Characterization of the Oral and Gut Microbiota in Patients with Psoriatic Diseases: A Systematic Review

Authors

  • Tanja Todberg Department of Dermatology and Allergy, Herlev and Gentofte Hospital, University of Copenhagen, DK-2900 Hellerup, Denmark
  • Hannah Kaiser
  • Claus Zachariae
  • Alexander Egeberg
  • Anne-Sofie Halling-Overgaard
  • Lone Skov

DOI:

https://doi.org/10.2340/00015555-3882

Keywords:

psoriasis, psoriatic arthritis, microbiota, immune system, probiotics

Abstract

Advances in technology have led to an increased number of studies investigating the microbiome in patients with psoriasis. This systematic review examined data regarding the oral and gut microbiota in patients with psoriasis and/or psoriatic arthritis and the effect of probiotics on the microbiota and severity of psoriasis. Of 1,643 studies, 23 were included (22 observational, 1 interventional). Studies examined the microbiota using culture or 16S rRNA gene sequencing analysis. All culture-based studies identified an increased presence of oral Candida in patients with psoriasis, whereas small variations in the oral microbiota were found in a 16S rRNA gene-based study. All 16S rRNA gene sequencing based studies agreed that the gut microbiota of patients with psoriatic disease differed from that of healthy controls, but the results were heterogeneous. Probiotics were associated with a significant improvement in the severity of psoriasis, but did not change microbiota. Overall, studies lacked relevant inclusion criteria and baseline information. In conclusion, the role of the microbiota in patients with psoriasis requires further investigation using more robust methods.

Downloads

Download data is not yet available.

References

Parisi R, Iskandar IYK, Kontopantelis E, Augustin M, Griffiths CEM, Ashcroft DM. National, regional, and worldwide epidemiology of psoriasis: systematic analysis and modelling study. BMJ 2020; 369: m1590.

Alinaghi F, Tekin HG, Burisch J, Wu JJ, Thyssen JP, Egeberg A. Global prevalence and bidirectional association between psoriasis and inflammatory bowel disease – a systematic review and meta-analysis. J Crohn’s Colitis 2020; 14: 351–360.

Griffiths CEM, Armstrong AW, Gudjonsson JE, Barker JNWN. Psoriasis. Vol. 397, Lancet 2021; 397: 1301–1315.

Lynch S V., Pedersen O. The human intestinal microbiome in health and disease. N Engl J Med 2016; 375: 2369–2379.

Zákostelská Z, Málková J, Klimešová K, Rossmann P, Hornová M, Novosádová I, et al. Intestinal microbiota promotes psoriasis-like skin inflammation by enhancing Th17 response. PLoS One 2016; 11: e0159539.

Zanvit P, Konkel JE, Jiao X, Kasagi S, Zhang D, Wu R, et al. Antibiotics in neonatal life increase murine susceptibility to experimental psoriasis. Nat Commun 2015; 6: 2824.

Mas-Lloret J, Obón-Santacana M, Ibáñez-Sanz G, Guinó E, Pato ML, Rodriguez-Moranta F, et al. Gut microbiome diversity detected by high-coverage 16S and shotgun sequencing of paired stool and colon sample. Sci Data 2020; 7: 92.

Egeberg A, Mallbris L, Gislason G, Hansen PR, Mrowietz U. Risk of periodontitis in patients with psoriasis and psoriatic arthritis. J Eur Acad Dermatology Venereol 2017; 31: 288–293.

Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gøtzsche PC, Ioannidis JPA, et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: explanation and elaboration. BMJ 2009; 339: b2700.

Higgins JPT, Altman DG, Gøtzsche PC, Jüni P, Moher D, Oxman AD, et al. The Cochrane Collaboration’s tool for assessing risk of bias in randomised trials. BMJ 2011; 343: d5928.

Taheri Sarvtin M, Shokohi T, Hajheydari Z, Yazdani J, Hedayati MT. Evaluation of candidal colonization and specific humoral responses against Candida albicans in patients with psoriasis. Int J Dermatol 2014; 53: e555–560.

Codoñer FM, Ramírez-Bosca A, Climent E, Carrión-Gutierrez M, Guerrero M, Pérez-Orquín JM, et al. Gut microbial composition in patients with psoriasis. Sci Rep 2018; 8: 3812.

Waldman A, Gilhar A, Duek L, Berdicevsky I. Incidence of Candida in psoriasis–a study on the fungal flora of psoriatic patients. Mycoses 2001; 44: 77–81.

Scher JU, Ubeda C, Artacho A, Attur M, Isaac S, Reddy SM, et al. Decreased bacterial diversity characterizes the altered gut microbiota in patients with psoriatic arthritis, resembling dysbiosis in inflammatory bowel disease. Arthritis Rheumatol 2015; 67: 128–139.

Eppinga H, Thio HB, Schreurs MWJ, Blakaj B, Tahitu RI, Konstantinov SR, et al. Depletion of Saccharomyces cerevisiae in psoriasis patients, restored by Dimethylfumarate therapy (DMF). PLoS One 2017; 12: e0176955.

Hidalgo-Cantabrana C, Gomez J, Delgado S, Requena-Lopez S, Queiro-Silva R, Margolles A, et al. Gut microbiota dysbiosis in a cohort of patients with psoriasis. Br J Dermatol 2019; 181: 1287–1295.

Huang L, Gao R, Yu N, Zhu Y, Ding Y, Qin H. Dysbiosis of gut microbiota was closely associated with psoriasis. Sci China Life Sci 2019; 62: 807–815.

Chen Y-J, Ho HJ, Tseng C-H, Lai Z-L, Shieh J-J, Wu C-Y. Intestinal microbiota profiling and predicted metabolic dysregulation in psoriasis patients. Exp Dermatol 2018; 27: 1336–1343.

Yeh N-L, Hsu C-Y, Tsai T-F, Chiu H-Y. Gut microbiome in psoriasis is perturbed differently during secukinumab and ustekinumab therapy and associated with response to treatment. Clin Drug Investig 2019; 39: 1195–203.

Dei-Cas I, Giliberto F, Luce L, Dopazo H, Penas-Steinhardt A. Metagenomic analysis of gut microbiota in non-treated plaque psoriasis patients stratified by disease severity: development of a new Psoriasis-Microbiome Index. Sci Rep 2020; 10: 12754.

Yegorov S, Babenko D, Kozhakhmetov S, Akhmaltdinova L, Kadyrova I, Nurgozhina A, et al. Psoriasis Is associated with elevated gut IL-1α and intestinal microbiome alterations. Front Immunol 2020; 11: 571319.

Zhang X, Shi L, Sun T, Guo K, Geng S. Dysbiosis of gut microbiota and its correlation with dysregulation of cytokines in psoriasis patients. BMC Microbiol 2021; 21: 78.

Wang X, Zhai W, Ma J, Xu S, Liu M, Zhang X, et al. Substantial alterations of the intestinal microbiota in psoriasis patients of China. Exp Dermatol 2021 Feb 3. [Online ahead of print].

Lesan S, Toosi R, Aliakbarzadeh R, Daneshpazhooh M, Mahmoudi L, Tavakolpour S, et al. Oral Candida colonization and plaque type psoriasis: is there any relationship? J Investig Clin Dent 2018; 9: e12335.

Tan L, Zhao S, Zhu W, Wu L, Li J, Shen M, et al. The Akkermansia muciniphila is a gut microbiota signature in psoriasis. Exp Dermatol 2018; 27 : 144–149.

Navarro-Lopez V, Martinez-Andres A, Ramirez-Bosca A, Ruzafa-Costas B, Nunez-Delegido E, Carrion-Gutierrez MA, et al. Efficacy and safety of oral administration of a mixture of probiotic strains in patients with psoriasis: a randomized controlled clinical trial. Acta Derm Venereol 2019; 99: 1078–1084.

Eppinga H, Sperna Weiland CJ, Thio HB, van der Woude CJ, Nijsten TEC, Peppelenbosch MP, et al. Similar depletion of protective Faecalibacterium prausnitzii in psoriasis and inflammatory bowel disease, but not in hidradenitis suppurativa. J Crohns Colitis 2016; 10: 1067–1075.

Buslau M, Menzel I, Holzmann H. Fungal flora of human faeces in psoriasis and atopic dermatitis. Mycoses 1990; 33: 90–94.

Bedair AA, Darwazeh AMG, Al-Aboosi MM. Oral Candida colonization and candidiasis in patients with psoriasis. Oral Surg Oral Med Oral Pathol Oral Radiol 2012; 114: 610–615.

Belstrom D, Eiberg JM, Enevold C, Grande MA, Jensen CAJ, Skov L, et al. Salivary microbiota and inflammation-related proteins in patients with psoriasis. Oral Dis 2020; 26: 677–687.

Shapiro J, Cohen NA, Shalev V, Uzan A, Koren O, Maharshak N, et al. Psoriatic patients have a distinct structural and functional fecal microbiota compared with controls. J Dermatol 2019; 46: 595–603.

Manasson J, Wallach DS, Guggino G, Stapylton M, Badri MH, Solomon G, et al. IL-17 Inhibition in spondyloarthritis associates with subclinical gut microbiome perturbations and a distinctive IL-25-driven intestinal inflammation. Arthritis Rheumatol 2019; 72: 645-657.

Smith G, Blackwell C, Nuki G. Faecal flora in spondyloarthropathy. Br J Rheumatol 1997; 36: 850–854.

Navarro-Lopez V, Martinez-Andres A, Ramirez-Bosca A, Ruzafa-Costas B, Nunez-Delegido E, Carrion-Gutierrez MA, et al. Efficacy and safety of oral administration of a mixture of probiotic strains in patients with psoriasis: a randomized controlled clinical trial. Acta Derm Venereol 2019; 99: 1078–1084.

Saunte DM, Mrowietz U, Puig L, Zachariae C. Candida infections in patients with psoriasis and psoriatic arthritis treated with interleukin-17 inhibitors and their practical management. Br J Dermatol 2017; 177: 47–62.

Duarte PM, Nogueira CFP, Silva SM, Pannuti CM, Schey KC, Miranda TS. Impact of Smoking Cessation on Periodontal Tissues. Int Dental J 2021 Feb 27 [Online ahead of print].

Gomes-Filho IS, Santos PNP, Cruz SS, Figueiredo ACMG, Trindade SC, Ladeia AM, et al. Periodontitis and its higher levels of severity are associated with the triglyceride/high density lipoprotein cholesterol (TG/HDL-C) ratio. J Periodontol 2021 Mar 10 [Online ahead of print].

Vieira Colombo AP, Magalhães CB, Hartenbach FARR, Martins do Souto R, Maciel da Silva-Boghossian C. Periodontal-disease-associated biofilm: a reservoir for pathogens of medical importance. Microb Pathog 2016; 94: 27–34.

Van Ende M, Wijnants S, Van Dijck P. Sugar sensing and signaling in Candida albicans and Candida glabrata. Front Microbiol 2019; 10: 99.

Alam MT, Amos GCA, Murphy ARJ, Murch S, Wellington EMH, Arasaradnam RP. Microbial imbalance in inflammatory bowel disease patients at different taxonomic levels. Gut Pathog 2020; 12: 1.

Matsuoka K, Kanai T. The gut microbiota and inflammatory bowel disease. Semin Immunopathol 2015; 37: 47–55.

Koren O, Knights D, Gonzalez A, Waldron L, Segata N, Knight R, et al. A guide to enterotypes across the human body: meta-analysis of microbial community structures in human microbiome datasets. PLoS Comput Biol 2013; 9: e1002863.

Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley RE, et al. A core gut microbiome in obese and lean twins. Nature 2009; 457: 480–484.

Fan Y, Pedersen O. Gut microbiota in human metabolic health and disease. Nature Rev Microbiol 2020; 19: 55–71.

Jensen P, Zachariae C, Christensen R, Geiker NRW, Schaadt BK, Stender S, et al. Effect of weight loss on the severity of psoriasis: a randomized clinical study. JAMA Dermatol 2013; 149: 795–801.

Seregin SS, Golovchenko N, Schaf B, Chen J, Pudlo NA, Mitchell J, et al. NLRP6 protects Il10−/− mice from colitis by limiting colonization of Akkermansia muciniphila. Cell Rep 2017; 19: 733–745.

Ganesh BP, Klopfleisch R, Loh G, Blaut M. Commensal Akkermansia muciniphila exacerbates gut inflammation in Salmonella typhimurium-infected gnotobiotic mice. PLoS One 2013; 8: 74963.

Ramírez-Boscá A, Navarro-López V, Martínez-Andrés A, Such J, Francés R, De La Parte J, et al. Identification of bacterial DNA in the peripheral blood of patientswith active psoriasis. JAMA Dermatol 2015; 151: 670–671.

Munch Roager H, Vogt JK, Kristensen M, Hansen LBS, Ibrügger S, Maerkedahl RB, et al. Whole grain-rich diet reduces body weight and systemic low-grade inflammation without inducing major changes of the gut microbiome: a randomised cross-over trial. Gut 2019; 68: 83–93.

Trastoy B, Naegeli A, Anso I, Sjögren J, Guerin ME. Structural basis of mammalian mucin processing by the human gut O-glycopeptidase OgpA from Akkermansia muciniphila. Nat Commun 2020; 11: 1–14.

Dao MC, Everard A, Aron-Wisnewsky J, Sokolovska N, Prifti E, Verger EO, et al. Akkermansia muciniphila and improved metabolic health during a dietary intervention in obesity: relationship with gut microbiome richness and ecology. Gut 2016; 65: 426–436.

Duscha A, Gisevius B, Hirschberg S, Yissachar N, Stangl GI, Eilers E, et al. Propionic acid shapes the multiple sclerosis disease course by an immunomodulatory mechanism. Cell 2020; 180: 1067–1080.

Venegas DP, De La Fuente MK, Landskron G, González MJ, Quera R, Dijkstra G, et al. Short chain fatty acids (SCFAs)mediated gut epithelial and immune regulation and its relevance for inflammatory bowel diseases. Front Immunol 2019; 10: 277.

Schwarz A, Philippsen R, Schwarz T. Induction of regulatory t cells and correction of cytokine disbalance by short-chain fatty acids: implications for psoriasis therapy. J Invest Dermatol 2020; 141: 95–104.

David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature 2014; 505: 559–563.

Sender R, Fuchs S, Milo R. Are we really vastly outnumbered? Revisiting the ratio of bacterial to host cells in humans. Cell 2016; 164: 337–340.

Kristensen NB, Bryrup T, Allin KH, Nielsen T, Hansen TH, Pedersen O. Alterations in fecal microbiota composition by probiotic supplementation in healthy adults: a systematic review of randomized controlled trials. Genome Med 2016; 8: 52.

Laursen MF, Laursen RP, Larnkjær A, Michaelsen KF, Bahl MI, Licht TR. Administration of two probiotic strains during early childhood does not affect the endogenous gut microbiota composition despite probiotic proliferation. BMC Microbiol 2017; 17: 175.

Knight R, Vrbanac A, Taylor BC, Aksenov A, Callewaert C, Debelius J, et al. Best practices for analysing microbiomes. Nature Rev Microbiol 2018; 16: 410–422.

Forslund K, Hildebrand F, Nielsen T, Falony G, Le Chatelier E, Sunagawa S, et al. Disentangling type 2 diabetes and metformin treatment signatures in the human gut microbiota. Nature 2015; 528: 262–266.

Imhann F, Bonder MJ, Vila AV, Fu J, Mujagic Z, Vork L, et al. Proton pump inhibitors affect the gut microbiome. Gut 2016; 65: 740–748.

Donaldson GP, Lee SM, Mazmanian SK. Gut biogeography of the bacterial microbiota. Nature Rev Microbiol 2015; 14: 20–32.

Graspeuntner S, Loeper N, Künzel S, Baines JF, Rupp J. Selection of validated hypervariable regions is crucial in 16S-based microbiota studies of the female genital tract. Sci Rep 2018; 8: 9678.

Fouhy F, Clooney AG, Stanton C, Claesson MJ, Cotter PD. 16S rRNA gene sequencing of mock microbial populations-impact of DNA extraction method, primer choice and sequencing platform. BMC Microbiol 2016; 16: 123.

Teng F, Darveekaran Nair SS, Zhu P, Li S, Huang S, Li X, et al. Impact of DNA extraction method and targeted 16S-rRNA hypervariable region on oral microbiota profiling. Sci Rep 2018; 8: 16321.

Van Rossum T, Ferretti P, Maistrenko OM, Bork P. Diversity within species: interpreting strains in microbiomes. Nature Rev Microbiol 2020; 18: 491–506.

Mills S, Shanahan F, Stanton C, Hill C, Coffey A, Ross RP. Movers and shakers. Gut Microbes 2013; 4: 4–16.

Additional Files

Published

2021-07-30

How to Cite

Todberg, T., Kaiser, H., Zachariae, C., Egeberg, A., Halling-Overgaard, A.-S., & Skov, L. (2021). Characterization of the Oral and Gut Microbiota in Patients with Psoriatic Diseases: A Systematic Review. Acta Dermato-Venereologica, 101(7), adv00512. https://doi.org/10.2340/00015555-3882