The Role of Staphylococcus aureus in Secondary Infections in Patients with Atopic Dermatitis (AD)


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Polish Journal of Microbiology

Polish Society of Microbiologists

Subject: Microbiology


ISSN: 1733-1331
eISSN: 2544-4646





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VOLUME 65 , ISSUE 3 (August 2016) > List of articles

The Role of Staphylococcus aureus in Secondary Infections in Patients with Atopic Dermatitis (AD)

Aneta Buda / Jacek Międzobrodzki *

Keywords : Staphylococcus aureus, atopic dermatitis (AD), opportunistic infections, secondary staphylococcal infections, skin lesions

Citation Information : Polish Journal of Microbiology. Volume 65, Issue 3, Pages 253-259, DOI:

License : (CC BY-NC-ND 4.0)

Received Date : 26-February-2016 / Accepted: 11-April-2016 / Published Online: 26-August-2016



Staphylococcus aureus colonizes the mucous membrane of the nasal vestibule of a significant number of healthy people. These microorgan­isms are opportunistic pathogens, that in favorable conditions, may cause infections of various course, location or manifestation. Second­ary infections emerge in cases when other risk factors contribute to such a change. One of the diseases during which S. aureus changes its saprophytic character to a pathogenic one is atopic dermatitis (AD), an allergic skin condition of a chronic and recurrent nature. Patients with AD are highly predisposed to secondary staphylococcal infections due to active S. aureus colonization of the stratum corneum, dam­age of the skin barrier or a defective immune response. Microorganisms present in skin lesions destroy the tissue by secreting enzymes and toxins, and additionally stimulate secondary allergic reactions. The toxins secreted by strains of S. aureus also act as superantigens and penetrate the skin barrier contributing to a chronic inflammation of the atopic skin lesions. The S. aureus species also releases proinflam­matory proteins, including enzymes that cause tissue damage. When initiating treatment it is particularly important to properly assess that the onset of the secondary bacterial infection is caused by S. aureus and thus justifying the inclusion of antibiotic therapy. Depending on the severity and extent of the staphylococcal infection, topical antibiotics are used, usually mupirocin or fusidic acid, or general antibiotic treatment is introduced. Another therapeutic strategy without antibiotics has given a positive effect in patients.

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Abeck D. and M. Mempel. 1988. Staphylococcus aureus colonization in atopic dermatitis and its therapeutic implications. Br. J. Dermatol. 139 (Suppl 53): 13–16.


Adamek-Guzik T., T.J. Guzik, M. Bzowska, G. Czerniawska-Mysik, D. Szmyd, J. Miedzobrodzki and J. Pryjma. 2001. Selected parameters of the cellular and humoral immunity in atopic dermatitis. Relationship to the severity of the disease (in Polish). Przegl. Lek. 58(12): 1029–1033.


Bogdali M.A., G. Antoszczyk, W. Dyga, A. Obtulowicz, A. Bialecka, A. Kasprowicz, Z. Magnowska and K. Obtulowicz. 2016. Nickel allergy and relationship with Staphylococcus aureus in atopic dermatitis. J. Trace. Elem. Med. Biol. 33: 1–7.


Baran-Raunstrup K., J. Międzobrodzki and T. Ternowitz. 1998. Characteristics of Staphylococcus aureus isolates from atopic dermatitis with reference to proteolytic activity. Acta Microbiol. Pol. 47(2): 167–175.


Boguniewicz M. and D.Y. Leung. 2011. Atopic dermatitis:a disease of altered skin barrier and immune dysregulation. Immunol. Rev. 242(1): 233–246.


Bukowski M., B. Wladyka and G. Dubin. 2010. Exfoliative toxins of Staphylococcus aureus. Toxins (Basel) 2(5): 1148–1165.


Bussmann C., S. Weidinger and N. Novak. 2011. Genetics of atopic dermatitis. J. Dtsch. Dermatol. Ges. 9(9): 670–676.


Cavalcante F.S., E.D. Abad, Y.C. Lyra, S.B. , M. Ribeiro, D.C. Ferreira and K.R. dos Santos. 2015. High prevalence of methicillin resistance and PVL genes among Staphylococcus aureus isolates from the nares and skin lesions of pediatric patients with atopic dermatitis. Braz. J. Med. Biol. Res. 48(7): 588–594.


Cheung G.Y., H.S. Joo, S.S. Chatterjee and M. Otto. 2014. Phenol-soluble modulins-critical determinants of staphylococcal virulence. FEMS Microbiol. Rev. 38(4): 698–719.


Cogen A.L., K. Yamasaki, K.M. Sanchez, R.A. Dorschner, Y. Lai, D.T. MacLeod, J.W. Torpey, M. Otto, V. Nizet, J.E. Kim andR.L. Gallo. 2010. Selective antimicrobial action is provided by phenol-soluble modulins derived from Staphylococcus epidermidis, a normal resident of the skin. J. Invest. Dermatol. 130(1): 192–200.


Cork M.J., S.G. Danby, Y. Vasilopoulos, J. Hadgraft, M.E. Lane,M. Moustafa, R.H. Guy, A.L. Macgowan, R. Tazi-Ahnini andS.J. Ward. 2009. Epidermal barrier dysfunction in atopic dermatitis. J. Invest. Dermatol. 129: 1892–1908.


Foelster Holst R., S. Reitamo, R. Yankova, M. Worm, M. Kadurina, D. Thaci, T. Bieber, N. Tsankov, A. Enk, T. Luger and others. 2010. The novel protease inhibitor SRD441 ointment is not effective in the treatment of adult subjects with atopic dermatitis: results of a randomized, vehicle-controlled study. Allergy 65(12): 1594–1599.


Gelmetti C. 2008. Local antibiotics in dermatology. Derm. Ther. 21: 18.


Gloor M., G. Peters and D. Stoika. 1982. On the resident aerobic bacterial skin flora in unaffected skin of patients with atopic dermatitis and in healthy controls. Dermatologica 164(4): 258–265.


Gong J.Q., L. Lin, T. Lin, F. Hao, F.Q. Zeng, Z.G. Bi, D. Yi andB. Zhao. 2006. 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. 155(4): 680–687.


Gordon R.J. and F.D. Lowy. 2008. Pathogenesis of methicillin-resistant Staphylococcus aureus infection. Clin. Infect. Dis. 46(Suppl 5): S350–359.


Grice E.A. and J.A. Segre. 2011. The skin microbiome. Nat. Rev. Microbiol. 9(4): 244–253. Erratum in: Nat. Rev. Microbiol. 9(8): 626.


Guzik T.J., M. Bzowska, A. Kasprowicz, G. Czerniawska-Mysik, K. Wójcik, D. Szmyd, T. Adamek-Guzik and J. Pryjma. 2005. Persistent skin colonization with Staphylococcus aureus in atopic dermatitis: relationship to clinical and immunological parameters. Clin. Exp. Allergy 35(4): 448–455.


Hanifin J.M. and Rajka G. 1980. Diagnostic features of atopic dermatitis. Acta Derm Venerol. 92: 44.


Hauser C., B. Wuethrich, L. Matter, J.A. Wilhelm, W. Sonnabend and K. Schopfer. 1985. Staphylococcus aureus skin colonization in atopic dermatitis patients. Dermatologica 170: 35–39.


Ide F., T. Matsubara, M. Kaneko, T. Ichiyama, T. Mukouyama and S. Furukawa. 2004. Staphylococcal enterotoxin-specific IgE antibodies in atopic dermatitis. Pediatr. Int. 46(3): 337–341.


Jahreis A., P. Beckheinrich and U.F. Haustein. 2000. Effects of two novel cationic staphylococcal proteins (NP-tase and p70) and enterotoxin B on IgE synthesis and interleukin-4 and interferon-γ production in patients with atopic dermatitis. Br. J. Dermatol.142: 680–687.


Kloos W.E. and Schleifer K.H. 1986. Staphylococcus, pp. 431–434. In: Holt J.G. (ed). Bergey’s manual of systematic bacteriology. Williams & Wilkins, New York, USA.


Kobayashi S.D. and F.R. DeLeo. 2009. An update on community associated MRSA virulence. Curr. Opin. Pharmacol. 9(5): 545–551.


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


Leung D.Y., M. Boguniewicz, M.D. Howell, I. Nomura andQ.A. Hamid. 2004. New insights into atopic dermatitis. J. Clin. Invest. 113(5): 651–657.


Leyden J.J., R.R. Marples and A.M. Kligman. 1974. Staphylococcus aureus in the lesions of atopic dermatitis. Br. J. Dermatol. 90(5): 525–530.


Lis G., E. Cichocka-Jarosz, D. Gazurek, T. Szczerbiński, I. Głodzik,P. Sawiec and B. Białoruska. 2002. Relationships between atopy and bronchial hyper-reactivity in Polish school age children (in Polish). Przegl. Lek. 59(10): 780–784.


Lomholt H., K.E. Andersen and M. Kilian. 2005. Staphylococcus aureus clonal dynamics and virulence factors in children with atopic dermatitis. J. Invest. Dermatol. 125(5): 977–982.


Lübbe J. 2003. Secondary infections in patients with atopic dermatitis. Am. J. Clin. Dermatol. 4( 9): 641–654.


Matsubara M., D. Harada, H. Manabe and K. Hasegawa. 2004. Staphylococcus aureus peptidoglycan stimulates granulocyte macrophage colony-stimulating factor production from human epidermal keratinocytes via mitogen-activated protein kinases. J. Invest. Dermatol. 566(1-3): 195–200.


Międzobrodzki J., A.S. Naidu, J.L. Watts, P. Ciborowski, K. Palmand T. Wadstrom. 1989. Influence of milk on fibronectin and collagen type I binding to Staphylococcus aureus and coagulase-negative staphylococci isolated from Bovine mastitis. J. Clin. Microbiol. 27: 540–544.


Międzobrodzki J. and P. Kaszycki. 2000. Modyfication of ReactiveOxygen intermediates (ROi) production by monocyte/macrophage treated with Staphylococcus aureus serine protease. Acta Microbiol. Pol. 49: 237–242


Międzobrodzki J., P. Kaszycki, A. Białecka and A. Kasprowicz. 2002. Proteolytic activity of Staphylococcus aureus strains isolated from the colonized skin of patients with acute-phase atopic dermatitis. Eur. J. Clin. Microbiol. Infect. Dis. 21: 269–276.


Miedzobrodzki J., T. Panz, P.M. Płonka, K. Zajac, J. Dracz,K. Pytel, Ł. Mateuszuk and S. Chłopicki. 2008. Platelets augment respiratory burst in neutrophils activated by selected species of gram-positive or gram-negative bacteria. Folia Histochem. Cytobiol. 46(3): 383–388.


Na S.Y., J.Y. Roh, J.M. Kim, M.D. Tamang and J.R. Lee. 2012. Analysis of colonization and genotyping of the exotoxins of Staphylococcus aureus in patients with atopic dermatitis. Ann. Dermatol. 24(4): 413–419.


Naidu A.S., J. Miedzobrodzki and A. Forsgren. 1991. Human lactoferrin binding in clinical isolates of Staphylococcus aureus. J. Med. Microbiol. 34: 323–328.


Nakamura Y., J. Oscherwitz, K.B. Cease, S.M. Chan, R. Muñoz-Planillo, M. Hasegawa, A.E. Villaruz, G.Y. Cheung, M.J. McGavin, J.B. Travers and others. 2013. Staphylococcus δ-toxin induces allergic skin disease by activating mast cells. Nature 503(7476): 397–401.


Nutten S. 2015. Atopic dermatitis: global epidemiology and risk factors. Ann. Nutr. Metab. 66(Suppl 1):8–16.


Orfali R.L., M.N. Sato, V.G. Santos, T.O. Titz, C.A. Brito,A.J. Duarte, R. Takaoka and V. Aoki. 2015. Staphylococcal enterotoxin B induces specific IgG4 and IgE antibody serum levels in atopic dermatitis. Int. J. Dermatol. 54(8): 898–904.


Otto M. 2014. Staphylococcus aureus toxins. Curr. Opin. Microbiol. 17: 32–37.


Palmer C.N., A.D. Irvine, A. Terron-Kwiatkowski, Y. Zhao,H. Liao, S.P. Lee, D.R. Goudie, A. Sandilands, L.E. Campbell,F.J. Smith and others. 2006. Common loss-of-function variants of the epidermal barrier protein filaggrin are a major predisposing factor for atopic dermatitis. Nat. Genet. 38: 441–446.


Petry V., G.R. Bessa, C.S. Poziomczyck, C.F. Oliveira, M.B. Weber,R.R. Bonamigo and P.A. d’Azevedo. 2012. Bacterial skin colonization and infections in patients with atopic dermatitis. An. Bras. Dermatol. 87(5): 729–734.


Reginald K., K. Westritschnig, T. Werfel, A. Heratizadeh, N. Novak, M. Focke-Tejkl, A.M. Hirschl, D.Y. Leung, O. Elisyutina, E. Fedenko and others. 2011. Immunoglobulin E antibody reactivity to bacterial antigens in atopic dermatitis patients. Clin. Exp. Allergy 41(3): 357–369.


Ring J., A. Alomar, T. Bieber, M. Deleuran, A. Fink-Wagner,C. Gelmetti, U. Gieler, J. Lipozencic, T. Luger, A.P. Oranje and others. 2012. Guidelines for treatment of atopic eczema (atopic dermatitis). Part I. J. Eur. Acad. Dermatol. Venereol. 26(8): 1045–1060.


Ring J., D. Abeck and K. Neuber. 1992. Atopic eczema: role of microorganisms on the skin surface. Allergy 47(4 Pt 1): 265–269.


Rojo A., A. Aguinaga, S. Monecke, J.R. Yuste, G. Gastaminza and A. España. 2014. Staphylococcus aureus genomic pattern and atopic dermatitis: may factors other than superantigens be involved? Eur. J. Clin. Microbiol. Infect. Dis. 33(4): 651–658.


Roll A., A. Cozzio, B. Fischer and P. Schmid-Grendelmeier. 2004. Microbial colonization and atopic dermatitis. Curr. Opin. Allergy Clin. Immunol. 4: 373–378.


Sabat A.J., B. Wladyka., K. Kosowska-Shick, H. Grundmann,J.M. van Dijl, J. Kowal, P.C. Appelbaum, A. Dubin and W. Hryniewicz. 2008. Polymorphism, genetic exchange and intragenic recombination of the aureolysin gene among Staphylococcus aureus strains. BMC Microbiol. 29(8): 129.


Schlievert P.M., L.C. Case, K.L. Strandberg, B.B. Abrams andD.Y. Leung. 2008. Superantigen profile of Staphylococcus aureus isolates from patients with steroid-resistant atopic dermatitis. Clin. Infect. Dis. 46(10): 1562–1567.


Schlievert P.M., K.L. Strandberg, Y.C. Lin, M.L. Peterson andD.Y. Leung. 2010. Secreted virulence factor comparison between methicillin-resistant and methicillin-sensitive Staphylococcus aureus, and its relevance to atopic dermatitis. J. Allergy Clin. Immunol. 125(1): 39–49.


Soares J., C. Lopes, F. Tavaria, L. Delgado and M. Pintado. 2013. A diversity profile from the staphylococcal community on atopic der-matitis skin: a molecular approach. J. Appl. Microbiol. 115(6): 1411–1419.


Sonesson A., J. Bartosik, J. Christiansen, I. Roscher, F. Nilsson,A. Schmidtchen and O. Bäck. 2013. Sensitization to skin-associated microorganisms in adult patients with atopic dermatitis is of impor-tance for disease severity. Acta Derm. Venereol. 93(3): 340–345.


Sybilski A.J., F. Raciborski, A. Lipiec, A. Tomaszewska, A. Lusawa, P. Samel-Kowalik, A. Walkiewicz, E. Krzych, J. Komorowski and B. Samoliński. 2015. Atopic dermatitis is a serious health problem in Poland. Epidemiology studies based on the ECAP study (inPolish). Postepy Dermatol. Alergol. 32(1): 1–10.


Ternowitz T. and T. Herlin. 1986. Defective monocyte and polymorphonuclear leukocyte chemotaxis and clinical characteristics in atopic dermatitis. Arch. Dermatol. Res. 278(6): 454–459.


Werfel T. 2009. The role of leukocytes, keratinocytes, and allergen-specific IgE in the development of atopic dermatitis. J. Invest. Dermatol. 129: 1878–1891.


Wilburg J., A. Kasprowicz and P.B. Heczko. 1984. Composition of normal bacterial flora of human skin in relation to the age and sex of examined persons (in Polish). Przegl. Dermatol. 71(6): 551–557.