 21 Feb 2024, Published online: 12 Mar 2024

References

  • Hooda S, Minamoto Y, Suchodolski JS, et al. Current state of knowledge: the canine gastrointestinal microbiome. Anim Health Res Rev. 2012;13(1):78–21. doi: 10.1017/S1466252312000059
  • Honneffer JB, Steiner JM, Lidbury JA, et al. Variation of the microbiota and metabolome along the canine gastrointestinal tract. Metabolomics. 2017;13(3):26. doi:10.1007/s11306-017-1165-3
  • Cassmann E, White R, Atherly T, et al. Alterations of the ileal and colonic mucosal microbiota in canine chronic enteropathies. PloS One. 2016;11(2):e0147321. doi: 10.1371/journal.pone.0147321
  • Dubbelboer IR, Barmpatsalou V, Rodler A, et al. Gastrointestinal mucus in dog: physiological characteristics, composition, and structural properties. Eur J Pharm Biopharm. 2022;S0939-6411(22):00040–6. doi: 10.1016/j.ejpb.2022.02.019
  • Simpson KW, Dogan B, Rishniw M, et al. Adherent and invasive Escherichia coli is associated with granulomatous colitis in boxer dogs. Infect Immun. 2006;74(8):4778–4792. doi: 10.1128/IAI.00067-06
  • Blake AB, Suchodolski JS. Importance of gut microbiota for the health and disease of dogs and cats. Animal Front. 2016;6(3):37–42. doi: 10.2527/af.2016-0032
  • Kakimoto T, Kanemoto H, Fukushima K, et al. Effect of a high-fat–high-cholesterol diet on gallbladder bile acid composition and gallbladder motility in dogs. Am J Vet Res. 2017;78(12):1406–1413. doi: 10.2460/ajvr.78.12.1406
  • Deschamps C, Humbert D, Zentek J, et al. From Chihuahua to Saint-Bernard: how did digestion and microbiota evolve with dog sizes. Int J Biol Sci. 2022b;18(13):5086–5102. doi: 10.7150/ijbs.72770
  • Bjarnason I, MacPherson A, Hollander D. Intestinal permeability: an overview. Gastroenterology. 1995;108(5):1566–1581. doi: 10.1016/0016-5085(95)90708-4
  • Weber MP, Biourge VC, Nguyen PG. Digestive sensitivity varies according to size of dogs: a review. J Anim Physiol Anim Nutr (Berl). 2017;101(1):1–9. doi: 10.1111/jpn.12507
  • Weber MP, Hernot D, Nguyen PG, et al. Effect of size on electrolyte apparent absorption rates and fermentative activity in dogs. J Anim Physiol Anim Nutr (Berl). 2004;88(9–10):356–365. doi:10.1111/j.1439-0396.2004.00494.x
  • Weber MP, Martin LJ, Dumon HJ, et al. Influence of age and body size on intestinal permeability and absorption in healthy dogs. Am J Vet Res. 2002a;63(9):1323–1328. doi: 10.2460/ajvr.2002.63.1323
  • Weber MP, Stambouli F, Martin LJ, et al. Influence of age and body size on gastrointestinal transit time of radiopaque markers in healthy dogs. Am J Vet Res. 2002b;63(5):677–682. doi: 10.2460/ajvr.2002.63.677
  • Zentek J, Meyer H. Normal handling of diets–are all dogs created equal? J Small Anim Pract. 1995;36(8):354–359. doi: 10.1111/j.1748-5827.1995.tb02949.x
  • Alexander C, Guard BC, Suchodolski JS, et al. Cholestyramine decreases apparent total tract macronutrient digestibility and alters fecal characteristics and metabolites of healthy adult dogs. J Anim Sci. 2019;97(3):1020–1026. doi:10.1093/jas/sky437
  • Beloshapka AN, Alexander LG, Buff PR, et al. The effects of feeding resistant starch on apparent total tract macronutrient digestibility, faecal characteristics and faecal fermentative end-products in healthy adult dogs. J Nutr Sci. 2014;3:e38. doi: 10.1017/jns.2014.28
  • Beloshapka AN, Wolff AK, Swanson KS. Effects of feeding polydextrose on faecal characteristics, microbiota and fermentative end products in healthy adult dogs. Br J Nutr. 2012;108(4):638–644. doi: 10.1017/S0007114511005927
  • Detweiler KB, He F, Mangian HF, et al. Effects of high inclusion of soybean hulls on apparent total tract macronutrient digestibility, fecal quality, and fecal fermentative end-product concentrations in extruded diets of adult dogs. J Anim Sci. 2019;97(3):1027–1035. doi: 10.1093/jas/skz015
  • Goudez R, Weber M, Biourge V, et al. Influence of different levels and sources of resistant starch on faecal quality of dogs of various body sizes. Br J Nutr. 2011;106(Suppl S1):SS211–S215. doi: 10.1017/S0007114511003345
  • Nogueira JPDS, He F, Mangian HF, et al. Dietary supplementation of a fiber-prebiotic and saccharin-eugenol blend in extruded diets fed to dogs. J Anim Sci. 2019;97(11):4519–4531. doi:10.1093/jas/skz293
  • Guard BC, Honneffer JB, Jergens AE, et al. Longitudinal assessment of microbial dysbiosis, fecal unconjugated bile acid concentrations, and disease activity in dogs with steroid-responsive chronic inflammatory enteropathy. J Vet Intern Med. 2019;33(3):1295–1305. doi:10.1111/jvim.15493
  • 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(3):567–578. doi: 10.1111/j.1574-6941.2008.00521.x
  • Deschamps C, Denis S, Humbert D, et al. In vitro models of the canine digestive tract as an alternative to in vivo assays: Advances and current challenges. ALTEX. 2022a;39:235–257. doi: 10.14573/altex.2109011
  • Russel WMS, Burch RL. The principles of humane experimental technique. 1959.
  • Van den Abbeele P, Moens F, Pignataro G, et al. Yeast-derived formulations are differentially fermented by the canine and feline microbiome as assessed in a novel in vitro colonic fermentation model. J Agric Food Chem. 2020;68(46):13102–13110. doi: 10.1021/acs.jafc.9b05085
  • Deschamps C, Denis S, Humbert D, et al. Canine Mucosal Artificial Colon: development of a new colonic in vitro model adapted to dog sizes. Appl Microbiol Biotechnol. 2024;108(1):166. doi:10.1007/s00253-023-12987-2
  • Deschamps C, Fournier E, Uriot O, et al. Comparative methods for fecal sample storage to preserve gut microbial structure and function in an in vitro model of the human colon. Appl Microbiol Biotechnol. 2020;104(23):10233–10247. doi:10.1007/s00253-020-10959-4
  • Yu Y, Lee C, Kim J, et al. Group-specific primer and probe sets to detect methanogenic communities using quantitative real-time polymerase chain reaction. Biotechnol Bioeng. 2005;89(6):670–679. doi: 10.1002/bit.20347
  • Theil S, Rifa E. rANOMALY: AmplicoN wOrkflow for microbial community AnaLYsis. F1000Res. 2021;10:7. doi: 10.12688/f1000research.27268.1
  • Callahan BJ, McMurdie PJ, Rosen MJ, et al. DADA2: High-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13(7):581–583. doi: 10.1038/nmeth.3869
  • Murali A, Bhargava A, Wright ES. IDTAXA: a novel approach for accurate taxonomic classification of microbiome sequences. Microbiome. 2018;6(1):140. doi: 10.1186/s40168-018-0521-5
  • Quast C, Pruesse E, Yilmaz P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41(D1):D590–D596. doi: 10.1093/nar/gks1219
  • Parks DH, Chuvochina M, Rinke C, et al. GTDB: an ongoing census of bacterial and archaeal diversity through a phylogenetically consistent, rank normalized and complete genome-based taxonomy. Nucleic Acids Res. 2022;50(D1):D785–D794. doi:10.1093/nar/gkab776
  • Lê Cao K-A, González I, Déjean S. integrOmics: an R package to unravel relationships between two omics datasets. Bioinformatics. 2009;25(21):2855–2856. doi: 10.1093/bioinformatics/btp515
  • Liu C, Cui Y, Li X, et al. microeco: an R package for data mining in microbial community ecology. FEMS Microbiol Ecol. 2021;97(2):fiaa255. doi:10.1093/femsec/fiaa255
  • Algya KM, Cross T-W, Leuck KN, et al. Apparent total-tract macronutrient digestibility, serum chemistry, urinalysis, and fecal characteristics, metabolites and microbiota of adult dogs fed extruded, mildly cooked, and raw diets1. J Anim Sci. 2018;96(9):3670–3683. doi: 10.1093/jas/sky235
  • Case L, Carey D, Hirakawa D, et al. Canine and feline nutrition : a resource for companion animal professionals. Amsterdam, The Netherlands: Elsevier; 2011.
  • Flickinger EA, Schreijen EMWC, Patil AR, et al. Nutrient digestibilities, microbial populations, and protein catabolites as affected by fructan supplementation of dog diets. J Anim Sci. 2003;81:2008–2018. doi: 10.2527/2003.8182008x
  • Gazzola KM, Nelson LL, Fritz MC, et al. Effects of prophylactic incisional gastropexy on markers of gastric motility in dogs as determined by use of a novel wireless motility device. Am J Vet Res. 2017;78(1):100–106. doi: 10.2460/ajvr.78.1.100
  • Hendriks WH, Thomas DG, Bosch G, et al. Comparison of ileal and total tract nutrient digestibility of dry dog foods. J Anim Sci. 2013;91(8):3807–3814. doi:10.2527/jas.2012-5864
  • Koziolek M, Grimm M, Bollmann T, et al. Characterization of the GI transit conditions in Beagle dogs with a telemetric motility capsule. Eur J Pharm Biopharm. 2019;136:221–230. doi: 10.1016/j.ejpb.2019.01.026
  • Hang I, Heilmann RM, Grützner N, et al. Impact of diets with a high content of greaves-meal protein or carbohydrates on faecal characteristics, volatile fatty acids and faecal calprotectin concentrations in healthy dogs. BMC Vet Res. 2013;9(1):201. doi: 10.1186/1746-6148-9-201
  • Hang I, Rinttila T, Zentek J, et al. Effect of high contents of dietary animal-derived protein or carbohydrates on canine faecal microbiota. BMC Vet Res. 2012;8(1):90. doi: 10.1186/1746-6148-8-90
  • Pilla R, Suchodolski JS. The role of the canine gut microbiome and metabolome in health and gastrointestinal disease. Front Vet Sci. 2020;6:498. doi: 10.3389/fvets.2019.00498
  • Maria APJ, Ayane L, Putarov TC, et al. The effect of age and carbohydrate and protein sources on digestibility, fecal microbiota, fermentation products, fecal IgA, and immunological blood parameters in dogs 1,2. J Anim Sci. 2017;95(6):2452–2466. doi: 10.2527/jas.2016.1302
  • Middelbos IS, Vester Boler BM, Qu A, et al. Phylogenetic characterization of fecal microbial communities of dogs fed diets with or without supplemental dietary fiber using 454 pyrosequencing. PloS One. 2010;5(3):e9768. doi: 10.1371/journal.pone.0009768
  • Swanson KS, Dowd SE, Suchodolski JS, et al. Phylogenetic and gene-centric metagenomics of the canine intestinal microbiome reveals similarities with humans and mice. Isme J. 2011;5(4):639–649. doi:10.1038/ismej.2010.162
  • Oliphant K, Allen-Vercoe E. Macronutrient metabolism by the human gut microbiome: major fermentation by-products and their impact on host health. Microbiome. 2019;7(1):91. doi: 10.1186/s40168-019-0704-8
  • Larabi AB, Masson HLP, Bäumler AJ. Bile acids as modulators of gut microbiota composition and function. Gut Microbes. 2023;15(1):2172671. doi: 10.1080/19490976.2023.2172671
  • Suchodolski JS. Intestinal microbiota of dogs and cats: a bigger world than we thought. Vet Clin North Am Small Anim Pract. 2011;41(2):261–272. doi: 10.1016/j.cvsm.2010.12.006
  • Jia J, Frantz N, Khoo C, et al. Investigation of â??the faecal microbiota associated with canine chronic diarrhoea. FEMS Microbiology Ecology. 2010;71(2):304–312. doi: 10.1111/j.1574-6941.2009.00812.x
  • Kashyap PC, Marcobal A, Ursell LK, et al. Complex interactions among diet, gastrointestinal transit, and gut microbiota in humanized mice. Gastroenterology. 2013;144(5):967–977. doi: 10.1053/j.gastro.2013.01.047
  • Tottey W, Feria-Gervasio D, Gaci N, et al. Colonic transit time is a driven force of the gut microbiota composition and metabolism: In Vitro evidence. J Neurogastroenterol Motil. 2017;23(1):124–134. doi:10.5056/jnm16042
  • Pham VT, Chassard C, Rifa E, et al. Lactate metabolism is strongly modulated by fecal inoculum, pH, and retention time in PolyFermS continuous colonic fermentation models mimicking young infant proximal colon. mSystems. 2019;4(4):e00264–18. doi: 10.1128/mSystems.00264-18
  • Asnicar F, Leeming ER, Dimidi E, et al. Blue poo: impact of gut transit time on the gut microbiome using a novel marker. Gut. 2021;70(9):1665–1674. doi: 10.1136/gutjnl-2020-323877
  • Haindl R, Schick S, Kulozik U. Influence of cultivation pH on composition, diversity, and metabolic production in an in vitro human intestinal microbiota. Fermentation. 2021;7(3):156. doi: 10.3390/fermentation7030156
  • Nejati S, Wang J, Sedaghat S, et al. Smart capsule for targeted proximal colon microbiome sampling. Acta Biomaterialia. 2022;154:83–96. doi: 10.1016/j.actbio.2022.09.050
  • Beaumont M, Cauquil L, Bertide A, et al. Gut microbiota-derived metabolite signature in suckling and weaned piglets. J Proteome Res. 2021;20(1):982–994. doi: 10.1021/acs.jproteome.0c00745
  • Deschamps C, Humbert D, Zentek J, et al. From Chihuahua to Saint-Bernard: how did digestion and microbiota evolve with dog sizes. Int J Biol Sci. 2022c;18(13):5086–5102. doi: 10.7150/ijbs.72770
  • Kim J, An J-U, Kim W, et al. Differences in the gut microbiota of dogs (Canis lupus familiaris) fed a natural diet or a commercial feed revealed by the Illumina MiSeq platform. Gut Pathogens. 2017;9. doi: 10.1186/s13099-017-0218-5
  • Omatsu T, Omura M, Katayama Y, et al. Molecular diversity of the faecal microbiota of Toy Poodles in Japan. J Vet Med Sci. 2018;80:749–754. doi: 10.1292/jvms.17-0582
  • You I, Kim MJ. Comparison of Gut Microbiota of 96 Healthy Dogs by Individual Traits: Breed, Age, and Body Condition Score. Animals. 2021;11:2432. doi: 10.3390/ani11082432
  • Garcia-Mazcorro JF, Minamoto Y, Kawas JR, et al. Akkermansia and Microbial Degradation of Mucus in Cats and Dogs: Implications to the Growing Worldwide Epidemic of Pet Obesity. Vet Sci. 2020;7(2):44. doi: 10.3390/vetsci7020044
  • Kubinyi E, Bel Rhali S, Sándor S, et al. Gut Microbiome Composition is Associated with Age and Memory Performance in Pet Dogs. Animals (Basel). 2020;10:E1488. doi: 10.3390/ani10091488
  • Paßlack N, Kohn B, Vahjen W, et al. Effects of dietary cellobiose on the intestinal microbiota and excretion of nitrogen metabolites in healthy adult dogs. J Anim Physiol Anim Nutr (Berl). 2021. doi: 10.1111/jpn.13485
  • Sandri M, Dal Monego S, Conte G, et al. Raw meat based diet influences faecal microbiome and end products of fermentation in healthy dogs. BMC Vet Res 2016;13. doi: 10.1186/s12917-017-0981-z
  • Hullar MAJ, Lampe JW, Torok-Storb BJ, et al. The canine gut microbiome is associated with higher risk of gastric dilatation-volvulus and high risk genetic variants of the immune system. PLoS One. 2018;131. doi: 10.1371/journal.pone.0197686
  • Warrit K, Boscan P, Ferguson LE, et al. Effect of hospitalization on gastrointestinal motility and pH in dogs. Journal of the American Veterinary Medical Association 2017;251:65–70. doi: 10.2460/javma.251.1.65