#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Altered microbiota, fecal lactate, and fecal bile acids in dogs with gastrointestinal disease


Autoři: Amanda B. Blake aff001;  Blake C. Guard aff001;  Julia B. Honneffer aff001;  Jonathan A. Lidbury aff001;  Jörg M. Steiner aff001;  Jan S. Suchodolski aff001
Působiště autorů: Gastrointestinal Laboratory, Texas A&M University, Texas, United States of America aff001
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0224454

Souhrn

The intestinal microbiota plays an important role in health and disease and produces, through fermentative reactions, several metabolic products, such as lactate, that can affect the host. The microbiota also interacts with and metabolizes compounds produced by the host, such as primary bile acids. Lactate and bile acids (BA) are of particular interest in gastrointestinal diseases because they have been associated with metabolic acidosis and bile acid diarrhea, respectively. The objectives of this study were to validate an enzymatic assay to quantify D-, L-, and total lactate in canine feces, and to characterize fecal lactate and BA concentrations as well as bacterial abundances in healthy dogs and dogs with gastrointestinal diseases. Fecal samples were collected from 34 healthy dogs, 15 dogs with chronic enteropathy (CE), and 36 dogs with exocrine pancreatic insufficiency (EPI). Lactate was quantified with an enzymatic assay, BA with gas chromatography-mass spectrometry, and 11 bacterial groups with qPCR. A fecal lactate reference interval was established from 34 healthy dogs and was 0.7–1.4 mM, 0.3–6.0 mM, and 1.0–7.0 mM for D-, L-, and total lactate, respectively. The assay to measure D-, L-, and total lactate in canine fecal samples was linear, accurate, precise, and reproducible. Significant increases in fecal lactate and decreases in secondary BA concentrations were observed in dogs with CE and dogs with EPI. Dogs with EPI had an increased abundance of Escherichia coli, Lactobacillus, and Bifidobacterium; a decreased abundance of Fusobacterium and Clostridium hiranonis; and a higher Dysbiosis Index when compared to healthy dogs. Further studies are necessary to determine the clinical utility of lactate and BA quantification in canine feces. These metabolites suggest functional alterations of intestinal dysbiosis and may become promising targets for further elucidating the role of the microbiota in health and disease.

Klíčová slova:

Bacterial pathogens – Bile – Diet – Dogs – Enzyme assays – Gastrointestinal tract – Metabolites – Microbiome


Zdroje

1. Blake AB, Suchodolski JS. Importance of gut microbiota in the health and disease of dogs and cats. Animal Frontiers. 2016;6:37–42. doi: 10.2527/af.2016-0032

2. Suchodolski JS, Markel ME, Garcia-Mazcorro JF, Unterer S, Heilmann RM, Dowd SE, et al. The fecal microbiome in dogs with acute diarrhea and idiopathic inflammatory bowel disease. PLoS One. 2012;7(12):e51907. doi: 10.1371/journal.pone.0051907 23300577

3. Isaiah A, Parambeth JC, Steiner JM, Lidbury JA, Suchodolski JS. The fecal microbiome of dogs with exocrine pancreatic insufficiency. Anaerobe. 2017. doi: 10.1016/j.anaerobe.2017.02.010 28223257

4. 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(3):579–89. doi: 10.1111/j.1574-6941.2008.00556.x 18647355

5. Honneffer JB, Minamoto Y, Suchodolski JS. Microbiota alterations in acute and chronic gastrointestinal inflammation of cats and dogs. World J Gastroenterol. 2014;20(44):16489–97. doi: 10.3748/wjg.v20.i44.16489 25469017

6. AlShawaqfeh MK, Wajid B, Minamoto Y, Markel M, Lidbury JA, Steiner JM, et al. A dysbiosis index to assess microbial changes in fecal samples of dogs with chronic inflammatory enteropathy. FEMS Microbiol Ecol. 2017;93(11):fix136. doi: 10.1093/femsec/fix136 29040443

7. Suchodolski JS. Diagnosis and interpretation of intestinal dysbiosis in dogs and cats. Vet J. 2016;215:30–7. doi: 10.1016/j.tvjl.2016.04.011 27160005

8. Minamoto Y, Minamoto T, Isaiah A, Sattasathuchana P, Buono A, Rangachari VR, et al. Fecal short-chain fatty acid concentrations and dysbiosis in dogs with chronic enteropathy. J Vet Intern Med. 2019. doi: 10.1111/jvim.15520 31099928

9. Guard BC, Barr JW, Reddivari L, Klemashevich C, Jayaraman A, Steiner JM, et al. Characterization of microbial dysbiosis and metabolomic changes in dogs with acute diarrhea. PLoS One. 2015;10(5):e0127259. doi: 10.1371/journal.pone.0127259 26000959

10. Guard BC, Honneffer JB, Jergens AE, Jonika MM, Toresson L, Lawrence YA, 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):1295–305. doi: 10.1111/jvim.15493 30957301

11. Markel M, Berghoff N, Unterer S, Oliveira-Barros LM, Grellet A, Allenspach K, et al. Characterization of fecal dysbiosis in dogs with chronic enteropathies and acute hemorrhagic diarrhea. J Vet Intern Med. 2012;26(3):765–6. doi: 10.1111/j.1939-1676.2012.00937.x

12. Minamoto Y, Otoni CC, Steelman SM, Buyukleblebici O, Steiner JM, Jergens AE, et al. Alteration of the fecal microbiota and serum metabolite profiles in dogs with idiopathic inflammatory bowel disease. Gut microbes. 2015;6(1):33–47. doi: 10.1080/19490976.2014.997612 25531678

13. Langille MGI, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, et al. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol. 2013;31(9):814–21. doi: 10.1038/nbt.2676 23975157

14. Suchodolski JS. Companion animals symposium: microbes and gastrointestinal health of dogs and cats. Journal of animal science. 2011;89(5):1520–30. doi: 10.2527/jas.2010-3377 21075970

15. Roediger WE. Utilization of nutrients by isolated epithelial cells of the rat colon. Gastroenterology. 1982;83(2):424–9. 7084619

16. Morrison DJ, Preston T. Formation of short chain fatty acids by the gut microbiota and their impact on human metabolism. Gut microbes. 2016;0(0):1–12. doi: 10.1080/19490976.2015.1134082 26963409

17. Edwards CA, Duerden BI, Read NW. The effects of pH on colonic bacteria grown in continuous culture. Journal of medical microbiology. 1985;19(2):169–80. doi: 10.1099/00222615-19-2-169 3920398

18. Bustos D, Pons S, Pernas JC, Gonzalez H, Caldarini MI, Ogawa K, et al. Fecal lactate and short-bowel syndrome. Dig Dis Sci. 1994;39(11):2315–9. doi: 10.1007/bf02087644 7956597

19. Hove H, Mortensen PB. Colonic lactate metabolism and D-lactic acidosis. Dig Dis Sci. 1995;40(2):320–30. doi: 10.1007/bf02065417 7851197

20. Honneffer J, Guard B, Steiner JM, Suchodolski JS. Untargeted metabolomics reveals disruption within bile acid, cholesterol, and tryptophan metabolic pathways in dogs with idiopathic inflammatory bowel disease. Gastroenterology. 2015;148(4):S715–S.

21. Fall PJ, Szerlip HM. Lactic acidosis: from sour milk to septic shock. J Intensive Care Med. 2005;20:255–71. doi: 10.1177/0885066605278644 16145217

22. Thornalley PJ. The glyoxalase system in health and disease. Mol Aspects Med. 1993;14(4):287–371. doi: 10.1016/0098-2997(93)90002-U 8277832

23. Liu S-Q. Practical implications of lactate and pyruvate metabolism by lactic acid bacteria in food and beverage fermentations. Int J Food Microbiol. 2003;83(2):115–31. doi: 10.1016/s0168-1605(02)00366-5 12706034

24. Stiles ME, Holzapfel WH. Lactic acid bacteria of foods and their current taxonomy. Int J Food Microbiol. 1997;36:1–29. doi: 10.1016/s0168-1605(96)01233-0 9168311

25. Sheedy JR, Wettenhall RE, Scanlon D, Gooley PR, Lewis DP, McGregor N, et al. Increased d-lactic acid intestinal bacteria in patients with chronic fatigue syndrome. In Vivo. 2009;23(4):621–8. 19567398

26. Uribarri J, Oh MS, Carroll HJ. D-lactic acidosis: A review of clinical presentation, biochemical features, and pathophysiologic mechanisms. Medicine (Baltimore). 1998;77(2):73–82.

27. Swanson KS, Grieshop CM, Flickinger EA, Bauer LL, Chow J, Wolf BW, et al. Fructooligosaccharides and Lactobacillus acidophilus modify gut microbial populations, total tract nutrient digestibilities and fecal protein catabolite concentrations in healthy adult dogs. J Nutr. 2002;132(12):3721–31. doi: 10.1093/jn/132.12.3721 12468613

28. Gilliland SE. Health and nutritional benefits from lactic acid bacteria. FEMS Microbiol Rev. 1990;7(1–2):175–88. doi: 10.1111/j.1574-6968.1990.tb04887.x 2271223

29. Sharkey LC, Wellman ML. Use of lactate in small animal clinical practice. Clin Lab Med. 2015;35(3):567–77. doi: 10.1016/j.cll.2015.05.006 26297404

30. Ewaschuk JB, Naylor JM, Zello GA. D-lactate in human and ruminant metabolism. J Nutr. 2005;135(7):1619–25. doi: 10.1093/jn/135.7.1619 15987839

31. Kowlgi NG, Chhabra L. D-lactic acidosis: An underrecognized complication of short bowel syndrome. Gastroenterol Res Pract. 2015;2015:476215. doi: 10.1155/2015/476215 25977687

32. Lorenz I. Influence of D-lactate on metabolic acidosis and on prognosis in neonatal calves with diarrhoea. J Vet Med A. 2004;51(9–10):425–8. doi: 10.1111/j.1439-0442.2004.00662.x 15610486

33. Packer RA, Cohn LA, Wohlstadter DR, Shelton GD, Naylor JM, Zello GA, et al. D-lactic acidosis secondary to exocrine pancreatic insufficiency in a cat. J Vet Intern Med. 2005;19(1):106–10. doi: 10.1892/0891-6640(2005)19<106:dastep>2.0.co;2 15715057

34. Mayeur C, Gratadoux J-J, Bridonneau C, Chegdani F, Larroque B, Kapel N, et al. Faecal D/L lactate ratio is a metabolic signature of microbiota imbalance in patients with short bowel syndrome. PLos One. 2013;8(1):e54335. doi: 10.1371/journal.pone.0054335 23372709

35. Shimomura Y, Sato H. Fecal D- and L-lactate, succinate, and volatile fatty acid levels in young dairy calves. J Vet Med Sci. 2006;68(9):973–7. doi: 10.1292/jvms.68.973 17019068

36. Sato H, Koiwa M. Fecal D- and L-lactate, succinate and volatile fatty acid levels, and relationships with fecal acidity and diarrhea in neonatal calves. Anim Sci J. 2008;79(2):187–92. doi: 10.1111/j.1740-0929.2008.00516.x

37. Rul F, Ben-Yahia L, Chegdani F, Wrzosek L, Thomas S, Noordine M-L, et al. Impact of the metabolic activity of Streptococcus thermophilus on the colon epithelium of gnotobiotic rats. J Biol Chem. 2011;286(12):10288–96. doi: 10.1074/jbc.M110.168666 21239485

38. Russell DW, Setchell KD. Bile acid biosynthesis. Biochemistry. 1992;31(20):4737–49. doi: 10.1021/bi00135a001 1591235

39. Scott R, Strasberg S, El-Sharkawy T, Diamant N. Regulation of the fasting enterohepatic circulation of bile acids by the migrating myoelectric complex in dogs. J Clin Invest. 1983;71(3):644. doi: 10.1172/JCI110811 6826728

40. Ridlon JM, Kang D-J, Hylemon PB. Bile salt biotransformations by human intestinal bacteria. J Lipid Res. 2006;47(2):241–59. doi: 10.1194/jlr.R500013-JLR200 16299351

41. Greve JW, Gouma DJ, Buurman WA. Bile acids inhibit endotoxin‐induced release of tumor necrosis factor by monocytes: An in Vitro study. Hepatology. 1989;10(4):454–8. doi: 10.1002/hep.1840100409 2777206

42. Sun J, Mustafi R, Cerda S, Chumsangsri A, Xia YR, Li YC, et al. Lithocholic acid down-regulation of NF-κB activity through vitamin D receptor in colonic cancer cells. J Steroid Biochem Mol Biol. 2008;111(1):37–40. doi: 10.1016/j.jsbmb.2008.01.003 18515093

43. Wargovich MJ, Eng VW, Newmark HL, Bruce WR. Calcium ameliorates the toxic effect of deoxycholic acid on colonic epithelium. Carcinogenesis. 1983;4(9):1205–7. doi: 10.1093/carcin/4.9.1205 6883640

44. Ogawa A, Murate T, Suzuki M, Nimura Y, Yoshida S. Lithocholic acid, a putative tumor promoter, inhibits mammalian DNA polymerase β. Jpn J Clin Oncol. 1998;89(11):1154–9. doi: 10.1111/j.1349-7006.1998.tb00510.x 9914784

45. Batta AK, Salen G, Rapole KR, Batta M, Batta P, Alberts D, et al. Highly simplified method for gas-liquid chromatographic quantitation of bile acids and sterols in human stool. J Lipid Res. 1999;40(6):1148–54. 10357847

46. Batta AK, Salen G, Batta P, Tint GS, Alberts DS, Earnest DL. Simultaneous quantitation of fatty acids, sterols and bile acids in human stool by capillary gas-liquid chromatography. J Chromatogr B Analyt Technol Biomed Life Sci. 2002;775(2):153–61. doi: 10.1016/s1570-0232(02)00289-1 12113981

47. Belenguer A, Duncan SH, Holtrop G, Anderson SE, Lobley GE, Flint HJ. Impact of pH on lactate formation and utilization by human fecal microbial communities. Appl Environ Microbiol. 2007;73(20):6526–33. doi: 10.1128/AEM.00508-07 17766450

48. Nishiyama H, Nagai T, Kudo M, Okazaki Y, Azuma Y, Watanabe T, et al. Supplementation of pancreatic digestive enzymes alters the composition of intestinal microbiota in mice. Biochem Biophys Res Commun. 2018;495(1):273–9. doi: 10.1016/j.bbrc.2017.10.130 29106956

49. Giaretta PR, Rech RR, Guard BC, Blake AB, Blick AK, Steiner JM, et al. Comparison of intestinal expression of the apical sodium-dependent bile acid transporter between dogs with and without chronic inflammatory enteropathy. J Vet Intern Med. 2018;32(6):1918–26. doi: 10.1111/jvim.15332 30315593

50. Pereira GQ, Gomes LA, Santos IS, Alfieri AF, Weese JS, Costa MC. Fecal microbiota transplantation in puppies with canine parvovirus infection. J Vet Intern Med. 2018;32(2):707–11. doi: 10.1111/jvim.15072 29460302

51. D’Angelo S, Fracassi F, Bresciani F, Galuppi R, Diana A, Linta N, et al. Effect of Saccharomyces boulardii in dogs with chronic enteropathies: double-blinded, placebo-controlled study. The Veterinary record. 2018;182(9):258. doi: 10.1136/vr.104241 29212912

52. Gómez-Gallego C, Junnila J, Männikkö S, Hämeenoja P, Valtonen E, Salminen S, et al. A canine-specific probiotic product in treating acute or intermittent diarrhea in dogs: A double-blind placebo-controlled efficacy study. Vet Microbiol. 2016;197:122–8. doi: 10.1016/j.vetmic.2016.11.015 27938673

53. Kelley RL, Minikhiem D, Kiely B, O'Mahony L, O'Sullivan D, Boileau T, et al. Clinical benefits of probiotic canine-derived Bifidobacterium animalis strain AHC7 in dogs with acute idiopathic diarrhea. Veterinary therapeutics: research in applied veterinary medicine. 2009;10(3):121–30.

54. Rossi G, Pengo G, Caldin M, Piccionello AP, Steiner JM, Cohen ND, et al. 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(4):e94699. doi: 10.1371/journal.pone.0094699 24722235

55. White R, Atherly T, Guard B, Rossi G, Wang C, Mosher C, et al. Randomized, controlled trial evaluating the effect of multi-strain probiotic on the mucosal microbiota in canine idiopathic inflammatory bowel disease. Gut microbes. 2017;8(5):451–66. doi: 10.1080/19490976.2017.1334754 28678609

56. Schmidt M, Unterer S, Suchodolski JS, Honneffer JB, Guard BC, Lidbury JA, et al. The fecal microbiome and metabolome differs between dogs fed Bones and Raw Food (BARF) diets and dogs fed commercial diets. PLoS One. 2018;13(8):e0201279. doi: 10.1371/journal.pone.0201279 30110340

57. Li Q, Lauber CL, Czarnecki-Maulden G, Pan Y, Hannah SS. Effects of the dietary protein and carbohydrate ratio on gut microbiomes in dogs of different body conditions. mBio. 2017;8(1):e01703–16. doi: 10.1128/mBio.01703-16 28119466

58. Sandri M, Dal Monego S, Conte G, Sgorlon S, Stefanon B. Raw meat based diet influences faecal microbiome and end products of fermentation in healthy dogs. BMC Veterinary Research. 2017;13(1):65. doi: 10.1186/s12917-017-0981-z 28245817

59. Bresciani F, Minamoto Y, Suchodolski JS, Galiazzo G, Vecchiato CG, Pinna C, et al. Effect of an extruded animal protein-free diet on fecal microbiota of dogs with food-responsive enteropathy. J Vet Intern Med. 2018;32(6):1903–10. doi: 10.1111/jvim.15227 30353569

60. Pilla R, Guard BC, Steiner JM, Gaschen FP, Olson E, Werling D, et al. Administration of a synbiotic containing Enterococcus faecium does not significantly alter fecal microbiota richness or diversity in dogs with and without food-responsive chronic enteropathy. Front Vet Sci. 2019;6(277). doi: 10.3389/fvets.2019.00277 31552278

61. Doerner KC, Takamine F, LaVoie CP, Mallonee DH, Hylemon PB. Assessment of fecal bacteria with bile acid 7 alpha-dehydroxylating activity for the presence of bai-like genes. Appl Environ Microbiol. 1997;63(3):1185–8. 9055436

62. Duboc H, Rajca S, Rainteau D, Benarous D, Maubert M-A, Quervain E, et al. Connecting dysbiosis, bile-acid dysmetabolism and gut inflammation in inflammatory bowel diseases. Gut. 2013;62(4):531–9. doi: 10.1136/gutjnl-2012-302578 22993202

63. Williams A, Merrick M, Eastwood M. Idiopathic bile acid malabsorption—a review of clinical presentation, diagnosis, and response to treatment. Gut. 1991;32(9):1004–6. doi: 10.1136/gut.32.9.1004 1916479

64. Walters JR, Pattni SS. Managing bile acid diarrhoea. Therap Adv Gastroenterol. 2010;3(6):349–57. doi: 10.1177/1756283X10377126 21180614

65. Camilleri M, Nadeau A, Tremaine WJ, Lamsam J, Burton D, Odunsi S, et al. Measurement of serum 7α‐hydroxy‐4‐cholesten‐3‐one (or 7αC4), a surrogate test for bile acid malabsorption in health, ileal disease and irritable bowel syndrome using liquid chromatography‐tandem mass spectrometry. Neurogastroenterol Motil. 2009;21(7):734–e43. doi: 10.1111/j.1365-2982.2009.01288.x 19368662

66. Kent A, Cross G, Taylor D, Sherwood R, Watson P. Measurement of serum 7α-hydroxy-4-cholesten-3-one as a marker of bile acid malabsorption in dogs with chronic diarrhoea: a pilot study. Vet Rec Open. 2016;3(1):e000163. doi: 10.1136/vetreco-2015-000163 27110372


Článek vyšel v časopise

PLOS One


2019 Číslo 10
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

KOST
Koncepce osteologické péče pro gynekology a praktické lékaře
nový kurz
Autoři: MUDr. František Šenk

Sekvenční léčba schizofrenie
Autoři: MUDr. Jana Hořínková

Hypertenze a hypercholesterolémie – synergický efekt léčby
Autoři: prof. MUDr. Hana Rosolová, DrSc.

Svět praktické medicíny 5/2023 (znalostní test z časopisu)

Imunopatologie? … a co my s tím???
Autoři: doc. MUDr. Helena Lahoda Brodská, Ph.D.

Všechny kurzy
Kurzy Podcasty Doporučená témata Časopisy
Přihlášení
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

#ADS_BOTTOM_SCRIPTS#