Skin microbiota signature distinguishes IBD patients and reflects skin adverse events during anti-TNF therapy

. 2022 ; 12 () : 1064537. [epub] 20230110

Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid36704107

Crohn's disease (CD) and ulcerative colitis (UC) are two forms of inflammatory bowel disease (IBD), where the role of gut but not skin dysbiosis is well recognized. Inhibitors of TNF have been successful in IBD treatment, but up to a quarter of patients suffer from unpredictable skin adverse events (SkAE). For this purpose, we analyzed temporal dynamics of skin microbiota and serum markers of inflammation and epithelial barrier integrity during anti-TNF therapy and SkAE manifestation in IBD patients. We observed that the skin microbiota signature of IBD patients differs markedly from healthy subjects. In particular, the skin microbiota of CD patients differs significantly from that of UC patients and healthy subjects, mainly in the retroauricular crease. In addition, we showed that anti-TNF-related SkAE are associated with specific shifts in skin microbiota profile and with a decrease in serum levels of L-FABP and I-FABP in IBD patients. For the first time, we showed that shifts in microbial composition in IBD patients are not limited to the gut and that skin microbiota and serum markers of the epithelium barrier may be suitable markers of SkAE during anti-TNF therapy.

Zobrazit více v PubMed

Alatab S., Sepanlou S. G., Ikuta K., Vahedi H., Bisignano C., Safiri S., et al. (2020). The global, regional, and national burden of inflammatory bowel disease in 195 countries and territories, 1990–2017: A systematic analysis for the global burden of disease study 2017. Lancet Gastroenterol. Hepatol. 5 (1), 17–30. doi: 10.1016/S2468-1253(19)30333-4 PubMed DOI PMC

Aldars-García L., Chaparro M., Gisbert J. P. (2021). Systematic review: The gut microbiome and its potential clinical application in inflammatory bowel disease. Microorganisms 9 (5), 977. doi: 10.3390/microorganisms9050977 PubMed DOI PMC

Alinaghi F., Tekin H. G., Burisch J., Wu J. J., Thyssen J. P., Egeberg A. (2020). Global prevalence and bidirectional association between psoriasis and inflammatory bowel disease–a systematic review and meta-analysis. J. Crohn's Colitis. 14 (3), 351–360. doi: 10.1093/ecco-jcc/jjz152 PubMed DOI

Alipour M., Zaidi D., Valcheva R., Jovel J., Martínez I., Sergi C., et al. (2016). Mucosal barrier depletion and loss of bacterial diversity are primary abnormalities in paediatric ulcerative colitis. J. Crohn's Colitis. 10 (4), 462–471. doi: 10.1093/ecco-jcc/jjv223 PubMed DOI PMC

Andoh A., Imaeda H., Aomatsu T., Inatomi O., Bamba S., Sasaki M., et al. (2011). Comparison of the fecal microbiota profiles between ulcerative colitis and crohn's disease using terminal restriction fragment length polymorphism analysis. J. Gastroenterol. 46 (4), 479–486. doi: 10.1007/s00535-010-0368-4 PubMed DOI

Bajaj J. S., Fagan A., Sikaroodi M., Kakiyama G., Takei H., Degefu Y., et al. (2019). Alterations in skin microbiomes of patients with cirrhosis. Clin. Gastroenterol. Hepatol. 17 (12), 2581–91.e15. doi: 10.1016/j.cgh.2019.03.028 PubMed DOI PMC

Bajer L., Kverka M., Kostovcik M., Macinga P., Dvorak J., Stehlikova Z., et al. (2017). Distinct gut microbiota profiles in patients with primary sclerosing cholangitis and ulcerative colitis. World J. Gastroenterol. 23 (25), 4548–4558. doi: 10.3748/wjg.v23.i25.4548 PubMed DOI PMC

Baran A., Kiluk P., Maciaszek M., Swiderska M., Flisiak I. (2019). Liver fatty acid-binding protein might be a predictive marker of clinical response to systemic treatment in psoriasis. Arch. Dermatol. Res. 311 (5), 389–397. doi: 10.1007/s00403-019-01917-w PubMed DOI PMC

Bates D., Mächler M., Bolker B., Walker S. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67(1), 1–48. doi:  10.18637/jss.v067.i01 DOI

Bazin T., Hooks K. B., Barnetche T., Truchetet M.-E., Enaud R., Richez C., et al. (2018). Microbiota composition may predict anti-TNF alpha response in spondyloarthritis patients: an exploratory study. Sci. Rep. 8 (1), 1–11. doi: 10.1038/s41598-018-23571-4 PubMed DOI PMC

Bilgin H., Sarmis A., Tigen E., Soyletir G., Mulazimoglu L. (2015). Delftia acidovorans: A rare pathogen in immunocompetent and immunocompromised patients. Can. J. Infect. Dis. Med. Microbiol. 26 (5), 277–279. doi: 10.1155/2015/973284 PubMed DOI PMC

Bouma G., Strober W. (2003). The immunological and genetic basis of inflammatory bowel disease. Nat. Rev. Immunol. 3 (7), 521–533. doi: 10.1038/nri1132 PubMed DOI

Byrd A. L., Deming C., Cassidy S. K., Harrison O. J., Ng W.-I., Conlan S., et al. (2017). Staphylococcus aureus and staphylococcus epidermidis strain diversity underlying pediatric atopic dermatitis. Sci. Trans. Med. 9 (397), eaal4651. doi:  10.1126/scitranslmed.aal4651 PubMed DOI PMC

Caruso R., Lo B. C., Núñez G. (2020). Host–microbiota interactions in inflammatory bowel disease. Nat. Rev. Immunol. 20 (7), 411–426. doi: 10.1038/s41577-019-0268-7 PubMed DOI

Chang J., Leong R. W., Wasinger V. C., Ip M., Yang M., Phan T. G. (2017). Impaired intestinal permeability contributes to ongoing bowel symptoms in patients with inflammatory bowel disease and mucosal healing. Gastroenterology 153 (3), 723–31.e1. doi: 10.1053/j.gastro.2017.05.056 PubMed DOI

Chang H.-W., Yan D., Singh R., Liu J., Lu X., Ucmak D., et al. (2018). Alteration of the cutaneous microbiome in psoriasis and potential role in Th17 polarization. Microbiome 6 (1), 1–27. doi: 10.1186/s40168-018-0533-1 PubMed DOI PMC

Chen Y.-J., Lee W.-H., Ho H. J., Tseng C.-H., Wu C.-Y. (2021). An altered fecal microbial profiling in rosacea patients compared to matched controls. J. Formosan Med. Assoc. 120 (1), 256–264. doi: 10.1016/j.jfma.2020.04.034 PubMed DOI

Chng K. R., Tay A. S. L., Li C., Ng A. H. Q., Wang J., Suri B. K., et al. (2016). Whole metagenome profiling reveals skin microbiome-dependent susceptibility to atopic dermatitis flare. Nat. Microbiol. 1 (9), 1–10. doi: 10.1038/nmicrobiol.2016.106 PubMed DOI

Clark C., Kountouri A., MacKinder M., Hansen R., Russell R., Gerasimidis K. (2016). “Intestinal fatty acid binding protein as a biomarker of intestinal damage in children with coeliac and crohn's disease,” in Journal of crohns & Colitis (England: Oxford univ press great Clarendon St, Oxford Ox2 6DP; ).

Cleynen I., Vermeire S. (2012). Paradoxical inflammation induced by anti-TNF agents in patients with IBD. Nat. Rev. Gastroenterol. Hepatol. 9 (9), 496–503. doi: 10.1038/nrgastro.2012.125 PubMed DOI

Conrad C., Di Domizio J., Mylonas A., Belkhodja C., Demaria O., Navarini A. A., et al. (2018). TNF blockade induces a dysregulated type I interferon response without autoimmunity in paradoxical psoriasis. Nat. Commun. 9 (1), 1–11. doi: 10.1038/s41467-017-02466-4 PubMed DOI PMC

The Human Microbiome Project Consortium (2012). Structure, function and diversity of the healthy human microbiome. Nature 486 (7402), 207. doi:  10.1038/nature11234 PubMed DOI PMC

Cossio M.-L., Genois A., Jantchou P., Hatami A., Deslandres C., McCuaig C. (2020). Skin manifestations in pediatric patients treated with a TNF-alpha inhibitor for inflammatory bowel disease: a retrospective study. J. Cutaneous Med. Surg. 24 (4), 333–339. doi: 10.1177/1203475420917387 PubMed DOI

Costello E. K., Lauber C. L., Hamady M., Fierer N., Gordon J. I., Knight R. (2009). Bacterial community variation in human body habitats across space and time. Science 326 (5960), 1694–1697. doi:  10.1126/science.1177486 PubMed DOI PMC

Coufal S., Galanova N., Bajer L., Gajdarova Z., Schierova D., Jiraskova Zakostelska Z., et al. (2019). Inflammatory bowel disease types differ in markers of inflammation, gut barrier and in specific anti-bacterial response. Cells 8 (7), 719. doi: 10.3390/cells8070719 PubMed DOI PMC

Fidder H., Schnitzler F., Ferrante M., Noman M., Katsanos K., Segaert S., et al. (2009). Long-term safety of infliximab for the treatment of inflammatory bowel disease: A single-centre cohort study. Gut 58 (4), 501–508. doi: 10.1136/gut.2008.163642 PubMed DOI

Fu Y., Lee C.-H., Chi C.-C. (2018). Association of psoriasis with inflammatory bowel disease: A systematic review and meta-analysis. JAMA Dermatol. 154 (12), 1417–1423. doi: 10.1001/jamadermatol.2018.3631 PubMed DOI PMC

Georgiou S., Pasmatzi E., Monastirli A., Tsambaos D. (2006). Cutaneous manifestations of inflammatory bowel disease. Hosp. Chronicles 1 (3), 158–168. https://scholar.google.com/scholar_lookup?journal=Hosp.+Chron.&title=Cutaneous+manifestations+of+inflammatory+bowel+disease&author=G.+Georgiou&author=E.+Pasmatzi&author=A.+Monastirli&author=D.+Tsambaos&volume=1&publication_year=2006&pages=158-168&

Grice E. A., Kong H. H., Conlan S., Deming C. B., Davis J., Young A. C., et al. (2009). Topographical and temporal diversity of the human skin microbiome. Science 324 (5931), 1190–1192. doi:  10.1126/science.1171700 PubMed DOI PMC

Grice E. A., Segre J. A. (2011). The skin microbiome. Nat. Rev. Microbiol. 9 (4), 244–253. doi: 10.1038/nrmicro2537 PubMed DOI PMC

Harbord M., Annese V., Vavricka S. R., Allez M., Barreiro-de Acosta M., Boberg K. M., et al. (2016). The first European evidence-based consensus on extra-intestinal manifestations in inflammatory bowel disease. J. Crohn's Colitis. 10 (3), 239–254. doi: 10.1093/ecco-jcc/jjv213 PubMed DOI PMC

Harvey R., Bradshaw J. (1980). A simple index of crohn's-disease activity. Lancet 315 (8167), 514. doi: 10.1016/S0140-6736(80)92767-1 PubMed DOI

Hold G. L., Smith M., Grange C., Watt E. R., El-Omar E. M., Mukhopadhya I. (2014). Role of the gut microbiota in inflammatory bowel disease pathogenesis: What have we learnt in the past 10 years? World J. Gastroenterol.: WJG 20 (5), 1192. doi:  10.3748/wjg.v20.i5.1192 PubMed DOI PMC

Ho N. T., Li F., Wang S., Kuhn L. (2019). metamicrobiomeR: An r package for analysis of microbiome relative abundance data using zero-inflated beta GAMLSS and meta-analysis across studies using random effects models. BMC Bioinf. 20 (1), 1–15. doi: 10.1186/s12859-019-2744-2 PubMed DOI PMC

Huang B. L., Chandra S., Shih D. Q. (2012). Skin manifestations of inflammatory bowel disease. Front. Physiol. 3, 13. doi: 10.3389/fphys.2012.00013 PubMed DOI PMC

Jarkovský J., Benešová K., Hejduk K., Dušek L., Lukáš M. (2017). Epidemiologie, hospitalizační léčba a migrace IBD pacientů za specializovanou péčí v České republice. Gastroenterol. Hepatol. 71 (6), 501–509. doi:  10.14735/amgh2017501 DOI

Koerner R. J., Goodfellow M., Jones A. L. (2009). The genus dietzia: a new home for some known and emerging opportunist pathogens. FEMS Immunol. Med. Microbiol. 55 (3), 296–305. doi: 10.1111/j.1574-695X.2008.00513.x PubMed DOI

Ko J K., Auyeung K K. (2014). Inflammatory bowel disease: etiology, pathogenesis and current therapy. Curr. Pharm. Des. 20 (7), 1082–1096. doi: 10.2174/13816128113199990416 PubMed DOI

Kong H. H., Oh J., Deming C., Conlan S., Grice E. A., Beatson M. A., et al. (2012). Temporal shifts in the skin microbiome associated with disease flares and treatment in children with atopic dermatitis. Genome Res. 22 (5), 850–859. doi: 10.1101/gr.131029.111 PubMed DOI PMC

Kornbluth A. (1998). Infliximab approved for use in crohn's disease: a report on the FDA GI advisory committee conference. Inflammatory Bowel Diseases 4 (4), 328–329. doi: 10.1097/00054725-199811000-00014 PubMed DOI

Lee C. H., Lui D. T. W., Lam K. S. L. (2021). Adipocyte fatty acid-binding protein, cardiovascular diseases and mortality. Front. Immunol. 12, 589206. doi: 10.3389/fimmu.2021.589206 PubMed DOI PMC

Logan M., MacKinder M., Clark C. M., Kountouri A., Jere M., Ijaz U. Z., et al. (2022). Intestinal fatty acid binding protein is a disease biomarker in paediatric coeliac disease and crohn's disease. BMC Gastroenterol. 22 (1), 260. doi: 10.1186/s12876-022-02334-6 PubMed DOI PMC

Lolli E., Saraceno R., Calabrese E., Ascolani M., Scarozza P., Chiricozzi A., et al. (2015). Psoriasis phenotype in inflammatory bowel disease: a case-control prospective study. J. Crohn's Colitis. 9 (9), 699–707. doi: 10.1093/ecco-jcc/jjv068 PubMed DOI

Maaser C., Sturm A., Vavricka S. R., Kucharzik T., Fiorino G., Annese V., et al. (2019). ECCO-ESGAR guideline for diagnostic assessment in IBD part 1: Initial diagnosis, monitoring of known IBD, detection of complications. J. Crohn's Colitis 13 (2), 144–64K. doi: 10.1093/ecco-jcc/jjy113 PubMed DOI

Magnusson M. K., Strid H., Sapnara M., Lasson A., Bajor A., Ung K.-A., et al. (2016). Anti-TNF therapy response in patients with ulcerative colitis is associated with colonic antimicrobial peptide expression and microbiota composition. J. Crohn's Colitis. 10 (8), 943–952. doi: 10.1093/ecco-jcc/jjw051 PubMed DOI

Mayslich C., Grange P., Dupin N. (2021). Cutibacterium acnes as an opportunistic pathogen: An update of its virulence-associated factors. Microorganisms 9, 303. doi:  10.3390/microorganisms9020303 PubMed DOI PMC

Mocci G., Marzo M., Papa A., Armuzzi A., Guidi L. (2013). Dermatological adverse reactions during anti-TNF treatments: Focus on inflammatory bowel disease. J. Crohn's Colitis. 7 (10), 769–779. doi: 10.1016/j.crohns.2013.01.009 PubMed DOI

Moschen A., Kaser A., Enrich B., Ludwiczek O., Gabriel M., Obrist P., et al. (2005). The RANKL/OPG system is activated in inflammatory bowel disease and relates to the state of bone loss. Gut 54 (4), 479–487. doi: 10.1136/gut.2004.044370 PubMed DOI PMC

Murdoch D. (1998). Gram-positive anaerobic cocci. Clin. Microbiol. Rev. 11 (1), 81–120. doi: 10.1128/CMR.11.1.81 PubMed DOI PMC

Navaratnam J., Dedi L., Tjølsen A. M., Bragadottir R. (2018). Identification of dietzia species in a patient with endophthalmitis following penetrating injury with retained intraocular metallic foreign body. Case Rep. Infect. Dis. 2018, 3027846. doi: 10.1155/2018/3027846 PubMed DOI PMC

Nehring P., Przybyłkowski A. (2020). Is psoriasis treatment a risk factor for inflammatory bowel disease? Pharm. Med. 34, 257–262. doi:  10.1007/s40290-020-00340-1 PubMed DOI PMC

Nigam G. B., Bhandare A. P., Antoniou G. A., Limdi J. K. (2021). Systematic review and meta-analysis of dermatological reactions in patients with inflammatory bowel disease treated with anti-tumour necrosis factor therapy. Eur. J. Gastroenterol. Hepatol. 33 (3), 346–357. doi: 10.1097/MEG.0000000000001917 PubMed DOI

Noll M., Jäger M., Lux L., Buettner C., Axt-Gadermann M. (2021). Improvement of atopic dermatitis by synbiotic baths. Microorganisms 9 (3), 527. doi: 10.3390/microorganisms9030527 PubMed DOI PMC

Oh J., Byrd A. L., Deming C., Conlan S., Kong H. H., Segre J. A. (2014). Biogeography and individuality shape function in the human skin metagenome. Nature 514 (7520), 59–64. doi:  10.1038/nature13786 PubMed DOI PMC

Otto M. (2009). Staphylococcus epidermidis–the'accidental'pathogen. Nat. Rev. Microbiol. 7 (8), 555–567. doi: 10.1038/nrmicro2182 PubMed DOI PMC

Otto M. (2010). Staphylococcus colonization of the skin and antimicrobial peptides. Expert Rev. Dermatol. 5 (2), 183–195. doi: 10.1586/edm.10.6 PubMed DOI PMC

Owczarczyk-Saczonek A., Czerwiñska J., Orylska M., Placek W. (2020). Effect of methotrexate treatment on the expression of epidermal-fatty acid-binding protein (E-FABP) and apolipoproteins in patients with psoriasis. Adv. Dermatol. Allergology/Postȩpy Dermatologii i Alergologii. 37 (3), 401. doi: 10.5114/ada.2020.96109 PubMed DOI PMC

Packey C., Sartor R. (2008). Interplay of commensal and pathogenic bacteria, genetic mutations, and immunoregulatory defects in the pathogenesis of inflammatory bowel diseases. J. Internal Med. 263 (6), 597–606. doi: 10.1111/j.1365-2796.2008.01962.x PubMed DOI

Pittayanon R., Lau J. T., Leontiadis G. I., Tse F., Yuan Y., Surette M., et al. (2020). Differences in gut microbiota in patients with vs without inflammatory bowel diseases: A systematic review. Gastroenterology 158 (4), 930–46.e1. doi: 10.1053/j.gastro.2019.11.294 PubMed DOI

Pujada A., Walter L., Patel A., Bui T. A., Zhang Z., Zhang Y., et al. (2017). Matrix metalloproteinase MMP9 maintains epithelial barrier function and preserves mucosal lining in colitis associated cancer. Oncotarget 8 (55), 94650. doi: 10.18632/oncotarget.21841 PubMed DOI PMC

Ruder B., Atreya R., Becker C. (2019). Tumour necrosis factor alpha in intestinal homeostasis and gut related diseases. Int. J. Mol. Sci. 20 (8), 1887. doi: 10.3390/ijms20081887 PubMed DOI PMC

Ryu S., Song P. I., Seo C. H., Cheong H., Park Y. (2014). Colonization and infection of the skin by s. aureus: immune system evasion and the response to cationic antimicrobial peptides. Int. J. Mol. Sci. 15 (5), 8753–8772. doi:  10.3390/ijms15058753 PubMed DOI PMC

Sankarasubramanian J., Ahmad R., Avuthu N., Singh A. B., Guda C. (2020). Gut microbiota and metabolic specificity in ulcerative colitis and crohn's disease. Front. Med. (Lausanne). 7, 606298. doi:  10.3389/fmed.2020.606298 PubMed DOI PMC

Schierova D., Roubalova R., Kolar M., Stehlikova Z., Rob F., Jackova Z., et al. (2021). Fecal microbiome changes and specific anti-bacterial response in patients with IBD during anti-TNF therapy. Cells 10 (11), 3188. doi:  10.3390/cells10113188 PubMed DOI PMC

Schroeder K. W., Tremaine W. J., Ilstrup D. M. (1987). Coated oral 5-aminosalicylic acid therapy for mildly to moderately active ulcerative colitis. New Engl. J. Med. 317 (26), 1625–1629. doi:  10.1056/NEJM198712243172603 PubMed DOI

Schumann R. R., Zweigner J. (1999). A novel acute-phase marker: lipopolysaccharide binding protein (LBP). Clin Chem Lab Med. 37 (3), 271–4. doi:  10.1515/CCLM.1999.047. PubMed DOI

Sikora M., Stec A., Chrabaszcz M., Waskiel-Burnat A., Zaremba M., Olszewska M., et al. (2019). Intestinal fatty acid binding protein, a biomarker of intestinal barrier, is associated with severity of psoriasis. J. Clin. Med. 8 (7), 1021. doi: 10.3390/jcm8071021 PubMed DOI PMC

Skroza N., Proietti I., Pampena R., La Viola G., Bernardini N., Nicolucci F., et al. (2013). Correlations between psoriasis and inflammatory bowel diseases. Biomed. Res. Int. 2013, 983902. doi:  10.1155/2013/983902 PubMed DOI PMC

Sokol H., Leducq V., Aschard H., Pham H.-P., Jegou S., Landman C., et al. (2017). Fungal microbiota dysbiosis in IBD. Gut 66 (6), 1039–1048. doi: 10.1136/gutjnl-2015-310746 PubMed DOI PMC

Sridhar S., Maltz R. M., Boyle B., Kim S. C. (2018). Dermatological manifestations in pediatric patients with inflammatory bowel diseases on anti-TNF therapy. Inflammatory Bowel Diseases 24 (9), 2086–2092. doi: 10.1093/ibd/izy112 PubMed DOI

Stehlikova Z., Kostovcik M., Kostovcikova K., Kverka M., Juzlova K., Rob F., et al. (2019. a). Dysbiosis of skin microbiota in psoriatic patients: Co-occurrence of fungal and bacterial communities. Front. Microbiol. 10, 438. doi: 10.3389/fmicb.2019.00438 PubMed DOI PMC

Stehlikova Z., Kostovcikova K., Kverka M., Rossmann P., Dvorak J., Novosadova I., et al. (2019. b). Crucial role of microbiota in experimental psoriasis revealed by a gnotobiotic mouse model. Front. Microbiol. 10, 236. doi: 10.3389/fmicb.2019.00236 PubMed DOI PMC

Stehlikova Z., Tlaskal V., Galanova N., Roubalova R., Kreisinger J., Dvorak J., et al. (2019. c). Oral microbiota composition and antimicrobial antibody response in patients with recurrent aphthous stomatitis. Microorganisms 7 (12), 636. doi: 10.3390/microorganisms7120636 PubMed DOI PMC

Swidsinski A., Loening-Baucke V., Vaneechoutte M., Doerffel Y. (2008). Active crohn's disease and ulcerative colitis can be specifically diagnosed and monitored based on the biostructure of the fecal flora. Inflammation Bowel Dis. 14 (2), 147–161. doi: 10.1002/ibd.20330 PubMed DOI

Takahashi T., Gallo R. L. (2017). The critical and multifunctional roles of antimicrobial peptides in dermatology. Dermatologic clinics. 35 (1), 39–50. doi: 10.1016/j.det.2016.07.006 PubMed DOI

Tlaskalová-Hogenová H., Štěpánková R., Kozáková H., Hudcovic T., Vannucci L., Tučková L., et al. (2011). The role of gut microbiota (commensal bacteria) and the mucosal barrier in the pathogenesis of inflammatory and autoimmune diseases and cancer: contribution of germ-free and gnotobiotic animal models of human diseases. Cell. Mol. Immunol. 8 (2), 110–120. doi: 10.1038/cmi.2010.67 PubMed DOI PMC

Vasudevan A., Gibson P. R., Van Langenberg D. R. (2017). Time to clinical response and remission for therapeutics in inflammatory bowel diseases: What should the clinician expect, what should patients be told? World J. Gastroenterol. 23 (35), 6385. doi: 10.3748/wjg.v23.i35.6385 PubMed DOI PMC

Vavricka S. R., Brun L., Ballabeni P., Pittet V., Vavricka B. M. P., Zeitz J., et al. (2011). Frequency and risk factors for extraintestinal manifestations in the Swiss inflammatory bowel disease cohort. Off. J. Am. Coll. Gastroenterol.| ACG. 106 (1), 110–119. doi: 10.1038/ajg.2010.343 PubMed DOI

Vlachos C., Gaitanis G., Katsanos K. H., Christodoulou D. K., Tsianos E., Bassukas I. D. (2016). Psoriasis and inflammatory bowel disease: Links and risks. Psoriasis (Auckland NZ). 6, 73–92. doi:  10.2147/PTT.S85194 PubMed DOI PMC

Wall I. B., Davies C. E., Hill K. E., Wilson M. J., Stephens P., Harding K. G., et al. (2002). Potential role of anaerobic cocci in impaired human wound healing. Wound Repair Regeneration 10 (6), 346–353. doi: 10.1046/j.1524-475X.2002.t01-1-10602.x PubMed DOI

Wang R., Farhat M., Na J., Li R., Wu Y. (2020). Bacterial and fungal microbiome characterization in patients with rosacea and healthy controls. Br. J. Dermatol. doi: 10.1111/bjd.19315 PubMed DOI

Watarai A., Amoh Y., Maejima H., Hamada Y., Katsuoka K. (2013). Nestin expression is increased in the suprabasal epidermal layer in psoriasis vulgaris. Acta dermato-venereologica. 93 (1), 39–43. doi: 10.2340/00015555-1420 PubMed DOI

Wildeboer-Veloo A., Harmsen H., Welling G., Degener J. (2007). Development of 16S rRNA-based probes for the identification of gram-positive anaerobic cocci isolated from human clinical specimens. Clin. Microbiol. Infect. 13 (10), 985–992. doi: 10.1111/j.1469-0691.2007.01803.x PubMed DOI

Winter J., Wenghoefer M. (2012). Human defensins: Potential tools for clinical applications. Polymers 4 (1), 691–709. doi: 10.3390/polym4010691 DOI

Wu D. C., Chan W. W., Metelitsa A. I., Fiorillo L., Lin A. N. (2011). Pseudomonas skin infection. Am. J. Clin. Dermatol. 12 (3), 157–169. doi: 10.2165/11539770-000000000-00000 PubMed DOI

Yin D., Hao J., Jin R., Yi Y., Bodduluri S. R., Hua Y., et al. (2022). Epidermal fatty Acid Binding protein mediates depilatory-induced acute skin inflammation. J. Invest. Dermatol. 142 (7), 1824–34.e7. doi: 10.1016/j.jid.2021.11.040 PubMed DOI PMC

Yost J., Gudjonsson J. E. (2009). The role of TNF inhibitors in psoriasis therapy: New implications for associated comorbidities. F1000 Med. Rep. 1, 30. doi: 10.3410/M1-30 PubMed DOI PMC

Nejnovějších 20 citací...

Zobrazit více v
Medvik | PubMed

Paradoxical Reactions to Anti-TNFα and Anti-IL-17 Treatment in Psoriasis Patients: Are Skin and/or Gut Microbiota Involved?

. 2023 Apr ; 13 (4) : 911-933. [epub] 20230315

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...