Top

European Journal of Clinical Microbiology & Infectious Diseases

Published in:

Open Access 01-07-2016 | Review

A systematic review and meta-analysis on Staphylococcus aureus carriage in psoriasis, acne and rosacea

Authors: J. E. E. Totté, W. T. van der Feltz, L. G. M. Bode, A. van Belkum, E. J. van Zuuren, S. G. M. A. Pasmans

Published in: European Journal of Clinical Microbiology & Infectious Diseases | Issue 7/2016

Abstract

Staphylococcus aureus might amplify symptoms in chronic inflammatory skin diseases. This study evaluates skin and mucosal colonization with S. aureus in patients with psoriasis, acne and rosacea. A systematic literature search was conducted. Both odds ratios (OR) for colonization in patients versus controls and the prevalence of colonization in patients are reported. Fifteen articles about psoriasis and 13 about acne (12 having a control group) were included. No study in rosacea met our inclusion criteria. For psoriasis, one study out of three controlled studies showed increased skin colonization (OR 18.86; 95 % confidence interval [CI] 2.20–161.99). Three out of the five studies that reported on nasal colonization showed significant ORs varying from 1.73 (95 % CI 1.16–2.58) to 14.64 (95 % CI 2.82–75.95). For acne one of the three studies that evaluated skin colonization reported a significant OR of 4.16 (95 % CI 1.74–9.94). A relation between nasal colonization and acne was not found. Limitations in study design and low sample sizes should be taken into consideration when interpreting the results. Colonisation with S. aureus seems to be increased in patients with psoriasis. This bacterial species, known for its potential to induce long-lasting inflammation, might be involved in psoriasis pathogenesis. Information on acne is limited. Prospective controlled studies should further investigate the role of S. aureus in chronic inflammatory skin diseases.

Available only for authorised users

Belkaid Y, Segre JA (2014) Dialogue between skin microbiota and immunity. Science 346(6212):954–959CrossRefPubMed

Chen YE, Tsao H (2013) The skin microbiome: Current perspectives and future challenges. J Am Acad Dermatol 69(1):143–155CrossRefPubMedPubMedCentral

Sanford JA, Gallo RL (2013) Functions of the skin microbiota in health and disease. Semin Immunol 25(5):370–377CrossRefPubMedPubMedCentral

Kong HH, Segre JA (2012) Skin microbiome: looking back to move forward. J Invest Dermatol 132(3 Pt 2):933–939CrossRefPubMed

Totte JE, van der Feltz WT, Hennekam M, van Belkum A, van Zuuren EJ, Pasmans SG (2016) Prevalence and odds of Staphylococcus aureus carriage in atopic dermatitis: a systematic review and meta-analysis. Br J Dermatol

Biedermann T, Skabytska Y, Kaesler S, Volz T (2015) Regulation of T Cell Immunity in Atopic Dermatitis by Microbes: The Yin and Yang of Cutaneous Inflammation. Front Immunol 6:353CrossRefPubMedPubMedCentral

Fry L, Baker BS (2007) Triggering psoriasis: the role of infections and medications. Clin Dermatol 25(6):606–615CrossRefPubMed

Holmes AD (2013) Potential role of microorganisms in the pathogenesis of rosacea. J Am Acad Dermatol 69(6):1025–1032CrossRefPubMed

Steinhoff M, Schauber J, Leyden JJ (2013) New insights into rosacea pathophysiology: a review of recent findings. J Am Acad Dermatol 69(6 Suppl 1):S15–26CrossRefPubMed

10.

Gollnick HPM (2015) From new findings in acne pathogenesis to new approaches in treatment. J Eur Acad Dermatol Venereol 29:1–7

11.

Gao Z, Tseng CH, Strober BE, Pei Z, Blaser MJ (2008) Substantial alterations of the cutaneous bacterial biota in psoriatic lesions. PLoS One 3(7):e2719CrossRefPubMedPubMedCentral

12.

Owen CM, Chalmers RJ, O’Sullivan T, Griffiths CE (2001) A systematic review of antistreptococcal interventions for guttate and chronic plaque psoriasis. Br J Dermatol 145(6):886–890CrossRefPubMed

13.

Balci DD, Duran N, Ozer B, Gunesacar R, Onlen Y, Yenin JZ (2009) High prevalence of Staphylococcus aureus cultivation and superantigen production in patients with psoriasis. Eur J Dermatol 19(3):238–242PubMed

14.

Chong HT, Kopecki Z, Cowin AJ (2013) Lifting the silver flakes: the pathogenesis and management of chronic plaque psoriasis. Biomed Res Int 2013:168321PubMedPubMedCentral

15.

Johannessen M, Sollid JE, Hanssen AM (2012) Host- and microbe determinants that may influence the success of S. aureus colonization. Front Cell Infect Microbiol 2:56CrossRefPubMedPubMedCentral

16.

Lynde CW, Poulin Y, Vender R, Bourcier M, Khalil S (2014) Interleukin 17A: toward a new understanding of psoriasis pathogenesis. J Am Acad Dermatol 71(1):141–150CrossRefPubMed

17.

Mahajan R, Handa S (2013) Pathophysiology of psoriasis. Indian J Dermatol Venereol Leprol 79(Suppl 7):S1–9PubMed

18.

van den Berg WB, McInnes IB (2013) Th17 cells and IL-17 a--focus on immunopathogenesis and immunotherapeutics. Semin Arthritis Rheum 43(2):158–170CrossRefPubMed

19.

Atefi N, Tabaie M, Noorbakhsh S, Tabatabaie A, Rezaee M, Rohaninasab M (2012) The role of staphylococcus superantigens in chronic plaque type psoriasis. Iran J Dermatol 15(59):1–3

20.

Leung DY, Walsh P, Giorno R, Norris DA (1993) A potential role for superantigens in the pathogenesis of psoriasis. J Invest Dermatol 100(3):225–228CrossRefPubMed

21.

Yamamoto T, Katayama I, Nishioka K (1998) Clinical analysis of staphylococcal superantigen hyper-reactive patients with psoriasis vulgaris. Eur J Dermatol 8(5):325–329PubMed

22.

Vazquez-Sanchez EA, Rodriguez-Romero M, Sanchez-Torres LE, Rodriguez-Martinez S, Cancino-Diaz JC, Rodriguez-Cortes O, Garcia-Lopez ES, Cancino-Diaz ME (2014) Peptidoglycan from Staphylococcus aureus has an anti-apoptotic effect in HaCaT keratinocytes mediated by the production of the cellular inhibitor of apoptosis protein-2. Microbiol Immunol 58(2):87–95CrossRefPubMed

23.

Bakry OA, Samaka RM, Sebika H, Seleit I (2014) Toll-like receptor 2 and P. acnes: do they trigger initial acne vulgaris lesions? Anal Quant Cytopathol Histpathol 36(2):100–110PubMed

24.

Beylot C, Auffret N, Poli F, Claudel JP, Leccia MT, Del Giudice P, Dreno B (2014) Propionibacterium acnes: An update on its role in the pathogenesis of acne. J Eur Acad Dermatol Venereol 28(3):271–278CrossRefPubMed

25.

Jugeau S, Tenaud I, Knol AC, Jarrousse V, Quereux G, Khammari A, Dreno B (2005) Induction of toll-like receptors by Propionibacterium acnes. Br J Dermatol 153(6):1105–1113CrossRefPubMed

26.

Kim J, Ochoa MT, Krutzik SR, Takeuchi O, Uematsu S, Legaspi AJ, Brightbill HD, Holland D, Cunliffe WJ, Akira S, Sieling PA, Godowski PJ, Modlin RL (2002) Activation of toll-like receptor 2 in acne triggers inflammatory cytokine responses. J Immunol 169(3):1535–1541CrossRefPubMedPubMedCentral

27.

Fitz-Gibbon S, Tomida S, Chiu BH, Nguyen L, Du C, Liu M, Elashoff D, Erfe MC, Loncaric A, Kim J, Modlin RL, Miller JF, Sodergren E, Craft N, Weinstock GM, Li H (2013) Propionibacterium acnes strain populations in the human skin microbiome associated with acne. J Invest Dermatol 133(9):2152–2160CrossRefPubMedPubMedCentral

28.

Tomida S, Nguyen L, Chiu BH, Liu J, Sodergren E, Weinstock GM, Li H (2013) Pan-genome and comparative genome analyses of propionibacterium acnes reveal its genomic diversity in the healthy and diseased human skin microbiome. MBio 4(3):e00003–00013CrossRefPubMedPubMedCentral

29.

Jahns AC, Eilers H, Ganceviciene R, Alexeyev OA (2015) Propionibacterium species and follicular keratinocyte activation in acneic and normal skin. Brit J Dermatol 172(4):981–987CrossRef

30.

Jarmuda S, O’Reilly N, Zaba R, Jakubowicz O, Szkaradkiewicz A, Kavanagh K (2012) Potential role of Demodex mites and bacteria in the induction of rosacea. J Med Microbiol 61(Pt 11):1504–1510CrossRefPubMed

31.

Koller B, Muller-Wiefel AS, Rupec R, Korting HC, Ruzicka T (2011) Chitin modulates innate immune responses of keratinocytes. PLoS One 6(2):e16594CrossRefPubMedPubMedCentral

32.

Allen HB, Vaze ND, Choi C, Hailu T, Tulbert BH, Cusack CA, Joshi SG (2014) The presence and impact of biofilm-producing staphylococci in atopic dermatitis. JAMA Dermatol 150(3):260–265CrossRefPubMed

33.

Fournier B (2012) The function of TLR2 during staphylococcal diseases. Front Cell Infect Microbiol 2:167PubMed

34.

Niebuhr M, Schorling K, Heratizadeh A, Werfel T (2015) Staphylococcal alpha-toxin induces a functional upregulation of TLR-2 on human peripheral blood monocytes. Exp Dermatol 24(5):381–383CrossRefPubMed

35.

Al Mishari MA (1987) Acne vulgaris: Treatment with tetracycline and its effect on bacterial flora. Curr Ther Res Clin Exp 41(3):351–355

36.

Jakobsson HE, Jernberg C, Andersson AF, Sjolund-Karlsson M, Jansson JK, Engstrand L (2010) Short-term antibiotic treatment has differing long-term impacts on the human throat and gut microbiome. PLoS One 5(3):e9836CrossRefPubMedPubMedCentral

37.

Relman DA (2012) The human microbiome: ecosystem resilience and health. Nutr Rev 70(Suppl 1):S2–9CrossRefPubMedPubMedCentral

38.

Leccia MT, Auffret N, Poli F, Claudel JP, Corvec S, Dreno B (2015) Topical acne treatments in Europe and the issue of antimicrobial resistance. J Eur Acad Dermatol Venereol 29:1485–92CrossRefPubMed

39.

Chon SY, Doan HQ, Mays RM, Singh SM, Gordon RA, Tyring SK (2012) Antibiotic overuse and resistance in dermatology. Dermatol Ther 25(1):55–69CrossRefPubMed

40.

World Health Organization (2001) Global Strategy for Containment of Antimicrobial Resistance. World Health Organization (WHO), Geneva

41.

World Health Organization (2014) Antimicrobial resistance. Global report on surveillance: World Health Organization (WHO)

42.

Knoll BM, Mylonakis E (2014) Antibacterial Bioagents Based on Principles of Bacteriophage Biology: An Overview. Clin Infect Dis 58(4):528–534CrossRefPubMed

43.

Wells G, Shea B, O’Connell D, Peterson J, Welch V, Losos M, Tugwell P (2012) The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses, http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp

44.

Dowlatshahi EA, Wakkee M, Arends LR, Nijsten T (2014) The prevalence and odds of depressive symptoms and clinical depression in psoriasis patients: a systematic review and meta-analysis. J Invest Dermatol 134(6):1542–1551CrossRefPubMed

45.

McPheeters ML, Kripalani S, Peterson NB, Idowu RT, Jerome RN, Potter SA, Andrews JC (2012) Quality improvement interventions to address health disparities. Closing the quality gap: revisiting the state of the science. Evidence Report No 208 (Prepared by the Vanderbilt University Evidence-based Practice Center under Contract No 290-2007-10065). Rockville, MD: Agency for healthcare research and quality

46.

Egger M, Davey Smith G, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315(7109):629–634CrossRefPubMedPubMedCentral

47.

Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gotzsche PC, Ioannidis JP, Clarke M, Devereaux PJ, Kleijnen J, Moher D (2009) The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: explanation and elaboration. BMJ 339:b2700CrossRefPubMedPubMedCentral

48.

Tabatabaei A, Atefi N, Noorbakhsh S (2011) Staphylococcal superantigens in skin biopsy of psoriatic patients: A case control study. Allergy Eur J Allergy Clin Immunol 66:306CrossRef

49.

Tomi NS, Kranke B, Aberer E (2005) Staphylococcal toxins in patients with psoriasis, atopic dermatitis, and erythroderma, and in healthy control subjects. J Am Acad Dermatol 53(1):67–72CrossRefPubMed

50.

Ryu JH, Lee J, Son SJ, Won YH, Oh JS (2003) Study of Bacterial Distribution on the Skin of Psoriasis by Tape Method. Korean J Dermatol 41(8):997–1003

51.

Brook I, Frazier EH, Yeager JK (1999) Microbiology of infected pustular psoriasis lesions. Int J Dermatol 38(8):579–581CrossRefPubMed

52.

Sayama K, Midorikawa K, Hanakawa Y, Sugai M, Hashimoto K (1998) Superantigen production by Staphylococcus aureus in psoriasis. Dermatology 196(2):194–198CrossRefPubMed

53.

Noah PW (1990) The role of microorganisms in psoriasis. Semin Dermatol 9(4):269–276PubMed

54.

Weissmann A, Noble WC (1980) Photochemotherapy of psoriasis: Effects on bacteria and surface lipids in uninvolved skin. Br J Dermatol 102(2):185–193CrossRefPubMed

55.

Aly R, Maibach HI, Mandel A (1976) Bacterial flora in psoriasis. Br J Dermatol 95(6):603–606CrossRefPubMed

56.

Andersen PS, Larsen LA, Fowler VG Jr, Stegger M, Skov RL, Christensen K (2013) Risk factors for Staphylococcus aureus nasal colonization in Danish middle-aged and elderly twins. Eur J Clin Microbiol Infect Dis 32(10):1321–1326CrossRefPubMedPubMedCentral

57.

Klein PA, Greene WH, Fuhrer J, Clark RA (1997) Prevalence of methicillin-resistant Staphylococcus aureus in outpatients with psoriasis, atopic dermatitis, or HIV infection. Arch Dermatol 133(11):1463–1465CrossRefPubMed

58.

Singh G, Rao DJ (1978) Bacteriology of psoriatic plaques. Dermatologica 157(1):21–27CrossRefPubMed

59.

Ajib R, Janbazian L, Rahal E, Matar GM, Zaynoun S, Kibbi AG, Abdelnoor AM (2005) HLA allele associations and V-beta T-lymphocyte expansions in patients with psoriasis, harboring toxin-producing Staphylococcus aureus. J Biomed Biotechnol 2005(4):310–315CrossRefPubMedPubMedCentral

60.

Numata S, Akamatsu H, Akaza N, Yagami A, Nakata S, Matsunaga K (2014) Analysis of facial skin-resident microbiota in Japanese acne patients. Dermatology 228(1):86–92CrossRefPubMed

61.

Moon SH, Roh HS, Kim YH, Kim JE, Ko JY, Ro YS (2012) Antibiotic resistance of microbial strains isolated from Korean acne patients. J Dermatol 39(10):833–837CrossRefPubMed

62.

Hassanzadeh P, Bahmani M, Mehrabani D (2008) Bacterial resistance to antibiotics in acne vulgaris: An in vitro study. Indian J Dermatol 53(3):122–124CrossRefPubMedPubMedCentral

63.

Williams RE, Doherty VR, Perkins W, Aitchison TC, Mackie RM (1992) Staphylococcus aureus and intra-nasal mupirocin in patients receiving isotretinoin for acne. Br J Dermatol 126(4):362–366CrossRefPubMed

64.

Leyden JJ, McGinley KJ, Foglia AN (1986) Qualitative and quantitative changes in cutaneous bacteria associated with systemic isotretinoin therapy for acne conglobata. J Invest Dermatol 86(4):390–393CrossRefPubMed

65.

Batova D, Hadam I (1971) Demonstration of skin microflora in patients with acne vulgaris. Cesk Dermatol 46(5):196–199PubMed

66.

Ozuguz P, Callioglu EE, Tulaci KG, Kacar SD, Balta I, Asik G, Karatas S, Karaca S (2014) Evaluation of nasal and oropharyngeal flora in patients with acne vulgaris according to treatment options. Int J Dermatol 53(11):1404–1408CrossRefPubMed

67.

Basak PY, Cetin ES, Gurses I, Ozseven AG (2013) The effects of systemic isotretinoin and antibiotic therapy on the microbial floras in patients with acne vulgaris. J Eur Acad Dermatol Venereol 27(3):332–336CrossRefPubMed

68.

Toyne H, Webber C, Collignon P, Dwan K, Kljakovic M (2012) Propionibacterium acnes (P. acnes) resistance and antibiotic use in patients attending Australian general practice. Australas J Dermatol 53(2):106–111CrossRefPubMed

69.

Khorvash F, Abdi F, Kashani HH, Naeini FF, Narimani T (2012) Staphylococcus aureus in Acne Pathogenesis: A Case–control Study. N Am J Med Sci 4(11):573–576CrossRefPubMedPubMedCentral

70.

Fanelli M, Kupperman E, Lautenbach E, Edelstein PH, Margolis DJ (2011) Antibiotics, acne, and Staphylococcus aureus colonization. Arch Dermatol 147(8):917–921CrossRefPubMedPubMedCentral

71.

Levy RM, Huang EY, Roling D, Leyden JJ, Margolis DJ (2003) Effect of antibiotics on the oropharyngeal flora in patients with acne. Arch Dermatol 139(4):467–471CrossRefPubMed

72.

Wertheim HF, Melles DC, Vos MC, van Leeuwen W, van Belkum A, Verbrugh HA, Nouwen JL (2005) The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect Dis 5(12):751–762CrossRefPubMed

73.

Chehoud C, Rafail S, Tyldsley AS, Seykora JT, Lambris JD, Grice EA (2013) Complement modulates the cutaneous microbiome and inflammatory milieu. Proc Natl Acad Sci U S A 110(37):15061–15066CrossRefPubMedPubMedCentral

74.

Grice EA, Segre JA (2011) The skin microbiome. Nat Rev Microbiol 9(4):244–253CrossRefPubMedPubMedCentral

75.

Krishna S, Miller LS (2012) Host-pathogen interactions between the skin and Staphylococcus aureus. Curr Opin Microbiol 15(1):28–35CrossRefPubMed

76.

Nakatsuji T, Chiang HI, Jiang SB, Nagarajan H, Zengler K, Gallo RL (2013) The microbiome extends to subepidermal compartments of normal skin. Nat Commun 4:1431CrossRefPubMedPubMedCentral

Title: A systematic review and meta-analysis on Staphylococcus aureus carriage in psoriasis, acne and rosacea
Authors: J. E. E. Totté
W. T. van der Feltz
L. G. M. Bode
A. van Belkum
E. J. van Zuuren
S. G. M. A. Pasmans
Publication date: 01-07-2016
Publisher: Springer Berlin Heidelberg
Published in: European Journal of Clinical Microbiology & Infectious Diseases / Issue 7/2016
Print ISSN: 0934-9723
Electronic ISSN: 1435-4373
DOI: https://doi.org/10.1007/s10096-016-2647-3

ACC 2024 Congress Coverage

Heart Failure Video

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

A systematic review and meta-analysis on Staphylococcus aureus carriage in psoriasis, acne and rosacea

Abstract

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 7/2016

A study to evaluate the first dose of gentamicin needed to achieve a peak plasma concentration of 30 mg/l in patients hospitalized for severe sepsis

Streptococcus salivarius by nasal spray for recurrent otitis: how good is the evidence?

Impact of microbiology cascade reporting on antibiotic de-escalation in cefazolin-susceptible Gram-negative bacteremia

Is Toxoplasma gondii type related to clinical outcome in human congenital infection? Systematic and critical review

Clinical and socioeconomic impact of moderate-to-severe versus mild influenza in children

The role of Clostridium difficile in the paediatric and neonatal gut — a narrative review

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page