Urinary Metabolites of Green Tea as Potential Markers of Colonization Resistance to Pathogenic Gut Bacteria in Mice

Mark E. Obrenovich, George Eugene Jaskiw, Thriveen Sankar Chittoor Mana, Christina P. Bennett, Jennifer Cadnum Cadnum, Curtis J. Donskey

Abstract


Background: The gut microbiome (GMB) generates numerous chemicals that are absorbed systemically and excreted in urine. Antibiotics can disrupt the GMB ecosystem and weaken its resistance to colonization by enteric pathogens such as Clostridium difficile. If the changes in GMB composition and metabolism are sufficiently large, they can be reflected in the urinary metabolome. Characterizing these changes could provide a potentially valuable biomarker of the status of the GMB. While preliminary studies suggest such a possibility, the high level of data variance presents a challenge to translational applications. Since many GMB-generated chemicals are derived from the biotransformation of plant-derived dietary polyphenols, administering an oral precursor challenge should amplify GMB-dependent changes in urinary metabolites.

Methods: A course of antibiotics (clindamycin, piperacillin/tazobactam, or aztreonam) was administered SC daily (days 1 and 2) to mice receiving polyphenol-rich green tea in drinking water. Urine was collected at baseline as well as days 3, 7, and 11. Levels of pyrogallol and pyrocatechol, two phenolic molecules unequivocally GMB-dependent in man but that had not been similarly examined in mice, were quantified.

Results: In confirmation of our hypothesis, differential changes in murine urinary pyrogallol levels identified the treatments (clindamycin, piperacillin/tazobactam) previously associated with a weakening of colonization resistance to Clostridium difficile. The changes in pyrocatechol levels did not withstand corrections for multiple comparisons.

Conclusions: In the mouse, urinary pyrogallol and, in all likelihood, pyrocatechol levels, are GMB-dependent and, in combination with precursor challenge, deserve further consideration as potential metabolomic biomarkers for the health and dysbiotic vulnerability of the GMB.


Keywords


microbiota, anaerobes, mice, clindamycin, aztreonam, piperacillin/tazobactam, polyphenols

Full Text:

HTML PDF

References


1. Kamada N, Chen GY, Inohara N, Nunez G. Control of pathogens and pathobionts by the gut microbiota. Nature Immunology. 2013;14(7):685-90. PubMed PMID: 23778796. Pubmed Central PMCID: PMC4083503. doi: 10.1038/ni.2608

2. Baumler AJ, Sperandio V. Interactions between the microbiota and pathogenic bacteria in the gut. Nature. 2016;535(7610):85-93. PubMed PMID: 27383983. Pubmed Central PMCID: PMC5114849. doi: 10.1038/nature18849

3. Pultz NJ, Donskey CJ. Effect of antibiotic treatment on growth of and toxin production by Clostridium difficile in the cecal contents of mice. Antimicrobial Agents and Chemotherapy. 2005;49(8):3529-32. PubMed PMID: 16048976. Pubmed Central PMCID: PMC1196291. doi: 10.1128/AAC.49.8.3529-3532.2005

4. Pultz NJ, Stiefel U, Subramanyan S, Helfand MS, Donskey CJ. Mechanisms by which anaerobic microbiota inhibit the establishment in mice of intestinal colonization by vancomycin-resistant Enterococcus. Journal of Infectious Diseases. 2005;191(6):949-56. PubMed PMID: 15717271. doi: 10.1086/428090

5. Jump RL, Polinkovsky A, Hurless K, Sitzlar B, Eckart K, Tomas M, Deshpande A, Nerandzic MM, Donskey CJ. Metabolomics analysis identifies intestinal microbiota-derived biomarkers of colonization resistance in clindamycin-treated mice. PloS One. 2014;9(7):e101267. PubMed PMID: 24988418. Pubmed Central PMCID: PMC4079339. doi: 10.1371/journal.pone.0101267

6. Deshpande A, Pant C, Olyaee M, Donskey CJ. Hospital readmissions related to Clostridium difficile infection in the United States. American Journal of Infection Control. 2018;46(3):346-7. PubMed PMID: 29050906. doi: 10.1016/j.ajic.2017.08.043

7. Wikoff WR, Anfora AT, Liu J, Schultz PG, Lesley SA, Peters EC, Siuzdak G. Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites. Proceedings of the National Academy of Sciences of the United States of America. 2009;106(10):3698-703. PubMed PMID: 19234110. Pubmed Central PMCID: PMC2656143. doi: 10.1073/pnas.0812874106

8. Collins SM, Surette M, Bercik P. The interplay between the intestinal microbiota and the brain. Nature Reviews: Microbiology. 2012;10(11):735-42. PubMed PMID: 23000955. doi: 10.1038/nrmicro2876

9. Wishart DS, Feunang YD, Marcu A, Guo AC, Liang K, Vazquez-Fresno R, Sajed T, Johnson D, Li C, Karu N, Sayeeda Z, Lo E, Assempour N, Berjanskii M, Singhal S, Arndt D, Liang Y, Badran H, Grant J, Serra-Cayuela A, Liu Y, Mandal R, Neveu V, Pon A, Knox C, Wilson M, Manach C, Scalbert A. HMDB 4.0: the human metabolome database for 2018. Nucleic Acids Research. 2018;46(D1):D608-D17. PubMed PMID: 29140435. Pubmed Central PMCID: PMC5753273. doi: 10.1093/nar/gkx1089

10. Obrenovich ME, Tima M, Polinkovsky A, Zhang R, Emancipator SN, Donskey CJ. Targeted Metabolomics Analysis Identifies Intestinal Microbiota-Derived Urinary Biomarkers of Colonization Resistance in Antibiotic-Treated Mice. Antimicrobial Agents and Chemotherapy. 2017;61(8):pii: e00477-17. PubMed PMID: 28584146. Pubmed Central PMCID: PMC5527637. doi: 10.1128/AAC.00477-17

11. Obrenovich ME, Jaskiw GE, Zhang R, Willard B, Donskey CJ. Identification and Quantification by Targeted Metabolomics of Antibiotic-Responsive Urinary Small Phenolic Molecules Derived from the Intestinal Microbiota in Mice. Pathogens and Immunity. 2019;4(1):85-103. doi: 10.20411/pai.v4i1.284

12. Roowi S, Stalmach A, Mullen W, Lean ME, Edwards CA, Crozier A. Green tea flavan-3-ols: colonic degradation and urinary excretion of catabolites by humans. Journal of Agricultural and Food Chemistry. 2010;58(2):1296-304. PubMed PMID: 20041649. doi: 10.1021/jf9032975

13. Kanehisa M, Furumichi M, Tanabe M, Sato Y, Morishima K. KEGG: new perspectives on genomes, pathways, diseases and drugs. Nucleic Acids Research. 2017;45(D1):D353-D61. PubMed PMID: 27899662. Pubmed Central PMCID: PMC5210567. doi: 10.1093/nar/gkw1092

14. Scheline RR. The decarboxylation of some phenolic acids by the rat. Acta Pharmacologica et Toxicologica. 1966;24(2):275-85. PubMed PMID: 6013094.

15. Zheng X, Xie G, Zhao A, Zhao L, Yao C, Chiu NH, Zhou Z, Bao Y, Jia W, Nicholson JK, Jia W. The footprints of gut microbial-mammalian co-metabolism. Journal of Proteome Research. 2011;10(12):5512-22. PubMed PMID: 21970572. doi: 10.1021/pr2007945

16. Wu WK, Chen CC, Liu PY, Panyod S, Liao BY, Chen PC, Kao HL, Kuo HC, Kuo CH, Chiu THT, Chen RA, Chuang HL, Huang YT, Zou HB, Hsu CC, Chang TY, Lin CL, Ho CT, Yu HT, Sheen LY, Wu MS. Identification of TMAO-producer phenotype and host-diet-gut dysbiosis by carnitine challenge test in human and germ-free mice. Gut. 2019;68(8):1439-49. PubMed PMID: 30377191. doi: 10.1136/gutjnl-2018-317155

17. Williamson G, Clifford MN. Role of the small intestine, colon and microbiota in determining the metabolic fate of polyphenols. Biochemical Pharmacology. 2017;139:24-39. PubMed PMID: 28322745. doi: 10.1016/j.bcp.2017.03.012

18. Kesli R, Gokcen C, Bulug U, Terzi Y. Investigation of the relation between anaerobic bacteria genus clostridium and late-onset autism etiology in children. J Immunoassay Immunochem. 2014;35(1):101-9.

19. Shaw W. Increased urinary excretion of a 3-(3-hydroxyphenyl)-3-hydroxypropionic acid (HPHPA), an abnormal phenylalanine metabolite of Clostridia spp. in the gastrointestinal tract, in urine samples from patients with autism and schizophrenia. Nutritional Neuroscience. 2010;13(3):135-43. PubMed PMID: 20423563. doi: 10.1179/147683010X12611460763968

20. Shaw W. Clostridia bacteria in the gastrointestinal tract as a major cause of depression and other neuropsychiatric disorders. In: Greenblatt J, Brogan K, editors. Integrative Psychiatry for Depression: Redefining Models for Assessment, Treatment, and Prevention of Mood Disorders. New York, NY: Taylor and Francis; 2016. p. 31-48.

21. Xiong X, Liu D, Wang Y, Zeng T, Peng Y. Urinary 3-(3-Hydroxyphenyl)-3-hydroxypropionic Acid, 3-Hydroxyphenylacetic Acid, and 3-Hydroxyhippuric Acid Are Elevated in Children with Autism Spectrum Disorders. Biomed Res Int. 2016;2016:9485412. PubMed PMID: 27123458. Pubmed Central PMCID: PMC4829699. doi: 10.1155/2016/9485412

22. Scalbert A, Williamson G. Dietary intake and bioavailability of polyphenols. Journal of Nutrition. 2000;130(8S Suppl):2073S-85S. PubMed PMID: 10917926. doi: 10.1093/jn/130.8.2073S

23. Borges G, Ottaviani JI, van der Hooft JJJ, Schroeter H, Crozier A. Absorption, metabolism, distribution and excretion of (-)-epicatechin: A review of recent findings. Molecular Aspects of Medicine. 2018;61:18-30. PubMed PMID: 29126853. doi: 10.1016/j.mam.2017.11.002

24. Chen HD, Sang SM. Biotransformation of tea polyphenols by gut microbiota. Journal of Functional Foods. 2014;7:26-42. PubMed PMID: WOS:000335203500003. doi: 10.1016/j.jff.2014.01.013

25. USDA Database for the Flavonoid Content of Selected Foods [Internet]. 2007. Available from: www.ars.usda.gov/ARSUserFiles/80400525/Data/Flav/Flav02-1.pdf.

26. Spencer JP. Metabolism of tea flavonoids in the gastrointestinal tract. Journal of Nutrition. 2003;133(10):3255S-61S. PubMed PMID: 14519823. doi: 10.1093/jn/133.10.3255S

27. Stalmach A, Mullen W, Steiling H, Williamson G, Lean ME, Crozier A. Absorption, metabolism, and excretion of green tea flavan-3-ols in humans with an ileostomy. Molecular Nutrition & Food Research. 2010;54(3):323-34. PubMed PMID: 19937856. doi: 10.1002/mnfr.200900194

28. Liu Z, Bruins ME, Ni L, Vincken JP. Green and Black Tea Phenolics: Bioavailability, Transformation by Colonic Microbiota, and Modulation of Colonic Microbiota. Journal of Agricultural and Food Chemistry. 2018;66(32):8469-77. PubMed PMID: 30020786. doi: 10.1021/acs.jafc.8b02233

29. Li C, Meng X, Winnik B, Lee MJ, Lu H, Sheng S, Buckley B, Yang CS. Analysis of urinary metabolites of tea catechins by liquid chromatography/electrospray ionization mass spectrometry. Chemical Research in Toxicology. 2001;14(6):702-7. PubMed PMID: 11409941.

30. Liu AB, Tao S, Lee MJ, Hu Q, Meng X, Lin Y, Yang CS. Effects of gut microbiota and time of treatment on tissue levels of green tea polyphenols in mice. Biofactors. 2018. PubMed PMID: 29740891. Pubmed Central PMCID: PMC6222019. doi: 10.1002/biof.1430

31. Madrid-Gambin F, Garcia-Aloy M, Vazquez-Fresno R, Vegas-Lozano E, Sanchez-Pla A, Misawa K, Hase T, Shimotoyodome A, Andres-Lacueva C. Metabolic Signature of a Functional High-Catechin Tea after Acute and Sustained Consumption in Healthy Volunteers through (1)H NMR Based Metabolomics Analysis of Urine. Journal of Agricultural and Food Chemistry. 2019;67(11):3118-24. PubMed PMID: 30574780. doi: 10.1021/acs.jafc.8b04198

32. Envigo. Teklad Global 18% Protein Extruded Rodent Diet (Sterilizable) 2018 [cited 2018 08/08/2018]. Diet composition]. Available from: www.envigo.com/resources/data-sheets/2018sx-datasheet-0915.pdf

33. Rutter, Sell, Fraser, Obrenovich, Zito, Starke-Reed, Monnier. Green Tea Extract Suppresses the Age-Related Increase in Collagen Crosslinking and Fluorescent Products in C57BL/6 Mice. International Journal for Vitamin and Nutrition Research. 2003;73(6):453-60. PubMed PMID: 14743550. doi: 10.1024/0300-9831.73.6.453

34. Khokhar S, Venema D, Hollman PC, Dekker M, Jongen W. A RP-HPLC method for the determination of tea catechins. Cancer Letters. 1997;114(1-2):171-2. PubMed PMID: 9103282. doi: 10.1016/s0304-3835(97)04653-3

35. Sysi-Aho M, Katajamaa M, Yetukuri L, Oresic M. Normalization method for metabolomics data using optimal selection of multiple internal standards. BMC Bioinformatics. 2007;8:93. PubMed PMID: 17362505. Pubmed Central PMCID: PMC1838434. doi: 10.1186/1471-2105-8-93

36. Meng X, Sang S, Zhu N, Lu H, Sheng S, Lee MJ, Ho CT, Yang CS. Identification and characterization of methylated and ring-fission metabolites of tea catechins formed in humans, mice, and rats. Chemical Research in Toxicology. 2002;15(8):1042-50. PubMed PMID: 12184788.

37. Donovan JL, Crespy V, Manach C, Morand C, Besson C, Scalbert A, Remesy C. Catechin is metabolized by both the small intestine and liver of rats. Journal of Nutrition. 2001;131(6):1753-7. PubMed PMID: 11385063. doi: 10.1093/jn/131.6.1753

38. Piskula MK, Terao J. Accumulation of (-)-epicatechin metabolites in rat plasma after oral administration and distribution of conjugation enzymes in rat tissues. Journal of Nutrition. 1998;128(7):1172-8. PubMed PMID: 9649602. doi: 10.1093/jn/128.7.1172

39. Shangari N, Chan TS, O'Brien PJ. Sulfation and glucuronidation of phenols: implications in coenyzme Q metabolism. Methods in Enzymology. 2005;400:342-59. PubMed PMID: 16399359. doi: 10.1016/S0076-6879(05)00020-0

40. Tourino S, Fuguet E, Vinardell MP, Cascante M, Torres JL. Phenolic metabolites of grape antioxidant dietary fiber in rat urine. Journal of Agricultural and Food Chemistry. 2009;57(23):11418-26. PubMed PMID: 19951002. doi: 10.1021/jf901972c

41. Shaw IC, Hackett AM, Griffiths LA. Metabolism and excretion of the liver-protective agent (+)-catechin in experimental hepatitis. Xenobiotica. 1982;12(7):405-16. PubMed PMID: 7147991.

42. Macfarlane GT, Cummings JH. The colonic flora, fermentation and large bowel digestive function. In: Phillips SF, Pemberton JH, Shorter RG, editors. The Large Intestine: Physiology, Pathophysiology and Disease. New York: Raven Press; 1991. p. 51-92.

43. Kuhnau J. The flavonoids. A class of semi-essential food components: their role in human nutrition. World Review of Nutrition and Dietetics. 1976;24:117-91. PubMed PMID: 790781.

44. Crozier A, Jaganath I, B., Clifford MN. Phenols, Polyphenols and Tannins: An Overview. In: Crozier A, Clifford MN, Ashihara H, editors. Plant Secondary Metabolites: Occurrence, Structure and Role in the Human Diet. Oxford, UK: Blackwell Publishing; 2006. p. 1-24.

45. Takagaki A, Kato Y, Nanjo F. Isolation and characterization of rat intestinal bacteria involved in biotransformation of (-)-epigallocatechin. Archives of Microbiology. 2014;196(10):681-95. PubMed PMID: 24947740. doi: 10.1007/s00203-014-1006-y

46. Das NP, Griffiths LA. Studies on flavonoid metabolism. Metabolism of (+)-[14C] catechin in the rat and guinea pig. Biochemical Journal. 1969;115(4):831-6. PubMed PMID: 5357023. Pubmed Central PMCID: PMC1185212. doi: 10.1042/bj1150831

47. Borges G, van der Hooft JJJ, Crozier A. A comprehensive evaluation of the [2-(14)C](-)-epicatechin metabolome in rats. Free Radical Biology and Medicine. 2016;99:128-38. PubMed PMID: 27495388. doi: 10.1016/j.freeradbiomed.2016.08.001

48. Ottaviani JI, Borges G, Momma TY, Spencer JP, Keen CL, Crozier A, Schroeter H. The metabolome of [2-(14)C](-)-epicatechin in humans: implications for the assessment of efficacy, safety, and mechanisms of action of polyphenolic bioactives. Scientific Reports. 2016;6:29034. PubMed PMID: 27363516. Pubmed Central PMCID: PMC4929566. doi: 10.1038/srep29034

49. Booth AN, Masri MS, Robbins DJ, Emerson OH, Jones FT, De Eds F. The metabolic fate of gallic acid and related compounds. Journal of Biological Chemistry. 1959;234:3014-6. PubMed PMID: 13802679.

50. Daglia M, Di Lorenzo A, Nabavi SF, Talas ZS, Nabavi SM. Polyphenols: well beyond the antioxidant capacity: gallic acid and related compounds as neuroprotective agents: you are what you eat! Current Pharmaceutical Biotechnology. 2014;15(4):362-72. PubMed PMID: 24938889.

51. Mandic AI, Dilas SM, Cetkovic GS, Canadanovic-Brunet JM, Tumbas VT. Polyphenolic Composition and Antioxidant Activities of Grape Seed Extract. International Journal of Food Properties. 2008;11(4):713-26. PubMed PMID: WOS:000261020200001. Pii 905635022. doi: 10.1080/10942910701584260

52. Del Bo C, Ciappellano S, Klimis-Zacas D, Martini D, Gardana C, Riso P, Porrini M. Anthocyanin absorption, metabolism, and distribution from a wild blueberry-enriched diet (Vaccinium angustifolium) is affected by diet duration in the Sprague-Dawley rat. Journal of Agricultural and Food Chemistry. 2010;58(4):2491-7. PubMed PMID: 20030330. doi: 10.1021/jf903472x

53. Abhijit S, Tripathi SJ, Bhagya V, Shankaranarayana Rao BS, Subramanyam MV, Asha Devi S. Antioxidant action of grape seed polyphenols and aerobic exercise in improving neuronal number in the hippocampus is associated with decrease in lipid peroxidation and hydrogen peroxide in adult and middle-aged rats. Experimental Gerontology. 2018;101:101-12. PubMed PMID: 29174497. doi: 10.1016/j.exger.2017.11.012

54. Vostalova J, Galandakova A, Palikova I, Ulrichova J, Dolezal D, Lichnovska R, Vrbkova J, Rajnochova Svobodova A. Lonicera caerulea fruits reduce UVA-induced damage in hairless mice. Journal of Photochemistry and Photobiology B: Biology. 2013;128:1-11. PubMed PMID: 23974431. doi: 10.1016/j.jphotobiol.2013.07.024

55. Chen H, Hayek S, Rivera Guzman J, Gillitt ND, Ibrahim SA, Jobin C, Sang S. The microbiota is essential for the generation of black tea theaflavins-derived metabolites. PloS One. 2012;7(12):e51001. PubMed PMID: 23227227. Pubmed Central PMCID: PMC3515489. doi: 10.1371/journal.pone.0051001

56. van't Slot G, Humpf HU. Degradation and metabolism of catechin, epigallocatechin-3-gallate (EGCG), and related compounds by the intestinal microbiota in the pig cecum model. Journal of Agricultural and Food Chemistry. 2009;57(17):8041-8. PubMed PMID: 19670865. doi: 10.1021/jf900458e

57. Meselhy MR, Nakamura N, Hattori M. Biotransformation of (-)-epicatechin 3-O-gallate by human intestinal bacteria. Chemical and Pharmaceutical Bulletin. 1997;45(5):888-93. PubMed PMID: 9178524. doi: 10.1248/cpb.45.888

58. Takagaki A, Nanjo F. Metabolism of (-)-epigallocatechin gallate by rat intestinal flora. Journal of Agricultural and Food Chemistry. 2010;58(2):1313-21. PubMed PMID: 20043675. doi: 10.1021/jf903375s

59. Shahrzad S, Aoyagi K, Winter A, Koyama A, Bitsch I. Pharmacokinetics of gallic acid and its relative bioavailability from tea in healthy humans. Journal of Nutrition. 2001;131(4):1207-10. PubMed PMID: 11285327. doi: 10.1093/jn/131.4.1207

60. Shahrzad S, Bitsch I. Determination of gallic acid and its metabolites in human plasma and urine by high-performance liquid chromatography. Journal of Chromatography B: Biomedical Sciences and Applications. 1998;705(1):87-95. PubMed PMID: 9498674.

61. Yasuda T, Inaba A, Ohmori M, Endo T, Kubo S, Ohsawa K. Urinary Metabolites of Gallic Acid in Rats and Their Radical-Scavenging Effects on 1,1-Diphenyl-2-picrylhydrazyl Radical. Journal of Natural Products. 2000;63(10):1444-6. doi: 10.1021/np0000421

62. Kohri T, Suzuki M, Nanjo F. Identification of metabolites of (-)-epicatechin gallate and their metabolic fate in the rat. Journal of Agricultural and Food Chemistry. 2003;51(18):5561-6. PubMed PMID: 12926915. doi: 10.1021/jf034450x

63. Feliciano RP, Istas G, Heiss C, Rodriguez-Mateos A. Plasma and Urinary Phenolic Profiles after Acute and Repetitive Intake of Wild Blueberry. Molecules. 2016;21(9). PubMed PMID: 27571052. Pubmed Central PMCID: PMC6273248. doi: 10.3390/molecules21091120

64. Pimpao RC, Dew T, Figueira ME, McDougall GJ, Stewart D, Ferreira RB, Santos CN, Williamson G. Urinary metabolite profiling identifies novel colonic metabolites and conjugates of phenolics in healthy volunteers. Molecular Nutrition & Food Research. 2014;58(7):1414-25. PubMed PMID: 24740799. doi: 10.1002/mnfr.201300822

65. Ancillotti C, Ulaszewska M, Mattivi F, Del Bubba M. Untargeted Metabolomics Analytical Strategy Based on Liquid Chromatography/Electrospray Ionization Linear Ion Trap Quadrupole/Orbitrap Mass Spectrometry for Discovering New Polyphenol Metabolites in Human Biofluids after Acute Ingestion of Vaccinium myrtillus Berry Supplement. Journal of the American Society for Mass Spectrometry. 2019;30(3):381-402. PubMed PMID: 30506347. doi: 10.1007/s13361-018-2111-y

66. Stalmach A, Edwards CA, Wightman JD, Crozier A. Colonic catabolism of dietary phenolic and polyphenolic compounds from Concord grape juice. Food & Function. 2013;4(1):52-62. PubMed PMID: 22961385. doi: 10.1039/c2fo30151b

67. Schantz M, Erk T, Richling E. Metabolism of green tea catechins by the human small intestine. Biotechnology Journal. 2010;5(10):1050-9. PubMed PMID: 20931601. doi: 10.1002/biot.201000214

68. Sanchez-Patan F, Barroso E, van de Wiele T, Jimenez-Giron A, Martin-Alvarez PJ, Moreno-Arribas MV, Martinez-Cuesta MC, Pelaez C, Requena T, Bartolome B. Comparative in vitro fermentations of cranberry and grape seed polyphenols with colonic microbiota. Food Chemistry. 2015;183:273-82. PubMed PMID: 25863636. doi: 10.1016/j.foodchem.2015.03.061

69. Sánchez-Patán F, Cueva C, Monagas M, Walton GE, Gibson GR, Martín-Álvarez PJ, Victoria Moreno-Arribas M, Bartolomé B. Gut microbial catabolism of grape seed flavan-3-ols by human faecal microbiota. Targetted analysis of precursor compounds, intermediate metabolites and end-products. Food Chemistry. 2012;131(1):337-47. doi: 10.1016/j.foodchem.2011.08.011

70. Sanchez-Patan F, Cueva C, Monagas M, Walton GE, Gibson GR, Quintanilla-Lopez JE, Lebron-Aguilar R, Martin-Alvarez PJ, Moreno-Arribas MV, Bartolome B. In vitro fermentation of a red wine extract by human gut microbiota: changes in microbial groups and formation of phenolic metabolites. Journal of Agricultural and Food Chemistry. 2012;60(9):2136-47. PubMed PMID: 22313337. doi: 10.1021/jf2040115

71. Munoz-Gonzalez C, Moreno-Arribas MV, Rodriguez-Bencomo JJ, Cueva C, Martin Alvarez PJ, Bartolome B, Pozo-Bayon MA. Feasibility and application of liquid-liquid extraction combined with gas chromatography-mass spectrometry for the analysis of phenolic acids from grape polyphenols degraded by human faecal microbiota. Food Chemistry. 2012;133(2):526-35. PubMed PMID: 25683429. doi: 10.1016/j.foodchem.2012.01.020

72. Rodríguez H, Landete JM, Rivas Bdl, Muñoz R. Metabolism of food phenolic acids by Lactobacillus plantarum CECT 748T. Food Chemistry. 2008;107(4):1393-8. doi: 10.1016/j.foodchem.2007.09.067

73. Sridharan GV, Choi K, Klemashevich C, Wu C, Prabakaran D, Pan LB, Steinmeyer S, Mueller C, Yousofshahi M, Alaniz RC, Lee K, Jayaraman A. Prediction and quantification of bioactive microbiota metabolites in the mouse gut. Nat Commun. 2014;5:5492. PubMed PMID: 25411059. doi: 10.1038/ncomms6492

74. Gonzalez-Barrio R, Edwards CA, Crozier A. Colonic catabolism of ellagitannins, ellagic acid, and raspberry anthocyanins: in vivo and in vitro studies. Drug Metabolism and Disposition: The Biological Fate of Chemicals. 2011;39(9):1680-8. PubMed PMID: 21622625. doi: 10.1124/dmd.111.039651

75. Xu B, Chang SK. Characterization of phenolic substances and antioxidant properties of food soybeans grown in the North Dakota-Minnesota region. Journal of Agricultural and Food Chemistry. 2008;56(19):9102-13. PubMed PMID: 18781761. doi: 10.1021/jf801451k

76. Zhao Z, Egashira Y, Sanada H. Phenolic antioxidants richly contained in corn bran are slightly bioavailable in rats. Journal of Agricultural and Food Chemistry. 2005;53(12):5030-5. PubMed PMID: 15941352. doi: 10.1021/jf050111n

77. Mattila P, Pihlava JM, Hellstrom J. Contents of phenolic acids, alkyl- and alkenylresorcinols, and avenanthramides in commercial grain products. Journal of Agricultural and Food Chemistry. 2005;53(21):8290-5. PubMed PMID: 16218677. doi: 10.1021/jf051437z

78. Hufeldt MR, Nielsen DS, Vogensen FK, Midtvedt T, Hansen AK. Variation in the gut microbiota of laboratory mice is related to both genetic and environmental factors. Comparative Medicine. 2010;60(5):336-47. PubMed PMID: 21262117. Pubmed Central PMCID: PMC2958200.

79. Lavelle A, Hoffmann TW, Pham HP, Langella P, Guedon E, Sokol H. Baseline microbiota composition modulates antibiotic-mediated effects on the gut microbiota and host. Microbiome. 2019;7(1):111. PubMed PMID: 31375137. Pubmed Central PMCID: PMC6676565. doi: 10.1186/s40168-019-0725-3

80. Ridder L, van der Hooft JJ, Verhoeven S, de Vos RC, Vervoort J, Bino RJ. In silico prediction and automatic LC-MS(n) annotation of green tea metabolites in urine. Analytical Chemistry. 2014;86(10):4767-74. PubMed PMID: 24779709. doi: 10.1021/ac403875b

81. Kim S, Lee MJ, Hong J, Li C, Smith TJ, Yang GY, Seril DN, Yang CS. Plasma and tissue levels of tea catechins in rats and mice during chronic consumption of green tea polyphenols. Nutrition and Cancer. 2000;37(1):41-8. PubMed PMID: 10965518. doi: 10.1207/s15327914nc3701_5

82. Westphal JF, Vetter D, Brogard JM. Hepatic side-effects of antibiotics. Journal of Antimicrobial Chemotherapy. 1994;33(3):387-401. PubMed PMID: 8040106. doi: 10.1093/jac/33.3.387

83. Buu NT. Relationship between catechol-O-methyltransferase and phenolsulfotransferase in the metabolism of dopamine in the rat brain. Journal of Neurochemistry. 1985;45(5):1612-9. PubMed PMID: 3930664. doi: 10.1111/j.1471-4159.1985.tb07234.x

84. Sugden RF, Eccleston D. Glycol sulphate ester formation from ( 14 C)noradrenaline in brain and the influence of a COMT inhibitor. Journal of Neurochemistry. 1971;18(12):2461-8. PubMed PMID: 5135906. doi: 10.1111/j.1471-4159.1971.tb00203.x

85. Nakamura Y, Tsuji S, Tonogai Y. Method for analysis of tannic acid and its metabolites in biological samples: application to tannic acid metabolism in the rat. Journal of Agricultural and Food Chemistry. 2003;51(1):331-9. PubMed PMID: 12502429. doi: 10.1021/jf020847+

86. Harrison CA, Laubitz D, Midura-Kiela MT, Jamwal DR, Besselsen DG, Ghishan FK, Kiela PR. Sexual Dimorphism in the Response to Broad-spectrum Antibiotics During T Cell-mediated Colitis. Journal of Crohn's & Colitis. 2019;13(1):115-26. PubMed PMID: 30252029. Pubmed Central PMCID: PMC6302957. doi: 10.1093/ecco-jcc/jjy144

87. Naz S, Siddiqi R, Ahmad S, Rasool SA, Sayeed SA. Antibacterial activity directed isolation of compounds from Punica granatum. Journal of Food Science. 2007;72(9):M341-5. PubMed PMID: 18034726. doi: 10.1111/j.1750-3841.2007.00533.x

88. Obrenovich ME, Donskey CJ, Schiefer IT, Bongiovanni R, Li L, Jaskiw GE. Quantification of phenolic acid metabolites in humans by LC-MS: a structural and targeted metabolomics approach. Bioanalysis. 2018;10(19):1591-608. PubMed PMID: 30295550. doi: 10.4155/bio-2018-0140

89. Rogers KJ, Angel A, Butterfield L. The penetration of catechol and pyrogallol into mouse brain and the effect on cerebral monoamine levels. Journal of Pharmacy and Pharmacology. 1968;20(9):727-9. PubMed PMID: 4386386. doi: 10.1111/j.2042-7158.1968.tb09845.x


Refbacks

  • There are currently no refbacks.




Copyright (c) 2019 George Eugene Jaskiw

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.

© Pathogens and Immunity 2019

Case Western Reserve University; Division of Infectious Diseases

10900 Euclid Ave.; Mailstop 4984; Cleveland, OH 44106

(216) 368-6317; ISSN: 2469-2964; info@paijournal.com