The intestinal microbiota in psoriasis
Monika Koper 1 , Anna Woźniacka 1 , Ewa Robak 1Abstract
Microbiota is a kind of ecosystem inhabiting some organs, supporting their proper functioning, but also having a significant impact on the development of the immune system. The largest reservoir of microbiota is the digestive tract, where the largest number of lymphocytes is also present. Literature gradually increases the number of studies assessing the relationship between intestinal dysbiosis and the development of various parenteral diseases. This article presents the latest data from the medical literature regarding intestinal microbiota and barrier in patients with psoriasis. In the cited studies, a quantitative advantage of Firmicutes phylum over Bacteroidetes phylum and a smaller colonization of Actinobacteria phylum has been demonstrated. In terms of the species, colonization of bacteria Faecalibacterium prausnitzii and Akkermansia muciniphilia was reduced, and Escherichia coli increased. Regarding the participation of individual taxonomic units, the results in the cited studies are partly different. However, all revealed significant differences between the intestinal microbiota of patients with psoriasis and a healthy population, which suggests the importance of intestinal dysbiosis in the development of this disease. It seems more important that what leads to disturbances in the metabolic balance is not so much the quantity of individual taxonomic units as their disproportions. In some studies, the deviations in microbiota correlated with the level of metabolites and indicators of inflammation. Moreover, some studies revealed a significantly higher incidence of Candida in the oral cavity as well as in the stool samples of patients with psoriasis. There are also reports in the literature in which the occurrence of intestinal inflammation and the impairment of the intestinal barrier in patients with psoriasis have been demonstrated. These observations indicate interrelations between psoriasis and intestinal disorders as well as the involvement of dysbiosis in both associations and the pathogenesis of psoriasis.
References
- 1. Alekseyenko A.V., Perez-Perez G.I., De Souza A., Strober B., Gao Z.,Bihan M., Li K., Methé B.A., Blaser M.J.: Community differentiationof the cutaneous microbiota in psoriasis. Microbiome, 2013; 1: 31
Google Scholar - 2. Arumugam M., Raes J., Pelletier E., Le Paslier D., Yamada T., MendeD.R., Fernandes G.R., Tap J., Bruls T., Batto J.M., Bertalan M., BorruelN., Casellas F., Fernandez L., Gautier L. i wsp.: Enterotypes of the humangut microbiome. Nature, 2011; 473: 174–180
Google Scholar - 3. Atarashi K., Tanoue T., Shima T., Imaoka A., Kuwahara T.,Momose Y., Cheng G., Yamasaki S., Saito T., Ohba Y., TaniguchiT., Takeda K., Hori S., Ivanov I.I., Umesaki Y. i wsp.: Induction ofcolonic regulatory T cells by indigenous Celostridium species. Science,2011; 331: 337–341
Google Scholar - 4. Ayala-Fontánez N., Soler D.C., McCormick T.S.: Current knowledgeon psoriasis and autoimmune diseases. Psoriasis, 2016; 6: 7–32
Google Scholar - 5. Baker B.S., Powles A., Fry L.: Peptidoglycan: A major aetiologicalfactor for psoriasis? Trends Immunol., 2006; 27: 545–551
Google Scholar - 6. Bischoff S.C.: ‘Gut health’: a new objective in medicine? BMCMed., 2011; 9: 24
Google Scholar - 7. Borrel G., Harris H.M., Tottey W., Mihajlovski A., Parisot N., PeyretailladeE., Peyret P., Gribaldo S., O’Toole P.W., Brugère J.F.: Genomesequence of “Candidatus Methanomethylophilus alvus” Mx1201,a methanogenic archaeon from the human gut belonging to a seventhorder of methanogens. J. Bacteriol., 2012; 194: 6944–6945
Google Scholar - 8. Boyman O., Conrad C., Tonel G., Gilliet M., Nestle F.O.: The pathogenicrole of tissue-resident immune cells in psoriasis. Trends Immunol.,2007; 28: 51–57
Google Scholar - 9. Brandtzaeg P.: The gut as communicator between environmentand host: Immunological consequences. Eur. J. Pharmacol., 2011;668: S16–S32
Google Scholar - 10. Buslau M., Menzel I., Holzmann H.: Fungal flora of human faecesin psoriasis and atopic dermatitis. Mycoses, 1990; 33: 90–94
Google Scholar - 11. Camilleri M., Madsen K., Spiller R., Greenwood-Van Meerveld B.,Verne G.N.: Intestinal barrier function in health and gastrointestinaldisease. Neurogastroenterol. Motil., 2012; 24: 503–512
Google Scholar - 12. Canani R.B., Costanzo M.D., Leone L., Bedogni G., Brambilla P., CianfaraniS., Nobili V., Pietrobelli A., Agostoni C.: Epigenetic mechanismselicited by nutrition in early life. Nutr. Res. Rev., 2011; 24: 198–205
Google Scholar - 13. Capon F.: The genetic basis of psoriasis. Int. J. Mol. Sci., 2017;18: E2526
Google Scholar - 14. Chen Y.J., Ho H.J., Tseng C.H., Lai Z.L., Shieh J.J., Wu C.Y.: Intestinalmicrobiota profiling and predicted metabolic dysregulation inpsoriasis patients. Exp Dermatol., 2018; 27: 1336–1343
Google Scholar - 15. Cho C.E., Taesuwan S., Malysheva O.V., Bender E., TulchinskyN.F., Yan J., Sutter J.L., Caudill M.A.: Trimethylamine-N-oxide (TMAO)response to animal source foods varies among healthy young menand is influenced by their gut microbiota composition: A randomizedcontrolled trial. Mol. Nutr. Food Res., 2016; 61: 1600324
Google Scholar - 16. Chularojanamontri L., Wongpraparut C., Tuchinda P., WinayanuwattikunW., Boonyasiri A., Kulthanan K., Thamlikitkul V.: OralCandida colonization in Thai patients with psoriasis. J. Med. Assoc.Thai., 2016; 99: 84–87
Google Scholar - 17. Claesson M.J., Cusack S., O’Sullivan O., Greene-Diniz R., De WeerdH., Flannery E., Marchesi J.R., Falush D., Dinan T., Fitzgerald G., StantonC., van Sinderen D., O’Connor M., Harnedy N., O’Connor K. i wsp.:Composition, variability, and temporal stability of the intestinal microbiotaof the elderly. Proc. Natl. Acad. Sci. USA, 2011; 108: 4586–4591
Google Scholar - 18. Codoñer F.M., Ramírez-Bosca A., Climent E., Carrión-GutierrezM., Guerrero M., Pérez-Orquín J.M., Horga de la Parte J., Genovés S.,Ramón D., Navarro-López V., Chenoll E.: Gut microbial compositionin patients with psoriasis. Sci. Rep., 2018; 8: 3812
Google Scholar - 19. Cotillard A., Kennedy S.P., Kong L.C., Prifti E., Pons N., Le ChatelierE., Almeida M., Quinquis B., Levenez F., Galleron N., Gougis S.,Rizkalla S., Batto J.M., Renault P., ANR MicroObes consortium i wsp.:Dietary intervention impact on gut microbial gene richness. Nature,2013; 500: 585–588
Google Scholar - 20. Daniel H., Gholami A.M., Berry D., Desmarchelier C., Hahne H.,Loh G., Mondot S., Lepage P., Rothballer M., Walker A., Böhm C., WenningM., Wagner M., Blaut M., Schmitt-Kopplin P. i wsp.: High-fat dietalters gut microbiota physiology in mice. ISME J., 2014; 8: 295–308
Google Scholar - 21. Davison S.C., Allen M.H., Mallon E., Barker J.N.: Contrasting patternsof streptococcal superantigen-induced T-cell proliferation inguttate vs. chronic plaque psoriasis. Br. J. Dermatol., 2001; 145: 245–251
Google Scholar - 22. de Groot P.F., Belzer C., Aydin Ö., Levin E., Levels J.H., AalvinkS., Boot F., Holleman F., van Raalte D.H., Scheithauer T.P., Simsek S.,Schaap F.G., Olde Damink S.W.M., Roep B.O., Hoekstra J.B. i wsp.: Distinctfecal and oral microbiota composition in human type 1 diabetes,an observational study. PLoS One, 2017; 12: e0188475
Google Scholar - 23. Drago L., De Grandi R., Altomare G., Pigatto P., Rossi O., ToscanoM.: Skin microbiota of first cousins affected by psoriasis and atopicdermatitis. Clin. Mol. Allergy., 2016; 14: 2
Google Scholar - 24. Dziarski R., Gupta D.: Review: Mammalian peptidoglycan recognitionproteins (PGRPs) in innate immunity. Innate Immun., 2010; 16: 168–174
Google Scholar - 25. Eppinga H., Sperna Weiland C.J., Thio H.B., van der Woude C.J.,Nijsten T.E., Peppelenbosch M.P., Konstantinov S.R.: Similar depletionof protective Faecalibacterium prausnitzii in psoriasis and inflammatorybowel disease, but not in hidradenitis suppurativa. J CrohnsColitis, 2016; 10: 1067–1075
Google Scholar - 26. Fahlén A., Engstrand L., Baker B.S., Powles A., Fry L.: Comparisonof bacterial microbiota in skin biopsies from normal and psoriaticskin. Arch. Dermatol. Res., 2012; 304: 15–22
Google Scholar - 27. Fouhy F., Ross R.P., Fitzgerald G.F., Stanton C., Cotter P.D.: Compositionof the early intestinal microbiota: knowledge, knowledgegaps and the use of high-throughput sequencing to address thesegaps. Gut Microbes, 2012; 3: 203–220
Google Scholar - 28. Gao Z., Tseng C.H., Strober B.E., Pei Z., Blaser M.J.: Substantialalterations of the cutaneous bacterial biota in psoriatic lesions. PLoSOne, 2008; 3: e2719
Google Scholar - 29. Gollin G., Marks C., Marks W.H.: Intestinal fatty acid binding proteinin serum and urine reflects early ischemic injury to the smallbowel. Surgery, 1993; 113: 545–551
Google Scholar - 30. Gottlieb A.B., Kircik L., Eisen D., Jackson J.M., Boh E.E., StroberB.E., Frankel E., Xia H.A., Stevens S.R.: Use of etanercept for psoriaticarthritis in the dermatology clinic: the Experience Diagnosing,Understanding Care, and Treatment with Etanercept (EDUCATE)study. J. Dermatol. Treat., 2006; 17: 343–352
Google Scholar - 31. Grice E.A., Segre J.A.: The skin microbiome. Nat. Rev. Microbiol.,2011; 9: 244–253
Google Scholar - 32. Groeger D., O’Mahony L., Murphy E.F., Bourke J.F., Dinan T.G.,Kiely B., Shanahan F., Quigley E.M.: Bifidobacterium infantis 35624modulates host inflammatory processes beyond the gut. Gut Microbes,2013; 4: 325–339
Google Scholar - 33. Groschwitz K.R., Hogan S.P.: Intestinal barrier function: Molecularregulation and disease pathogenesis. J. Allergy Clin. Immunol.,2009; 124: 3–20
Google Scholar - 34. Gueniche A., Philippe D., Bastien P., Reuteler G., Blum S., Castiel-Higounenc I., Breton L., Benyacoub J.: Randomised double-blindplacebo-controlled study of the effect of Lactobacillus paracasei NCC 2461 on skin reactivity. Benef. Microbes, 2014; 5: 137–145
Google Scholar - 35. Henseler T., Christophers E.: Disease concomitance in psoriasis.J Am. Acad. Dermatol., 1995; 32: 982–986
Google Scholar - 36. Hevia A., Milani C., López P., Cuervo A., Arboleya S., Duranti S.,Turroni F., González S., Suárez A., Gueimonde M., Ventura M., SánchezB., Margolles A.: Intestinal dysbiosis associated with systemiclupus erythematosus. mBio, 2014; 5: e01548–14
Google Scholar - 37. Hidalgo-Cantabrana C., Gómez J., Delgado S., Requena-LópezS., Queiro-Silva R., Margolles A., Coto E., Sánchez B., Coto-Segura P.:Gut microbiota dysbiosis in a cohort of patients with psoriasis. Br.J. Dermatol., 2019; 181: 1287–1295
Google Scholar - 38. Hindson J.: Multiple sclerosis: A possible link between multiplesclerosis and gut microbiota. Nat. Rev. Neurol., 2017; 13: 705
Google Scholar - 39. Huang L., Gao R., Yu N., Zhu Y., Ding Y., Qin H.: Dysbiosis of gutmicrobiota was closely associated with psoriasis. Sci. China Life Sci.,2019; 62: 807–815
Google Scholar - 40. Humbert P., Bidet A., Treffel P., Drobacheff C., Agache P.: Intestinalpermeability in patients with psoriasis. J. Dermatol. Sci., 1991; 2: 324–326
Google Scholar - 41. Jones B.V., Begley M., Hill C., Gahan C.G., Marchesi J.R.: Functionaland comparative metagenomic analysis of bile salt hydrolaseactivity in the human gut microbiome. Proc. Natl. Acad. Sci. USA,2008; 105: 13580–13585
Google Scholar - 42. Jovel J., Patterson J., Wang W., Hotte N., O’Keefe S., Mitchel T.,Perry T., Kao D., Mason A.L., Madsen K.L., Wong G.K.: Characterizationof the gut microbiome using 16S or shotgun metagenomics.Front. Microbiol., 2016; 7: 459
Google Scholar - 43. Kainu K., Kivinen K., Zucchelli M., Suomela S., Kere J., Inerot A.,Baker B.S., Powles A.V., Fry L., Samuelsson L., Saarialho-Kere U.: Associationof psoriasis to PGLYRP and SPRR genes at PSORS4 locus on1q shows heterogeneity between Finnish, Swedish and Irish families.Exp. Dermatol., 2009; 18: 109–115
Google Scholar - 44. Lee S.H.: Intestinal permeability regulation by tight junction: Implicationon inflammatory bowel diseases. Intest. Res., 2015; 13: 11–18
Google Scholar - 45. Lesan S., Toosi R., Aliakbarzadeh R., Daneshpazhooh M., MahmoudiL., Tavakolpour S., Mahmoudi H.: Oral Candida colonizationand plaque type psoriasis: Is there any relationship? J. Investig. Clin.Dent., 2018; 9: e12335
Google Scholar - 46. Lewis D.J., Chan W.H., Hinojosa T., Hsu S., Feldman S.R.: Mechanismsof microbial pathogenesis and the role of the skin microbiomein psoriasis: A review. Clin Dermatol., 2019; 37: 160–166
Google Scholar - 47. Ley R.E., Peterson D.A., Gordon J.I.: Ecological and evolutionaryforces shaping microbial diversity in the human intestine. Cell,2006; 124: 837–848
Google Scholar - 48. Ley R.E., Turnbaugh P.J., Klein S., Gordon J.I.: Microbial ecology:Human gut microbes associated with obesity. Nature, 2006;444: 1022–1023
Google Scholar - 49. Liberato M.V., Nascimento A.S., Ayers S.D., Lin J.Z., Cvoro A.,Silveira R.L., Martínez L., Souza P.C., Saidemberg D., Deng T., AmatoA.A., Togashi M., Hsueh W.A., Phillips K., Palma M.S. i wsp.: Mediumchain fatty acids are selective peroxisome proliferator activatedreceptor (PPAR) γ activators and panPPAR partial agonists. PLoSOne, 2012; 7: e36297
Google Scholar - 50. Lopez-Siles M., Khan T.M., Duncan S.H., Harmsen H.J., Garcia-GilL.J., Flint H.J.: Cultured representatives of two major phylogroups ofhuman colonic Faecalibacterium prausnitzii can utilize pectin, uronicacids, and host–derived substrates for growth. Appl. Environ. Microbiol.,2012; 78: 420–428
Google Scholar - 51. Luo C., Tsementzi D., Kyrpides N. C., Konstantinidis K.T.: Individualgenome assembly from complex community short-readmetagenomic datasets. ISME J., 2012; 6: 898–901
Google Scholar - 52. Marcobal A., Kashyap P.C., Nelson T.A., Aronov P.A., Donia M.S.,Spormann A., Fischbach M.A., Sonnenburg J.L.: A metabolomic viewof how the human gut microbiota impacts the host metabolomeusing humanized and gnotobiotic mice. ISME J., 2013; 7: 1933–1943
Google Scholar - 53. Masallat D., Moemen D., State A.F.: Gut bacterial microbiotain psoriasis: A case control study. Afr. J. Microbiol. Res., 2016; 10:1337–1343
Google Scholar - 54. Mazmanian S.K., Round J.L., Kasper D.L.: Amicrobial symbiosisfactor prevents intestinal inflammatory disease. Nature, 2008;453: 620–625
Google Scholar - 55. McFadden J., Valdimarsson H., Fry L.: Cross–reactivity betweenstreptococcal M surface antigen and human skin. Br. J. Dermatol.,1991; 125: 443–447
Google Scholar - 56. Miquel S., Martín R., Rossi O., Bermúdez-Humarán L.G., ChatelJ.M., Sokol H., Thomas M., Wells J.M., Langella P.: Faecalibacteriumprausnitzii and human intestinal health. Curr. Opin. Microbiol., 2013;16: 255–261
Google Scholar - 57. Mitra S., Förster-Fromme K., Damms-Machado A., ScheurenbrandT., Biskup S., Huson D.H., Bischoff S.C.: Analysis of the intestinalmicrobiota using SOLiD 16S rRNA gene sequencing and SOLiDshotgun sequencing. BMC Genomics, 2013; 14: S16
Google Scholar - 58. Nermes M., Kantele J.M., Atosuo T.J., Salminen S., Isolauri E.: Interactionof orally administered Lactobacillus rhamnosus GG with skinand gut microbiota and humoral immunity in infants with atopicdermatitis. Clin. Exp. Allergy, 2011; 41: 370–377
Google Scholar - 59. Norrlind R.: Psoriasis following infections with hemolytic streptococci.Acta Derm. Venereol., 1950; 30: 64–72
Google Scholar - 60. Norrlind R.: The significance of infections in the origination ofpsoriasis. Scand. J. Rheumatol., 1972; 1: 135–144
Google Scholar - 61. Ochoa-Repáraz J., Mielcarz D.W., Wang Y., Begum-Haque S., DasguptaS., Kasper D.L., Kasper L.H.: A polysaccharide from the humancommensal Bacteroides fragilis protects against CNS demyelinatingdisease. Mucosal Immunol., 2010; 3: 487–495
Google Scholar - 62. Palmer C., Bik E.M., DiGiulio D.B., Relman D.A., Brown P.O.: Developmentof the human infant intestinal microbiota. PLoS Biol.,2007; 5: e177
Google Scholar - 63. Picciani B.L., Michalski-Santos B., Carneiro S., Sampaio A.L.,Avelleira J.C., Azulay D.R., Pinto J.M., Dias E.P.: Oral candidiasis inpatients with psoriasis: Correlation of oral examination and cytopathologicalevaluation with psoriasis disease severity and treatment.J. Am. Acad. Dermatol., 2013; 68: 986–991
Google Scholar - 64. Qin J., Li R., Raes J., Arumugam M., Burgdorf K.S., Manichanh C.,Nielsen T., Pons N., Levenez F., Yamada T., Mende D.R., Li J., Xu J., LiS., Li D. i wsp.: A human gut microbial gene catalogue establishedby metagenomic sequencing. Nature, 2010; 464: 59–65
Google Scholar - 65. Rajilic–Stojanović M., Smidt H., de Vos W.M.: Diversity of thehuman gastrointestinal tract microbiota revisited. Environ. Microbiol.,2007; 9: 2125–2136
Google Scholar - 66. Ramírez-Boscá A., Navarro-López V., Martínez-Andrés A., SuchJ., Francés R., Horga de la Parte J., Asín-Llorca M.: Identification ofbacterial DNA in the peripheral blood of patients with active psoriasis.JAMA Dermatol., 2015; 151: 670–671
Google Scholar - 67. Rampelli S., Candela M., Turroni S., Biagi E., Collino S., FranceschiC., O’Toole P.W., Brigidi P.: Functional metagenomic profilingof intestinal microbiome in extreme ageing. Aging, 2013;5: 902–912
Google Scholar - 68. Ritchlin C.T., Colbert R.A., Gladman D.D.: Psoriatic arthritis. N.Engl. J. Med., 2017; 376: 957–970
Google Scholar - 69. Roh S.W., Abell G.C., Kim K.H., Nam Y.D., Bae J.W.: Comparingmicroarrays and next-generation sequencing technologies for microbialecology research. Trends Biotechnol., 2010; 28: 291–299
Google Scholar - 70. Scaldaferri F., Pizzoferrato M., Gerardi V., Lopetuso L., GasbarriniA.: The gut barrier: New acquisitions and therapeutic approaches. J.Clin. Gastroenterol., 2012; 46: S12–S17
Google Scholar - 71. Scarpa R., Manguso F., D’Arienzo A., D’Armiento F.P., Astarita C.,Mazzacca G., Ayala F.: Microscopic inflammatory changes in colon ofpatients with both active psoriasis and psoriatic arthritis withoutbowel symptoms. J. Rheumatol., 2000; 27: 1241–1246
Google Scholar - 72. Scher J.U., Ubeda C., Artacho A., Attur M., Isaac S., Reddy S.M.,Marmon S., Neimann A., Brusca S., Patel T., Manasson J., Pamer E.G.,Littman D.R., Abramson S.B.: Decreased bacterial diversity characterizesthe altered gut microbiota in patients with psoriatic arthritis,resembling dysbiosis in inflammatory bowel disease. ArthritisRheumatol., 2015; 67: 128–139
Google Scholar - 73. Shapiro J., Cohen N.A., Shalev V., Uzan A., Koren O., MaharshakN.: Psoriatic patients have a distinct structural and functional fecalmicrobiota compared with controls. J Dermatol. 2019; 46: 595–603
Google Scholar - 74. Sikora M., Chrabąszcz M., Maciejewski C., Zaremba M., WaśkielA., Olszewska M., Rudnicka L.: Intestinal barrier integrity in patientswith plaque psoriasis. J. Dermatol., 2018; 45: 1468–1470
Google Scholar - 75. Sikora M., Stec A., Chrabąszcz M., Waśkiel–Burnat A., ZarembaM., Olszewska M., Rudnicka L.: Intestinal fatty acid binding protein,a biomarker of intestinal barrier, is associated with severity of psoriasis.J. Clin. Med., 2019; 12: E1021
Google Scholar - 76. Takemoto A., Cho O., Morohoshi Y., Sugita T., Muto M.: Molecularcharacterization of the skin fungal microbiome in patients withpsoriasis. J. Dermatol., 2015; 42: 166–170
Google Scholar - 77. Tan L., Zhao S., Zhu W., Wu L., Li J., Shen M., Lei L., Chen X.,Peng C.: The Akkermansia muciniphila is a gut microbiota signaturein psoriasis. Exp. Dermatol., 2018; 27: 144–149
Google Scholar - 78. Tett A., Pasolli E., Farina S., Truong D.T., Asnicar F., Zolfo M.,Beghini F., Armanini F., Jousson O., De Sanctis V., Bertorelli R., GirolomoniG., Cristofolini M., Segata N.: Unexplored diversity andstrain–level structure of the skin microbiome associated with psoriasis.NPJ Biofilms Microbiomes, 2017; 3: 14
Google Scholar - 79. Thursby E., Juge N.: Introduction to the human gut microbiota.Biochem. J., 2017; 474: 1823–1836
Google Scholar - 80. Toussirot E., Aubin F., Dumoulin G.: Relationships between adiposetissue and psoriasis, with or without arthritis. Front. Immunol.,2014; 5: 368
Google Scholar - 81. van der Beek C.M., Dejong C.H., Troost F.J., Masclee A.A., LenaertsK.: Role of short–chain fatty acids in colonic inflammation,carcinogenesis, and mucosal protection and healing. Nutr. Rev.,2017; 75: 286–305
Google Scholar - 82. Veiga P., Gallini C.A., Beal C., Michaud M., Delaney M.L., DuBoisA., Khlebnikov A., van Hylckama Vlieg J.E., Punit S, Glickman J.N.,Onderdonk A., Glimcher L.H., Garrett W.S.: Bifidobacterium animalissubsp. lactis fermented milk product reduces inflammation by alteringa niche for colitogenic microbes. Proc. Natl. Acad. Sci. USA,2010; 107: 18132–18137
Google Scholar - 83. Vijayashankar M., Raghunath N.: Pustular psoriasis respondingto probiotics – A new insight. Our Dermatol. Online, 2012; 3: 326–328
Google Scholar - 84. Waldman A., Gilhar A., Duek L., Berdicevsky I.: Incidence of Candidain psoriasis – a study on the fungal flora of psoriatic patients.Mycoses, 2001; 44: 77–81
Google Scholar - 85. Wells J.M., Brummer R.J., Derrien M., MacDonald T.T., Troost F.,Cani P.D., Theodorou V., Dekker J., Méheust A., de Vos W.M., MercenierA., Nauta A., Garcia–Rodenas C.L.: Homeostasis of the gut barrierand potential biomarkers. Am. J. Physiol. Gastrointest. LiverPhysiol., 2017; 312: G171–G193
Google Scholar - 86. Wong J.M., de Souza R., Kendall C.W., Emam A., Jenkins D.J.:Colonic health: Fermentation and short chain fatty acids. J. Clin.Gastroenterol., 2006; 40: 235–243
Google Scholar - 87. Zákostelská Z., Málková J., Klimešová K., Rossmann P., Hornová M.,Novosádová I., Stehlíková Z., Kostovčík M., Hudcovic T., Štepánková R.,Jůzlová K., Hercogová J., Tlaskalová–Hogenová H., Kverka M.: Intestinalmicrobiota promotes psoriasis–like skin inflammation by enhancingTh17 response. PLoS One, 2016; 11: e0159539
Google Scholar