Subscribe to RSS
DOI: 10.1055/a-1647-2866
Gut Microbiota of Pigs Metabolizes Extracts of Filipendula ulmaria and Orthosiphon aristatus–Herbal Remedies Used in Urinary Tract Disorders
Supported by: Narodowe Centrum Nauki 2018/29/B/NZ7/01873Abstract
Urinary tract infections influence the mortality rate in pigs and are linked to extensive antibiotic usage in the farm industry. Filipendula ulmaria (L.) Maxim. and Orthosiphon aristatus (Blume) Miq. are widespread medicinal plants traditionally used to treat urinary tract disorders. As their preparations are orally administered, the metabolism of their constituents by gut microbiota before absorption should be considered. Until now, no experiments had been performed to describe the biotransformation of tthose plantsʼ extracts by animal gut microbiota. The study evaluates the influence of pig intestinal microbiota on the structure of active compounds in flowers of F. ulmaria and leaves of O. aristatus. The incubations of the extracts with piglet gut microbiota were performed in anaerobic conditions, and the samples of the batch culture were collected for 24 h. In F. ulmaria, the main metabolites were quercetin and kaempferol, which were products of the deglycosylation of flavonoids. After 24 h incubation of O. aristatus extract with the piglet gut microbiota, 2 main metabolites were observed. One, tentatively identified as 3-(3-dihydroxyphenyl)propionic acid, is likely the primary metabolite of the most abundant depsides and phenolic acids. The results confirm the formation of the compounds with anti-inflammatory and diuretic activity in the microbiota cultures, which might suggest F. ulmaria and O. aristatus for treating urinary tract disorders in piglets. Based on the similarities of human and pig gut microbiota, the pig model can help estimate the metabolic pathways of natural products in humans.
Key words
Filipendula ulmaria - Orthosiphon aristatus - Rosaceae - Lamiaceae - microbiota - metabolism - swine, piglets - urinary tractPublication History
Received: 01 April 2021
Accepted after revision: 25 August 2021
Article published online:
08 October 2021
© 2021. Thieme. All rights reserved.
Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany
-
References
- 1 Wichtl M. ed. Herbal Drugs and Phytopharmaceuticals: A Handbook for Practice on a Scientific Basis. Stuttgart: Medpharm GmbH Scientific Publishers; 2004
- 2 European Medicines Agency. Assessment report on Filipendula ulmaria (L.) Maxim., herba and Filipendula ulmaria (L.) Maxim., flos. 12.07.2011 44. 1-18 Accessed March 31, 2021 at: http://www.ema.europa.eu/docs/en_GB/document_library/Herbal_-_HMPC_assessment_report/2011/09/WC500115355.pdf
- 3 de Baïracli-Levy J. Herbal Handbook for Farm and Stable. Emmaus, Pa: Rodale Press; 1976
- 4 Wynn SG, Fougère B. Veterinary Herbal Medicine. St. Louis, Mo: Mosby Elsevier; 2007
- 5 Popowski D, Pawłowska KA, Piwowarski JP, Granica S. Gut microbiota-assisted isolation of flavonoids with a galloyl moiety from flowers of meadowsweet, Filipendula ulmaria (L.) Maxim. Phytochem Lett 2019; 30: 220-223
- 6 Olennikov DN, Kashchenko NI, Chirikova NK. Meadowsweet teas as new functional beverages: comparative analysis of nutrients, phytochemicals and biological effects of four Filipendula species. Molecules 2017; 22: 1-23
- 7 Katanić J, Boroja T, Stanković N, Mihailović V, Mladenović M, Kreft S, Vrvić MM. Bioactivity, stability and phenolic characterization of Filipendula ulmaria (L.) Maxim. Food Funct 2015; 6: 1164-1175
- 8 Ameer OZ, Salman IM, Asmawi MZ, Ibraheem ZO, Yam MF. Orthosiphon stamineus: Traditional uses, phytochemistry, pharmacology, and toxicology. J Med Food 2012; 15: 678-690
- 9 Akowuah GA, Ismail Z, Norhayati I, Sadikun A. The effects of different extraction solvents of varying polarities on polyphenols of Orthosiphon stamineus and evaluation of the free radical-scavenging activity. Food Chem 2005; 93: 311-317
- 10 Akowuah GA, Zhari I, Norhayati I, Sadikun A, Khamsah SM. Sinensetin, eupatorin, 3′-hydroxy-5,6,7,4′-tetramethoxyflavone and rosmarinic acid contents and antioxidative effect of Orthosiphon stamineus from Malaysia. Food Chem 2004; 87: 559-566
- 11 Orthosiphon. Wamine 2021. Accessed March 31, 2021 at: https://www.wamine.fr/plantes/orthosiphon/
- 12 Nutri Horse Detox. 2021 Accessed March 31, 2021 at: https://www.vaschovatel.pl/90640-syrop-nutri-horse-detox-1-5-l.html
- 13 Ekybleed. 2021 Accessed March 31, 2021 at: https://en.audevard.com/equine-effort/122-ekybleed.html
- 14 de Brito BG, Leite DS, Linhares RE, Vidotto MC. Virulence-associated factors of uropathogenic Escherichia coli strains isolated from pigs. Vet Microbiol 1999; 65: 123-132
- 15 Chagnon M, DʼAllaire S, Drolet R. A prospective study of sow mortality in breeding herds. Can J Vet Res 1991; 55: 180-184 Accessed May 6, 2021 at: https://www.scopus.com/inward/record.uri?eid=2-s2.0-0026145516&partnerID=40&md5=84ef6985e5fcad8de974c8e1f02cc7d4
- 16 Sanz M, Roberts JD, Perfumo CJ, Alvarez RM, Donovan T, Almond G. Assessment of sow mortality in a large herd. J Swine Heal Prod 2006; 15: 30-36 Accessed March 31, 2021 at: http://www.aasv.org/shap.html
- 17 Krag L, Hancock V, Aalbæk B, Klemm P. Genotypic and phenotypic characterisation of Escherichia coli strains associated with porcine pyelonephritis. Vet Microbiol 2009; 134: 318-326
- 18 Lekagul A, Tangcharoensathien V, Yeung S. Patterns of antibiotic use in global pig production: a systematic review. Vet Anim Sci 2019; 7: 100058
- 19 Rüel B, Kyriacou CC, Forat M. Evaluation of a dietary urine acidifier on urinary and reproduction parameters in sows. Proc Br Soc Anim Sci 2008; 2008: 278
- 20 Turner PV. The role of the gut microbiota on animal model reproducibility. Anim Model Exp Med 2018; 1: 109-115
- 21 Vernocchi P, Del Chierico F, Putignani L. Gut microbiota metabolism and interaction with food components. Int J Mol Sci 2020; 21: 3688
- 22 Rowland I, Gibson G, Heinken A, Scott K, Swann J, Thiele I, Tuohy K. Gut microbiota functions: metabolism of nutrients and other food components. Eur J Nutr 2018; 57: 1-24
- 23 Aura AM. Microbial metabolism of dietary phenolic compounds in the colon. Phytochemistry Reviews 2008; 7: 407-429
- 24 Reyes-Becerril M, Gijón D, Angulo M, Vázquez-Martínez J, López MG, Junco E, Armenta J, Guerra K, Angulo C. Composition, antioxidant capacity, intestinal, and immunobiological effects of oregano (Lippia palmeri Watts) in goats: preliminary in vitro and in vivo studies. Trop Anim Health Prod 2021; 53: 101
- 25 Tedeschi LO, Muir JP, Naumann HD, Norris AB, Ramírez-Restrepo CA, Mertens-Talcott SU. Nutritional aspects of ecologically relevant phytochemicals in ruminant production. Front Vet Sci 2021; 8: 1-24
- 26 Heinritz SN, Mosenthin R, Weiss E. Use of pigs as a potential model for research into dietary modulation of the human gut microbiota. Nutr Res Rev 2013; 26: 191-209
- 27 Guo Z, Liang X, Xie Y. Qualitative and quantitative analysis on the chemical constituents in Orthosiphon stamineus Benth. using ultra high-performance liquid chromatography coupled with electrospray ionization tandem mass spectrometry. J Pharm Biomed Anal 2019; 164: 135-147
- 28 Lee YH, Kim B, Kim S, Min-Sun K. Characterization of metabolite profiles from the leaves of green perilla (Perilla frutescens) by ultra high performance liquid chromatography coupled with electrospray ionization quadrupole time-of-flight mass spectrometry and screening for their antioxidant properties. J Food Drug Anal 2017; 25: 776-788
- 29 Sumaryono W, Proksch P, Wray V, Witte L, Hartmann T. Qualitative and quantitative analysis of the phenolic constituents from Orthosiphon aristatus . Planta Med 1991; 57: 176-180
- 30 Awale S, Tezuka Y, Banskota AH, Kouda K, Tun KM, Kadota S. Five novel highly oxygenated diterpenes of Orthosiphon stamineus from Myanmar. J Nat Prod 2001; 64: 592-596
- 31 Chen WD, Zhao YL, Sun WJ, He YJ, Liu YP, Jin Q, Yang XW, Luo XD. “Kidney tea” and its bioactive secondary metabolites for treatment of gout. J Agric Food Chem 2020; 68: 9131-9138
- 32 Braune A, Blaut M. Bacterial species involved in the conversion of dietary flavonoids in the human gut. Gut Microbes 2016; 7: 216-234
- 33 Bijttebier S, Van der Auwera A, Voorspoels S, Noten B, Hermans N, Pieters L, Apers S. A first step in the quest for the active constituents in Filipendula ulmaria (Meadowsweet): comprehensive phytochemical identification by liquid chromatography coupled to quadrupole-orbitrap mass spectrometry. Planta Med 2016; 82: 559-572
- 34 Selma MV, Espín JC, Tomás-Barberán FA. Interaction between phenolics and gut microbiota: role in human health. J Agric Food Chem 2009; 57: 6485-6501
- 35 Tomas-Barberan F, García-Villalba R, Quartieri A, Raimondi S, Amaretti A, Leonardi A, Rossi M. In vitro transformation of chlorogenic acid by human gut microbiota. Mol Nutr Food Res 2014; 58: 1122-1131
- 36 Li L, Chen Y, Feng X, Yin J, Li S, Sun Y, Zhang L. Identification of metabolites of eupatorin in vivo and in vitro based on UHPLC-Q-TOF-MS/MS. Molecules 2019; 24: 2658
- 37 Zhao W, Wang Y, Liu S, Huang J, Zhai Z, He C, Ding J, Wang J, Wang H, Fan W, Zhao J, Meng H. The dynamic distribution of porcine microbiota across different ages and gastrointestinal tract segments. PLoS One 2015; 10: e0117441
- 38 Tomas J, Langella P, Cherbuy C. The intestinal microbiota in the rat model: major breakthroughs from new technologies. Anim Heal Res Rev 2012; 13: 54-63
- 39 Vargas F, Romecín P, García-Guillén AI, Wangesteen R, Vargas-Tendero P, Paredes MD, Atucha NM, García-Estañ J. Flavonoids in kidney health and disease. Front Physiol 2018; 9: 1-12
- 40 Marín L, Miguélez EM, Villar CJ, Lombó F. Bioavailability of dietary polyphenols and gut microbiota metabolism: antimicrobial properties. Biomed Res Int 2015; 2015: 1-18
- 41 Nielsen TK, Petersen NA, Stærk K, Grønnemose RB, Palarasah Y, Nielsen LF, Kolmos HJ, Andersen TE, Lund L. A porcine model for urinary tract infection. Front Microbiol 2019; 10: 1-12
- 42 Rutkowski L. Klucz do oznaczania roślin naczyniowych Polski niżowej. Warsaw: Wydawnictwo Naukowe PWN; 2014: 218
- 43 Polish Pharmacopoeia XI, Volume 2. Warsaw: Office for Registration of Medicinal Products, Medical Devices and Biocidal Products; 2017: 1710-1711