Prevalence and odds of Staphylococcus aureus carriage in atopic dermatitis: a systematic review and meta-analysis

British Journal of Dermatology

Volumn 175, Issue 4, 2016, Pages 687-695

  Totte J E E ^a   van der Feltz, W T ^b   Hennekam, M ^a,e   van Belkum, A ^a,c   van Zuuren, E J ^d   Pasmans, S G M A ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

^c BIOMÉRIEUX   (France)

^d LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^e Youth Health Care Rijnmond   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ENTEROTOXIN;

ATOPIC DERMATITIS; BACTERIAL COLONIZATION; BACTERIAL LOAD; BACTERIUM CARRIER; CONTROLLED STUDY; DISEASE SEVERITY; HUMAN; INFLAMMATION; INFORMATION RETRIEVAL; META ANALYSIS; NOSE; OBSERVATIONAL STUDY; OUTCOME ASSESSMENT; PATHOGENESIS; PREVALENCE; PRIORITY JOURNAL; REVIEW; SKIN; STAPHYLOCOCCUS AUREUS; SYSTEMATIC REVIEW;

EID: 84990232820     PISSN: 00070963     EISSN: 13652133     Source Type: Journal    
DOI: 10.1111/bjd.14566     Document Type: Review

References (60)

1. Park HY, Kim CR, Huh IS et al. Staphylococcus aureus colonization in acute and chronic skin lesions of patients with atopic dermatitis. Ann Dermatol 2013; 25:410–16.
2. Matsui K, Nishikawa A, Suto H et al. Comparative study of Staphylococcus aureus isolated from lesional and non-lesional skin of atopic dermatitis patients. Microbiol Immunol 2000; 44:945–7.
3. Leyden JJ, Marples RR, Kligman AM. Staphylococcus aureus in the lesions of atopic dermatitis. Br J Dermatol 1974; 90:525–30.
4. Williams MR, Gallo RL. The role of the skin microbiome in atopic dermatitis. Curr Allergy Asthma Rep 2015; 15:65.
5. Kong HH, Oh J, Deming C et al. Temporal shifts in the skin microbiome associated with disease flares and treatment in children with atopic dermatitis. Genome Res 2012; 22:850–9.
6. Lebon A, Labout JA, Verbrugh HA et al. Role of Staphylococcus aureus nasal colonization in atopic dermatitis in infants: the Generation R Study. Arch Pediatr Adolesc Med 2009; 163:745–9.
7. Bieber T. Atopic dermatitis. Ann Dermatol 2010; 22:125–37.
8. Leung DY, Guttman-Yassky E. Deciphering the complexities of atopic dermatitis: shifting paradigms in treatment approaches. J Allergy Clin Immunol 2014; 134:769–79.
9. Brussow H. Turning the inside out: the microbiology of atopic dermatitis. Environ Microbiol 2015; DOI: 10.1111/1462-2920.13050.
10. Travers JB. Toxic interaction between Th2 cytokines and Staphylococcus aureus in atopic dermatitis. J Invest Dermatol 2014; 134:2069–71.
11. Nakamura Y, Oscherwitz J, Cease KB et al. Staphylococcus δ-toxin induces allergic skin disease by activating mast cells. Nature 2013; 503:397–401.
12. Brauweiler AM, Bin L, Kim BE et al. Filaggrin-dependent secretion of sphingomyelinase protects against staphylococcal α-toxin-induced keratinocyte death. J Allergy Clin Immunol 2013; 131:421–7.e1–2.
13. Kotzin BL, Leung DY, Kappler J, Marrack P. Superantigens and their potential role in human disease. Adv Immunol 1993; 54:99–166.
14. Giai C, Gonzalez C, Ledo C et al. Shedding of tumor necrosis factor receptor 1 induced by protein A decreases tumor necrosis factor alpha availability and inflammation during systemic Staphylococcus aureus infection. Infect Immun 2013; 81:4200–7.
15. Chon SY, Doan HQ, Mays RM et al. Antibiotic overuse and resistance in dermatology. Dermatol Ther 2012; 25:55–69.
16. Chaptini C, Quinn S, Marshman G. Methicillin-resistant Staphylococcus aureus in children with atopic dermatitis from 1999 to 2014: a longitudinal study. Australas J Dermatol 2016; 57:122–7.
17. Antonov NK, Garzon MC, Morel KD et al. High prevalence of mupirocin resistance in Staphylococcus aureus isolates from a pediatric population. Antimicrob Agents Chemother 2015; 59:3350–6.
18. Lapin B, Piorkowski J, Ownby D et al. Relationship between prenatal antibiotic use and asthma in at-risk children. Ann Allergy Asthma Immunol 2015; 114:203–7.
19. Knoll BM, Mylonakis E. Antibacterial bioagents based on principles of bacteriophage biology: an overview. Clin Infect Dis 2014; 58:528–34.
20. ™. Presented at the 24th European Congress of Clinical Microbiology and Infectious Diseases (ECCMID) 2014, Barcelona, Spain, 10–13 May 2014; abstr. R144.
21. Herpers BL, Badoux P, Totté JEE et al. Specific lysis of Staphylococcus aureus by the bacteriophage endolysin Staphefekt SA.100: in vitro studies and human case series. Presented at EuroSciCon: Anibiotic Alternatives for the New Millenium, London, U.K., 5–7 November 2014; 8.
22. Totté JEE, van den Boogaard M, Pardo Cortes LM et al. Staphylococcus aureus specific topical treatment of rosacea and acne with the endolysin Staphefekt SA.100. Presented at the 24th European Academy of Dermatology and Venereology Congress. Copenhagen, Denmark, 7–11 October 2015; abstr. P1212.
23. Williamson P, Kligman AM. A new method for the quantitative investigation of cutaneous bacteria. J Invest Dermatol 1965; 45:498–503.
24. Grice EA, Kong HH, Renaud G et al. A diversity profile of the human skin microbiota. Genome Res 2008; 18:1043–50.
25. Garcia-Garcera M, Garcia-Etxebarria K, Coscolla M, et al. A new method for extracting skin microbes allows metagenomic analysis of whole-deep skin. PLoS ONE 2013; 8:e74914.
26. Wells G, Shea B, O'Connell D et al. The Newcastle–Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. Available at: http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp (last accessed 26 June 2016)
27. Dowlatshahi EA, Wakkee M, Arends LR, Nijsten T. The prevalence and odds of depressive symptoms and clinical depression in psoriasis patients: a systematic review and meta-analysis. J Invest Dermatol 2014; 134:1542–51.
28. McPheeters ML, Kripalani S, Peterson NB et al. Quality improvement interventions to address health disparities. Closing the quality gap: revisiting the state of the science. Available at: https://www.effectivehealthcare.ahrq.gov/ehc/products/386/1242/EvidReport208_CQGHealthDisparities_FinalReport_20120824.pdf. (last accessed 26 June 2016).
29. Leshem YA, Hajar T, Hanifin JM, Simpson EL. What the Eczema Area and Severity Index score tells us about the severity of atopic dermatitis: an interpretability study. Br J Dermatol 2015; 172:1353–7.
30. Oranje AP. Practical issues on interpretation of scoring atopic dermatitis: SCORAD Index, objective SCORAD, patient-oriented SCORAD and Three-Item Severity score. Curr Probl Dermatol 2011; 41:149–55.
31. Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ 1997; 315:629–34.
32. Liberati A, Altman DG, Tetzlaff J 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.
33. Higgins JPT, Green S. Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0. Available at: http://handbook.cochrane.org (last accessed 26 June 2016).
34. Ong PY, Ohtake T, Brandt C et al. Endogenous antimicrobial peptides and skin infections in atopic dermatitis. N Engl J Med 2002; 347:1151–60.
35. Arikawa J, Ishibashi M, Kawashima M et al. Decreased levels of sphingosine, a natural antimicrobial agent, may be associated with vulnerability of the stratum corneum from patients with atopic dermatitis to colonization by Staphylococcus aureus. J Invest Dermatol 2002; 119:433–9.
36. Kobayashi T, Glatz M, Horiuchi K et al. Dysbiosis and Staphyloccus aureus colonization drives inflammation in atopic dermatitis. Immunity 2015; 42:756–66.
37. Bath-Hextall FJ, Birnie AJ, Ravenscroft JC, Williams HC. Interventions to reduce Staphylococcus aureus in the management of atopic eczema: an updated Cochrane review. Br J Dermatol 2011; 164:228.
38. Bath-Hextall FJ, Birnie AJ, Ravenscroft JC, Williams HC. Interventions to reduce Staphylococcus aureus in the management of atopic eczema: an updated Cochrane review. Br J Dermatol 2010; 163:12–26.
39. Wong SM, Ng TG, Baba R. Efficacy and safety of sodium hypochlorite (bleach) baths in patients with moderate to severe atopic dermatitis in Malaysia. J Dermatol 2013; 40:874–80.
40. Lever R, Hadley K, Downey D, Mackie R. Staphylococcal colonization in atopic dermatitis and the effect of topical mupirocin therapy. Br J Dermatol 1988; 119:189–98.
41. Gong JQ, Lin L, Lin T et al. Skin colonization by Staphylococcus aureus in patients with eczema and atopic dermatitis and relevant combined topical therapy: a double-blind multicentre randomized controlled trial. Br J Dermatol 2006; 155:680–7.
42. Stalder JF, Fleury M, Sourisse M et al. Local steroid therapy and bacterial skin flora in atopic dermatitis. Br J Dermatol 1994; 131:536–40.
43. Fahlen A, Engstrand L, Baker BS et al. Comparison of bacterial microbiota in skin biopsies from normal and psoriatic skin. Arch Dermatol Res 2012; 304:15–22.
44. Gao Z, Tseng CH, Strober BE et al. Substantial alterations of the cutaneous bacterial biota in psoriatic lesions. PLoS ONE 2008; 3:e2719.
45. Nakatsuji T, Chiang HI, Jiang SB et al. The microbiome extends to subepidermal compartments of normal skin. Nat Commun 2013; 4:1431.
46. Chehoud C, Rafail S, Tyldsley AS et al. Complement modulates the cutaneous microbiome and inflammatory milieu. Proc Natl Acad Sci USA 2013; 110:15061–6.
47. Grice EA, Segre JA. The skin microbiome. Nat Rev Microbiol 2011; 9:244–53.
48. Lai Y, Cogen AL, Radek KA et al. Activation of TLR2 by a small molecule produced by Staphylococcus epidermidis increases antimicrobial defense against bacterial skin infections. J Invest Dermatol 2010; 130:2211–21.
49. Wanke I, Steffen H, Christ C et al. Skin commensals amplify the innate immune response to pathogens by activation of distinct signaling pathways. J Invest Dermatol 2011; 131:382–90.
50. Krishna S, Miller LS. Host–pathogen interactions between the skin and Staphylococcus aureus. Curr Opin Microbiol 2012; 15:28–35.
51. Kuehnert MJ, Kruszon-Moran D, Hill HA et al. Prevalence of Staphylococcus aureus nasal colonization in the United States, 2001-2002. J Infect Dis 2006; 193:172–9.
52. Sahoo KC, Sahoo S, Marrone G et al. Climatic factors and community – associated methicillin-resistant Staphylococcus aureus skin and soft-tissue infections – a time-series analysis study. Int J Environ Res Public Health 2014; 11:8996–9007.
53. McAleer MA, Irvine AD. The multifunctional role of filaggrin in allergic skin disease. J Allergy Clin Immunol 2013; 131:280–91.
54. Howell MD, Kim BE, Gao P et al. Cytokine modulation of atopic dermatitis filaggrin skin expression. J Allergy Clin Immunol 2009; 124(3 Suppl. 2):R7–12.
55. Khattri S, Shemer A, Rozenblit M et al. Cyclosporine in patients with atopic dermatitis modulates activated inflammatory pathways and reverses epidermal pathology. J Allergy Clin Immunol 2014; 133:1626–34.
56. Ring J, Alomar A, Bieber T et al. Guidelines for treatment of atopic eczema (atopic dermatitis) part I. J Eur Acad Dermatol Venereol 2012; 26:1045–60.
57. Huang JT, Abrams M, Tlougan B et al. Treatment of Staphylococcus aureus colonization in atopic dermatitis decreases disease severity. Pediatrics 2009; 123:e808–14.
58. Breuer K, Haussler S, Kapp A, Werfel T. Staphylococcus aureus: colonizing features and influence of an antibacterial treatment in adults with atopic dermatitis. Br J Dermatol 2002; 147:55–61.
59. Lopes C, Silva D, Delgado L et al. Functional textiles for atopic dermatitis: a systematic review and meta-analysis. Pediatr Allergy Immunol 2013; 24:603–13.
60. Angelova-Fischer I, Neufang G, Jung K et al. A randomized, investigator-blinded efficacy assessment study of stand-alone emollient use in mild to moderately severe atopic dermatitis flares. J Eur Acad Dermatol Venereol 2014; 28:9–15.