Current Dermatology Reports

, Volume 6, Issue 2, pp 94–103 | Cite as

The Role of the Skin and Gut Microbiome in Psoriatic Disease

  • Di Yan
  • Naiem Issa
  • Ladan Afifi
  • Caleb Jeon
  • Hsin-Wen Chang
  • Wilson Liao
Psoriasis (J Wu, Section Editor)
Part of the following topical collections:
  1. Topical Collection on Psoriasis

Abstract

Purpose of Review

To understand the changes in the microbiome in psoriatic disease, we conducted a systematic review of studies comparing the skin and gut microbiota in psoriatic individuals and healthy controls.

Recent Findings

Our review of studies pertaining to the cutaneous microbiome showed a trend towards an increased relative abundance of Streptococcus and a decreased level of Propionibacterium in psoriasis patients compared to controls. In the gut microbiome, the ratio of Firmicutes and Bacteroidetes was perturbed in psoriatic individuals compared to healthy controls. Actinobacteria was also relatively underrepresented in psoriasis patients relative to healthy individuals.

Summary

Although the field of the psoriatic microbiome is relatively new, these first studies reveal interesting differences in microbiome composition that may be associated with the development of psoriatic comorbidities and serve as novel therapeutic targets.

Keywords

Microbiome Skin microbiota Gut bacteria Mycobiome Psoriasis Psoriatic arthritis 

Notes

Acknowledgments

This study was supported in part by grants to Wilson Liao (NIH R01 AR065174, NIH U01 AI119125, National Psoriasis Foundation Translational Research Award). Dr. Liao is also grateful for charitable support from the Dinsmore family. Di Yan acknowledges support from a National Psoriasis Foundation Fellowship.

Compliance with Ethical Standards

Conflict of Interest

Authors Wilson Liao, Di Yan, Ladan Afifi, Caleb Jeon, and Hsin-Win Chang report no conflicts of interest in this work.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

References

Papers of Particular Interest, Published Recently, Have Been Highlighted as: • of Importance

  1. 1.
    Clements SJ, Carding SR. Diet, the intestinal microbiota and immune health in ageing. Crit Rev food Sci Nutr. 2016; doi:10.1080/10408398.2016.1211086.PubMedGoogle Scholar
  2. 2.
    Cheng J, Palva AM, de Vos WM, et al. Contribution of the intestinal microbiota to human health: from birth to 100 years of age. Curr Top Microbiol Immunol. 2013;358:323–46. doi:10.1007/82_2011_189.PubMedGoogle Scholar
  3. 3.
    Scher JU, Littman DR, Abramson SB. Microbiome in inflammatory arthritis and human rheumatic diseases. Arthritis & Rheumatology (Hoboken, NJ). 2016;68(1):35–45. doi:10.1002/art.39259.CrossRefGoogle Scholar
  4. 4.
    Cho I, Blaser MJ. The human microbiome: at the interface of health and disease. Nat Rev Genet. 2012;13(4):260–70. doi:10.1038/nrg3182.PubMedPubMedCentralGoogle Scholar
  5. 5.
    David LA, Materna AC, Friedman J, et al. Host lifestyle affects human microbiota on daily timescales. Genome Biol. 2014;15(7):R89. doi:10.1186/gb-2014-15-7-r89.CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Salim SY, Kaplan GG, Madsen KL. Air pollution effects on the gut microbiota: a link between exposure and inflammatory disease. Gut Microbes. 2014;5(2):215–9. doi:10.4161/gmic.27251.CrossRefPubMedGoogle Scholar
  7. 7.
    Yeoh N, Burton JP, Suppiah P, et al. The role of the microbiome in rheumatic diseases. Curr Rheumatol Rep. 2013;15(3):314. doi:10.1007/s11926-012-0314-y.CrossRefPubMedGoogle Scholar
  8. 8.
    Longman RS, Littman DR. The functional impact of the intestinal microbiome on mucosal immunity and systemic autoimmunity. Curr Opin Rheumatol. 2015;27(4):381–7. doi:10.1097/bor.0000000000000190.CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Costello EK, Lauber CL, Hamady M, et al. Bacterial community variation in human body habitats across space and time. Science (New York, NY). 2009;326(5960):1694–7. doi:10.1126/science.1177486.CrossRefGoogle Scholar
  10. 10.
    Grice EA, Kong HH, Renaud G, et al. A diversity profile of the human skin microbiota. Genome Res. 2008;18(7):1043–50. doi:10.1101/gr.075549.107.CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Peterson J, Garges S, Giovanni M, et al. The NIH Human Microbiome Project. Genome Res. 2009;19(12):2317–23. doi:10.1101/gr.096651.109.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Aagaard K, Petrosino J, Keitel W, et al. The Human Microbiome Project strategy for comprehensive sampling of the human microbiome and why it matters. FASEB journal: official publication of the Federation of American Societies for Experimental Biology. 2013;27(3):1012–22. doi:10.1096/fj.12-220806.CrossRefGoogle Scholar
  13. 13.
    Fahlen A, Engstrand L, Baker BS, et al. Comparison of bacterial microbiota in skin biopsies from normal and psoriatic skin. Arch Dermatol Res. 2012;304(1):15–22. doi:10.1007/s00403-011-1189-x.CrossRefPubMedGoogle Scholar
  14. 14.
    Drago L, De Grandi R, Altomare G, et al. Skin microbiota of first cousins affected by psoriasis and atopic dermatitis. Clinical and molecular allergy : CMA. 2016;14:2. doi:10.1186/s12948-016-0038-z.CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Gao Z, Tseng CH, Strober BE, et al. Substantial alterations of the cutaneous bacterial biota in psoriatic lesions. PLoS One. 2008;3(7):e2719. doi:10.1371/journal.pone.0002719.CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Grice EA, Segre JA. The skin microbiome. Nat Rev Microbiol. 2011;9(4):244–53. doi:10.1038/nrmicro2537.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Jovel J, Patterson J, Wang W, et al. Characterization of the gut microbiome using 16S or shotgun metagenomics. Front Microbiol. 2016;7:459. doi:10.3389/fmicb.2016.00459.CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Meisel JS, Hannigan GD, Tyldsley AS, et al. Skin microbiome surveys are strongly influenced by experimental design. The Journal of investigative dermatology. 2016;136(5):947–56. doi:10.1016/j.jid.2016.01.016.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Zakostelska Z, Malkova J, Klimesova K, et al. Intestinal microbiota promotes psoriasis-like skin inflammation by enhancing Th17 response. PLoS One. 2016;11(7):e0159539. doi:10.1371/journal.pone.0159539.CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Horton DB, Scott FI, Haynes K, et al. Antibiotic exposure, infection, and the development of pediatric psoriasis: a nested case-control study. JAMA dermatology. 2016;152(2):191–9. doi:10.1001/jamadermatol.2015.3650.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    • Alekseyenko AV, Perez-Perez GI, De Souza A, et al. Community differentiation of the cutaneous microbiota in psoriasis. Microbiome. 2013;1(1):31. doi:10.1186/2049-2618-1-31. Here Alekseyenko et al. report the results of the largest study profiling the cutaneous microbiome in psoriasis to date. This study is also the only one to profile changes in the cutaneous microbiome after treatment for psoriasis.CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Paulino LC, Tseng CH, Strober BE, et al. Molecular analysis of fungal microbiota in samples from healthy human skin and psoriatic lesions. J Clin Microbiol. 2006;44(8):2933–41. doi:10.1128/jcm.00785-06.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Paulino LC, Tseng CH, Blaser MJ. Analysis of Malassezia microbiota in healthy superficial human skin and in psoriatic lesions by multiplex real-time PCR. FEMS Yeast Res. 2008;8(3):460–71. doi:10.1111/j.1567-1364.2008.00359.x.CrossRefPubMedGoogle Scholar
  24. 24.
    Jagielski T, Rup E, Ziolkowska A, et al. Distribution of Malassezia species on the skin of patients with atopic dermatitis, psoriasis, and healthy volunteers assessed by conventional and molecular identification methods. BMC Dermatol. 2014;14:3. doi:10.1186/1471-5945-14-3.CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Takemoto A, Cho O, Morohoshi Y, et al. Molecular characterization of the skin fungal microbiome in patients with psoriasis. J Dermatol. 2015;42(2):166–70. doi:10.1111/1346-8138.12739.CrossRefPubMedGoogle Scholar
  26. 26.
    Wolf P, Seidl H, Back B, et al. Increased prevalence of human papillomavirus in hairs plucked from patients with psoriasis treated with psoralen-UV-A. Arch Dermatol. 2004;140(3):317–24. doi:10.1001/archderm.140.3.317.CrossRefPubMedGoogle Scholar
  27. 27.
    Simeone P, Teson M, Latini A, et al. Human papillomavirus type 5 in primary keratinocytes from psoriatic skin. Exp Dermatol. 2005;14(11):824–9. doi:10.1111/j.1600-0625.2005.00358.x.CrossRefPubMedGoogle Scholar
  28. 28.
    Cronin JG, Mesher D, Purdie K, et al. Beta-papillomaviruses and psoriasis: an intra-patient comparison of human papillomavirus carriage in skin and hair. Br J Dermatol. 2008;159(1):113–9. doi:10.1111/j.1365-2133.2008.08627.x.CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Salem SA, Zuel-Fakkar NM, Fathi G, et al. Comparative study of human papilloma virus in untreated and ultraviolet-treated psoriatic patients. Photodermatology, photoimmunology & photomedicine. 2010;26(2):78–82. doi:10.1111/j.1600-0781.2010.00492.x.CrossRefGoogle Scholar
  30. 30.
    de Koning MN, Polderman MC, Waterboer T, et al. Marked differences in Betapapillomavirus DNA and antibody prevalence between patients with psoriasis and those with atopic dermatitis. Br J Dermatol. 2011;164(4):771–5. doi:10.1111/j.1365-2133.2010.10182.x.CrossRefPubMedGoogle Scholar
  31. 31.
    Bellaud G, Gheit T, Pugin A, et al. Prevalence of human papillomavirus DNA in eyebrow hairs plucked from patients with psoriasis treated with TNF inhibitors. Journal of the European Academy of Dermatology and Venereology : JEADV. 2014;28(12):1816–20. doi:10.1111/jdv.12308.CrossRefPubMedGoogle Scholar
  32. 32.
    Prignano G, Ferraro C, Mussi A, et al. Prevalence of human papilloma virus type 5 DNA in lesional and non-lesional skin scales of Italian plaque-type psoriatic patients: association with disease severity. Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases. 2005;11(1):47–51. doi:10.1111/j.1469-0691.2004.01040.x.CrossRefGoogle Scholar
  33. 33.
    Masallat D, Moemen D, State AF. Gut bacterial microbiota in psoriasis: a case control study. Afr J Microbiol Res. 2016;10(33):1337–43. doi:10.5897/AJMR2016.8046.CrossRefGoogle Scholar
  34. 34.
    • Scher JU, Ubeda C, Artacho A, et al. Decreased bacterial diversity characterizes the altered gut microbiota in patients with psoriatic arthritis, resembling dysbiosis in inflammatory bowel disease. Arthritis & rheumatology (Hoboken, NJ). 2015;67(1):128–39. doi:10.1002/art.38892. The study by Scher et al., is the only comprehensive, genus-level, profiling study of the gut microbiome in psoriatic disease to date. This study is also significant in that it correlates fecal metabolites with shifts in gut microbiome composition, providing the foundation for a mechanistic understanding of how bacteria can influence the host.CrossRefGoogle Scholar
  35. 35.
    Harwood CA, Surentheran T, McGregor JM, et al. Human papillomavirus infection and non-melanoma skin cancer in immunosuppressed and immunocompetent individuals. J Med Virol. 2000;61(3):289–97.CrossRefPubMedGoogle Scholar
  36. 36.
    Struijk L, Bouwes Bavinck JN, Wanningen P, et al. Presence of human papillomavirus DNA in plucked eyebrow hairs is associated with a history of cutaneous squamous cell carcinoma. The Journal of investigative dermatology. 2003;121(6):1531–5. doi:10.1046/j.1523-1747.2003.12632.x.CrossRefPubMedGoogle Scholar
  37. 37.
    Majewski S, Jablonska S. Do epidermodysplasia verruciformis human papillomaviruses contribute to malignant and benign epidermal proliferations? Arch Dermatol. 2002;138(5):649–54.CrossRefPubMedGoogle Scholar
  38. 38.
    Sahebjamiee M, Sand L, Karimi S, et al. Prevalence of human papillomavirus in oral lichen planus in an Iranian cohort. Journal of oral and maxillofacial pathology: JOMFP. 2015;19(2):170–4. doi:10.4103/0973-029x.164528.CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Dekio I, Hayashi H, Sakamoto M, et al. Detection of potentially novel bacterial components of the human skin microbiota using culture-independent molecular profiling. J Med Microbiol. 2005;54(Pt 12):1231–8. doi:10.1099/jmm.0.46075-0.CrossRefPubMedGoogle Scholar
  40. 40.
    Smith PM, Howitt MR, Panikov N, et al. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science (New York, NY). 2013;341(6145):569–73. doi:10.1126/science.1241165.CrossRefGoogle Scholar
  41. 41.
    Round JL, Mazmanian SK. The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol. 2009;9(5):313–23. doi:10.1038/nri2515.CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Gudjonsson JE, Thorarinsson AM, Sigurgeirsson B, et al. Streptococcal throat infections and exacerbation of chronic plaque psoriasis: a prospective study. Br J Dermatol. 2003;149(3):530–4.CrossRefPubMedGoogle Scholar
  43. 43.
    Naik S, Bouladoux N, Linehan JL, et al. Commensal-dendritic-cell interaction specifies a unique protective skin immune signature. Nature. 2015;520(7545):104–8. doi:10.1038/nature14052.CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Schirmer M, Smeekens SP, Vlamakis H, et al. Linking the human gut microbiome to inflammatory cytokine production capacity. Cell. 2016;167(4):1125–36.e8. doi:10.1016/j.cell.2016.10.020.CrossRefPubMedGoogle Scholar
  45. 45.
    Cantini F, Niccoli L, Nannini C, et al. Psoriatic arthritis: a systematic review. Int J Rheum Dis. 2010;13(4):300–17. doi:10.1111/j.1756-185X.2010.01540.x.CrossRefPubMedGoogle Scholar
  46. 46.
    Calcinaro F, Dionisi S, Marinaro M, et al. Oral probiotic administration induces interleukin-10 production and prevents spontaneous autoimmune diabetes in the non-obese diabetic mouse. Diabetologia. 2005;48(8):1565–75. doi:10.1007/s00125-005-1831-2.CrossRefPubMedGoogle Scholar
  47. 47.
    Lavasani S, Dzhambazov B, Nouri M, et al. A novel probiotic mixture exerts a therapeutic effect on experimental autoimmune encephalomyelitis mediated by IL-10 producing regulatory T cells. PLoS One. 2010;5(2):e9009. doi:10.1371/journal.pone.0009009.CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Groeger D, O’Mahony L, Murphy EF, et al. Bifidobacterium infantis 35624 modulates host inflammatory processes beyond the gut. Gut Microbes. 2013;4(4):325–39. doi:10.4161/gmic.25487.CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Wang Z, Klipfell E, Bennett BJ, et al. Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease. Nature. 2011;472(7341):57–63. doi:10.1038/nature09922.CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Koeth RA, Wang Z, Levison BS, et al. Intestinal microbiota metabolism of L-carnitine, a nutrient in red meat, promotes atherosclerosis. Nat Med. 2013;19(5):576–85. doi:10.1038/nm.3145.CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Tang WH, Wang Z, Levison BS, et al. Intestinal microbial metabolism of phosphatidylcholine and cardiovascular risk. N Engl J Med. 2013;368(17):1575–84. doi:10.1056/NEJMoa1109400.CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Cho CE, Taesuwan S, Malysheva OV, et al. Trimethylamine-N-oxide (TMAO) response to animal source foods varies among healthy young men and is influenced by their gut microbiota composition: a randomized controlled trial. Mol Nutr Food Res. 2016; doi:10.1002/mnfr.201600324.Google Scholar
  53. 53.
    Ley RE, Turnbaugh PJ, Klein S, et al. Microbial ecology: human gut microbes associated with obesity. Nature. 2006;444(7122):1022–3. doi:10.1038/4441022a.CrossRefPubMedGoogle Scholar
  54. 54.
    Duarte GV, Silva LP. Correlation between psoriasis’ severity and waist-to-height ratio. An Bras Dermatol. 2014;89(5):846–7.CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Armstrong AW, Harskamp CT, Armstrong EJ. The association between psoriasis and obesity: a systematic review and meta-analysis of observational studies. Nutrition & diabetes. 2012;2:e54. doi:10.1038/nutd.2012.26.CrossRefGoogle Scholar
  56. 56.
    Toussirot E, Aubin F, Dumoulin G. Relationships between adipose tissue and psoriasis, with or without arthritis. Front Immunol. 2014;5:368. doi:10.3389/fimmu.2014.00368.CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Abuabara K, Azfar RS, Shin DB, et al. Cause-specific mortality in patients with severe psoriasis: a population-based cohort study in the U.K. Br J Dermatol. 2010;163(3):586–92. doi:10.1111/j.1365-2133.2010.09941.x.CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Gelfand JM, Yeung H. Metabolic syndrome in patients with psoriatic disease. The Journal of rheumatology Supplement. 2012;89:24–8. doi:10.3899/jrheum.120237.CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    De Preter V, Machiels K, Joossens M, et al. Faecal metabolite profiling identifies medium-chain fatty acids as discriminating compounds in IBD. Gut. 2015;64(3):447–58. doi:10.1136/gutjnl-2013-306423.CrossRefPubMedGoogle Scholar
  60. 60.
    Kostic AD, Xavier RJ, Gevers D. The microbiome in inflammatory bowel disease: current status and the future ahead. Gastroenterology. 2014;146(6):1489–99. doi:10.1053/j.gastro.2014.02.009.CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Eppinga H, Konstantinov SR, Peppelenbosch MP, et al. The microbiome and psoriatic arthritis. Curr Rheumatol Rep. 2014;16(3):407. doi:10.1007/s11926-013-0407-2.CrossRefPubMedGoogle Scholar
  62. 62.
    Mueller S, Saunier K, Hanisch C, et al. Differences in fecal microbiota in different European study populations in relation to age, gender, and country: a cross-sectional study. Appl Environ Microbiol. 2006;72(2):1027–33. doi:10.1128/aem.72.2.1027-1033.2006.CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Markle JG, Frank DN, Adeli K, et al. Microbiome manipulation modifies sex-specific risk for autoimmunity. Gut Microbes. 2014;5(4):485–93. doi:10.4161/gmic.29795.CrossRefPubMedGoogle Scholar
  64. 64.
    David LA, Maurice CF, Carmody RN, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014;505(7484):559–63. doi:10.1038/nature12820.CrossRefPubMedGoogle Scholar
  65. 65.
    Structure, function and diversity of the healthy human microbiome. Nature. 2012;486(7402):207–14. doi:10.1038/nature11234.
  66. 66.
    O’Dell JR, Elliott JR, Mallek JA, et al. Treatment of early seropositive rheumatoid arthritis: doxycycline plus methotrexate versus methotrexate alone. Arthritis Rheum. 2006;54(2):621–7. doi:10.1002/art.21620.CrossRefPubMedGoogle Scholar
  67. 67.
    Tilley BC, Alarcon GS, Heyse SP, et al. Minocycline in rheumatoid arthritis. A 48-week, double-blind, placebo-controlled trial. MIRA Trial Group. Ann Intern Med. 1995;122(2):81–9.CrossRefPubMedGoogle Scholar
  68. 68.
    Lee CH, Steiner T, Petrof EO, et al. Frozen vs fresh fecal microbiota transplantation and clinical resolution of diarrhea in patients with recurrent Clostridium difficile infection: a randomized clinical trial. JAMA. 2016;315(2):142–9. doi:10.1001/jama.2015.18098.CrossRefPubMedGoogle Scholar
  69. 69.
    Estruch R, Ros E, Salas-Salvado J, et al. Primary prevention of cardiovascular disease with a Mediterranean diet. N Engl J Med. 2013;368(14):1279–90. doi:10.1056/NEJMoa1200303.CrossRefPubMedGoogle Scholar
  70. 70.
    Wang X, Thijssen B, Yu H. Target essentiality and centrality characterize drug side effects. PLoS Comput Biol. 2013;9(7):e1003119. doi:10.1371/journal.pcbi.1003119.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  • Di Yan
    • 1
  • Naiem Issa
    • 2
  • Ladan Afifi
    • 1
  • Caleb Jeon
    • 1
  • Hsin-Wen Chang
    • 1
  • Wilson Liao
    • 1
  1. 1.Department of DermatologyUniversity of California-San FranciscoSan FranciscoUSA
  2. 2.School of MedicineGeorgetown UniversityWashingtonUSA

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