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Published in: Clinical Reviews in Allergy & Immunology 3/2016

01-12-2016

Bacterial and Viral Infections in Atopic Dermatitis: a Comprehensive Review

Authors: Peck Y. Ong, Donald Y. M. Leung

Published in: Clinical Reviews in Allergy & Immunology | Issue 3/2016

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Abstract

Atopic dermatitis (AD) is the most common allergic skin disease in the general population. It is a chronic inflammatory skin disease complicated by recurrent bacterial and viral infections that, when left untreated, can lead to significant complications. The current article will review immunologic and molecular mechanisms underlying the propensity of AD patients to microbial infections. These infections include Staphylococcus aureus (S. aureus) skin infections, eczema herpeticum, eczema vaccinatum, and eczema coxsackium. Previous studies have shown that skin barrier defects, a decrease in antimicrobial peptides, increased skin pH, or Th2 cytokines such as IL-4 and IL-13 are potential contributing factors for the increased risk of skin infections in AD. In addition, bacterial virulence such as methicillin-resistant S. aureus (MRSA) produces significantly higher number of superantigens that increase their potential in causing infection and more severe cutaneous inflammation in AD patients. More recent studies suggest that skin microbiome including Staphylococcus epidermidis or other coagulase-negative staphylococci may play an important role in controlling S. aureus skin infections in AD. Other studies also suggest that genetic variants in the innate immune response may predispose AD patients to increased risk of viral skin infections. These genetic variants include thymic stromal lymphopoietin (TSLP), type I interferon (α, ß, ω), type II interferon (γ), and molecular pathways that lead to the production of interferons (interferon regulatory factor 2). A common staphylococcal toxin, α-toxin, may also play a role in enhancing herpes simplex virus skin infections in AD. Further understanding of these disease processes may have important clinical implications for the prevention and treatment of skin infections in this common skin disease.
Literature
1.
go back to reference Leung DYM, Guttman-Yassky E (2014) Deciphering the complexities of atopic dermatitis: shifting paradigms in treatment approaches. J Allergy Clin Immunol 134:769–779CrossRefPubMedPubMedCentral Leung DYM, Guttman-Yassky E (2014) Deciphering the complexities of atopic dermatitis: shifting paradigms in treatment approaches. J Allergy Clin Immunol 134:769–779CrossRefPubMedPubMedCentral
2.
go back to reference Grice K, Sattar H, Baker H, Sharratt M (1975) The relationship of transepidermal water loss to skin temperature in psoriasis and eczema. J Invest Dermatol 64(5):313–315CrossRefPubMed Grice K, Sattar H, Baker H, Sharratt M (1975) The relationship of transepidermal water loss to skin temperature in psoriasis and eczema. J Invest Dermatol 64(5):313–315CrossRefPubMed
3.
go back to reference Irvine AD, McLean WH, Leung DY (2011) Filaggrin mutations associated with skin and allergic diseases. N Engl J Med 365:1315–1327CrossRefPubMed Irvine AD, McLean WH, Leung DY (2011) Filaggrin mutations associated with skin and allergic diseases. N Engl J Med 365:1315–1327CrossRefPubMed
4.
go back to reference De Benedetto A, Rafaels NM, McGirt LY, Ivanov AI, Georas SN, Cheadle C, Berger A, Zhang K, Vidyasagar S, Yoshida T, Boguniewicz M, Hata T, Schneider LC, Hanifin JM, Gallo RL, Novak N, Weidinger S, Beaty TH, Leung DY, Barnes KC, Beck LA (2011) Tight junction defects in patients with atopic dermatitis. J Allergy Clin Immunol 127:773–786, e1-7 CrossRefPubMed De Benedetto A, Rafaels NM, McGirt LY, Ivanov AI, Georas SN, Cheadle C, Berger A, Zhang K, Vidyasagar S, Yoshida T, Boguniewicz M, Hata T, Schneider LC, Hanifin JM, Gallo RL, Novak N, Weidinger S, Beaty TH, Leung DY, Barnes KC, Beck LA (2011) Tight junction defects in patients with atopic dermatitis. J Allergy Clin Immunol 127:773–786, e1-7 CrossRefPubMed
5.
go back to reference Omori-Miyake M, Yamashita M, Tsunemi Y, Kawashima M, Yagi J (2014) In vitro assessment of IL-4- or IL-13-mediated changes in the structural components of keratinocytes in mice and humans. J Invest Dermatol 134:1342–1350CrossRefPubMed Omori-Miyake M, Yamashita M, Tsunemi Y, Kawashima M, Yagi J (2014) In vitro assessment of IL-4- or IL-13-mediated changes in the structural components of keratinocytes in mice and humans. J Invest Dermatol 134:1342–1350CrossRefPubMed
6.
go back to reference Gutowska-Owsiak D, Schaupp AL, Salimi M, Taylor S, Ogg GS (2011) Interleukin-22 downregulates filaggrin expression and affects expression of profilaggrin processing enzymes. Br J Dermatol 165:492–498CrossRefPubMed Gutowska-Owsiak D, Schaupp AL, Salimi M, Taylor S, Ogg GS (2011) Interleukin-22 downregulates filaggrin expression and affects expression of profilaggrin processing enzymes. Br J Dermatol 165:492–498CrossRefPubMed
7.
go back to reference Cai SC, Chen H, Koh WP, Common JE, van Bever HP, McLean WH, Lane EB, Giam YC, Tang MB (2012) Filaggrin mutations are associated with recurrent skin infection in Singaporean Chinese patients with atopic dermatitis. Br J Dermatol 166:200–203CrossRefPubMed Cai SC, Chen H, Koh WP, Common JE, van Bever HP, McLean WH, Lane EB, Giam YC, Tang MB (2012) Filaggrin mutations are associated with recurrent skin infection in Singaporean Chinese patients with atopic dermatitis. Br J Dermatol 166:200–203CrossRefPubMed
8.
go back to reference Miajlovic H, Fallon PG, Irvine AD, Foster TJ (2010) Effect of filaggrin breakdown products on growth of and protein expression by Staphylococcus aureus. J Allergy Clin Immunol 126:1184–1190CrossRefPubMedPubMedCentral Miajlovic H, Fallon PG, Irvine AD, Foster TJ (2010) Effect of filaggrin breakdown products on growth of and protein expression by Staphylococcus aureus. J Allergy Clin Immunol 126:1184–1190CrossRefPubMedPubMedCentral
9.
10.
go back to reference Fallon PG, Sasaki T, Sandilands A, Campbell LE, Saunders SP, Mangan NE, Callanan JJ, Kawasaki H, Shiohama A, Kubo A, Sundberg JP, Presland RB, Fleckman P, Shimizu N, Kudoh J, Irvine AD, Amagai M, McLean WH (2009) A homozygous frameshift mutation in the mouse Flg gene facilitates enhanced percutaneous allergen priming. Nat Genet 41:602–608CrossRefPubMedPubMedCentral Fallon PG, Sasaki T, Sandilands A, Campbell LE, Saunders SP, Mangan NE, Callanan JJ, Kawasaki H, Shiohama A, Kubo A, Sundberg JP, Presland RB, Fleckman P, Shimizu N, Kudoh J, Irvine AD, Amagai M, McLean WH (2009) A homozygous frameshift mutation in the mouse Flg gene facilitates enhanced percutaneous allergen priming. Nat Genet 41:602–608CrossRefPubMedPubMedCentral
11.
go back to reference Sasaki T, Shiohama A, Kubo A, Kawasaki H, Ishida-Yamamoto A, Yamada T, Hachiya T, Shimizu A, Okano H, Kudoh J, Amagai M (2013) A homozygous nonsense mutation in the gene for Tmem79, a component for the lamellar granule secretory system, produces spontaneous eczema in an experimental model of atopic dermatitis. J Allergy Clin Immunol 132:1111–1120CrossRefPubMed Sasaki T, Shiohama A, Kubo A, Kawasaki H, Ishida-Yamamoto A, Yamada T, Hachiya T, Shimizu A, Okano H, Kudoh J, Amagai M (2013) A homozygous nonsense mutation in the gene for Tmem79, a component for the lamellar granule secretory system, produces spontaneous eczema in an experimental model of atopic dermatitis. J Allergy Clin Immunol 132:1111–1120CrossRefPubMed
12.
go back to reference Saunders SP, Goh CS, Brown SJ, Palmer CN, Porter RM, Cole C, Campbell LE, Gierlinski M, Barton GJ, Schneider G, Balmain A, Prescott AR, Weidinger S, Baurecht H, Kabesch M, Gieger C, Lee YA, Tavendale R, Mukhopadhyay S, Turner SW, Madhok VB, Sullivan FM, Relton C, Burn J, Meggitt S, Smith CH, Allen MA, Barker JN, Reynolds NJ, Cordell HJ, Irvine AD, McLean WH, Sandilands A, Fallon PG (2013) Tmem79/Matt is the matted mouse gene and is a predisposing gene for atopic dermatitis in human subjects. J Allergy Clin Immunol 132:1121–1129CrossRefPubMedPubMedCentral Saunders SP, Goh CS, Brown SJ, Palmer CN, Porter RM, Cole C, Campbell LE, Gierlinski M, Barton GJ, Schneider G, Balmain A, Prescott AR, Weidinger S, Baurecht H, Kabesch M, Gieger C, Lee YA, Tavendale R, Mukhopadhyay S, Turner SW, Madhok VB, Sullivan FM, Relton C, Burn J, Meggitt S, Smith CH, Allen MA, Barker JN, Reynolds NJ, Cordell HJ, Irvine AD, McLean WH, Sandilands A, Fallon PG (2013) Tmem79/Matt is the matted mouse gene and is a predisposing gene for atopic dermatitis in human subjects. J Allergy Clin Immunol 132:1121–1129CrossRefPubMedPubMedCentral
13.
go back to reference Elias PM, Wakefield JS (2014) Mechanisms of abnormal lamellar body secretion and the dysfunctional skin barrier in patients with atopic dermatitis. J Allergy Clin Immunol 134:781–791CrossRefPubMedPubMedCentral Elias PM, Wakefield JS (2014) Mechanisms of abnormal lamellar body secretion and the dysfunctional skin barrier in patients with atopic dermatitis. J Allergy Clin Immunol 134:781–791CrossRefPubMedPubMedCentral
15.
go back to reference Mathias RA, Chavan S, Iyer K, Rafaels N, Boorgula M, Potee J, Hanifin JM, Paller A, and others. (2015) Identifying genetic determinants of atopic dermatitis and bacterial colonization using whole genome sequencing. J Allergy Clin Immunol 135(2):AB391 (abstract) Mathias RA, Chavan S, Iyer K, Rafaels N, Boorgula M, Potee J, Hanifin JM, Paller A, and others. (2015) Identifying genetic determinants of atopic dermatitis and bacterial colonization using whole genome sequencing. J Allergy Clin Immunol 135(2):AB391 (abstract)
16.
go back to reference Yoshida T, Rafaels N, Babineau D, Artis K, Lockhart A, David G, Boguniewicz M, Ong P, DeBenedetto A, Hanifin J, Simpson EL, Paller AS, Guttman-Yassky E, Schneider L, Mathias R, Barnes K, Leung D, Beck LA. (2015) Filaggrin mutations do not associate with skin colonization in European American atopic dermatitis subjects. J Invest Dermatol 135:S58–S69 (abstract) Yoshida T, Rafaels N, Babineau D, Artis K, Lockhart A, David G, Boguniewicz M, Ong P, DeBenedetto A, Hanifin J, Simpson EL, Paller AS, Guttman-Yassky E, Schneider L, Mathias R, Barnes K, Leung D, Beck LA. (2015) Filaggrin mutations do not associate with skin colonization in European American atopic dermatitis subjects. J Invest Dermatol 135:S58–S69 (abstract)
17.
go back to reference De Koning HD, Kamsteeg M, Rodijk-Olthuis D, Van Vlijmen-Willems IM, Van Erp PE, Schalkwijk J, Zeeuwen PL (2011) Epidermal expression of host response genes upon skin barrier disruption in normal skin and uninvolved skin of psoriasis and atopic dermatitis patients. J Invest Dermatol 131:263–266CrossRefPubMed De Koning HD, Kamsteeg M, Rodijk-Olthuis D, Van Vlijmen-Willems IM, Van Erp PE, Schalkwijk J, Zeeuwen PL (2011) Epidermal expression of host response genes upon skin barrier disruption in normal skin and uninvolved skin of psoriasis and atopic dermatitis patients. J Invest Dermatol 131:263–266CrossRefPubMed
18.
go back to reference Niebuhr M, Heratizadeh A, Wichmann K, Satzger I, Werfel T (2011) Intrinsic alterations of pro-inflammatory mediators in unstimulated and TLR-2 stimulated keratinocytes from atopic dermatitis patients. Exp Dermatol 20:468–472CrossRefPubMed Niebuhr M, Heratizadeh A, Wichmann K, Satzger I, Werfel T (2011) Intrinsic alterations of pro-inflammatory mediators in unstimulated and TLR-2 stimulated keratinocytes from atopic dermatitis patients. Exp Dermatol 20:468–472CrossRefPubMed
19.
go back to reference Ahmad-Nejad M-DS, Breuer K, Klotz M, Werfel T, Herz U, Heeg K, Neumaier M, Renz H (2004) The toll-like receptor 2 R753Q polymorphism defines a subgroup of patients with atopic dermatitis having severe phenotype. J Allergy Clin Immunol 113:565–567CrossRefPubMed Ahmad-Nejad M-DS, Breuer K, Klotz M, Werfel T, Herz U, Heeg K, Neumaier M, Renz H (2004) The toll-like receptor 2 R753Q polymorphism defines a subgroup of patients with atopic dermatitis having severe phenotype. J Allergy Clin Immunol 113:565–567CrossRefPubMed
20.
go back to reference Oh DY, Schumann RR, Hamann L, Neumann K, Worm M, Heine G (2009) Association of the toll-like receptor 2 A-16934T promoter polymorphism with severe atopic dermatitis. Allergy 64:1608–1615CrossRefPubMed Oh DY, Schumann RR, Hamann L, Neumann K, Worm M, Heine G (2009) Association of the toll-like receptor 2 A-16934T promoter polymorphism with severe atopic dermatitis. Allergy 64:1608–1615CrossRefPubMed
21.
go back to reference Kuo IH, Carpenter-Mendini A, Yoshida T, McGirt LY, Ivanov AI, Barnes KC, Gallo RL, Borkowski AW, Yamasaki K, Leung DY, Georas SN, De Benedetto A, Beck LA (2013) Activation of epidermal toll-like receptor 2 enhances tight junction function: implications for atopic dermatitis and skin barrier repair. J Invest Dermatol 133:988–998CrossRefPubMed Kuo IH, Carpenter-Mendini A, Yoshida T, McGirt LY, Ivanov AI, Barnes KC, Gallo RL, Borkowski AW, Yamasaki K, Leung DY, Georas SN, De Benedetto A, Beck LA (2013) Activation of epidermal toll-like receptor 2 enhances tight junction function: implications for atopic dermatitis and skin barrier repair. J Invest Dermatol 133:988–998CrossRefPubMed
22.
go back to reference Skabytska Y, Wölbing F, Günther C, Köberle M, Kaesler S, Chen KM, Guenova E, Demircioglu D, Kempf WE, Volz T, Rammensee HG, Schaller M, Röcken M, Götz F, Biedermann T (2014) Cutaneous innate immune sensing of Toll-like receptor 2–6 ligands suppresses T cell immunity by inducing myeloid-derived suppressor cells. Immunity 41:762–775CrossRefPubMed Skabytska Y, Wölbing F, Günther C, Köberle M, Kaesler S, Chen KM, Guenova E, Demircioglu D, Kempf WE, Volz T, Rammensee HG, Schaller M, Röcken M, Götz F, Biedermann T (2014) Cutaneous innate immune sensing of Toll-like receptor 2–6 ligands suppresses T cell immunity by inducing myeloid-derived suppressor cells. Immunity 41:762–775CrossRefPubMed
23.
go back to reference Vu AT, Chen X, Xie Y, Kamijo S, Ushio H, Kawasaki J, Hara M, Ikeda S, Okumura K, Ogawa H, Takai T (2011) Extracellular double-stranded RNA induces TSLP via an endosomal acidification- and NF-kB-dependent pathway in human keratinocytes. J Invest Dermatol 131:2205–2212CrossRefPubMed Vu AT, Chen X, Xie Y, Kamijo S, Ushio H, Kawasaki J, Hara M, Ikeda S, Okumura K, Ogawa H, Takai T (2011) Extracellular double-stranded RNA induces TSLP via an endosomal acidification- and NF-kB-dependent pathway in human keratinocytes. J Invest Dermatol 131:2205–2212CrossRefPubMed
24.
go back to reference Soumelis V, Reche PA, Kanzler H, Yuan W, Edward G, Homey B, Gilliet M, Ho S, Antonenko S, Lauerma A, Smith K, Gorman D, Zurawski S, Abrams J, Menon S, McClanahan T, De Waal-Malefyt RR, Bazan F, Kastelein RA, Liu YJ (2002) Human epithelial cells trigger dendritic cell mediated allergic inflammation by producing TSLP. Nat Immunol 3:673–680CrossRefPubMed Soumelis V, Reche PA, Kanzler H, Yuan W, Edward G, Homey B, Gilliet M, Ho S, Antonenko S, Lauerma A, Smith K, Gorman D, Zurawski S, Abrams J, Menon S, McClanahan T, De Waal-Malefyt RR, Bazan F, Kastelein RA, Liu YJ (2002) Human epithelial cells trigger dendritic cell mediated allergic inflammation by producing TSLP. Nat Immunol 3:673–680CrossRefPubMed
25.
go back to reference Nakajima S, Igyártó BZ, Honda T, Egawa G, Otsuka A, Hara-Chikuma M, Watanabe N, Ziegler SF, Tomura M, Inaba K, Miyachi Y, Kaplan DH, Kabashima K (2012) Langerhans cells are critical in epicutaneous sensitization with protein antigen via thymic stromal lymphopoietin receptor signaling. J Allergy Clin Immunol 129:1048–1055, e6 CrossRefPubMedPubMedCentral Nakajima S, Igyártó BZ, Honda T, Egawa G, Otsuka A, Hara-Chikuma M, Watanabe N, Ziegler SF, Tomura M, Inaba K, Miyachi Y, Kaplan DH, Kabashima K (2012) Langerhans cells are critical in epicutaneous sensitization with protein antigen via thymic stromal lymphopoietin receptor signaling. J Allergy Clin Immunol 129:1048–1055, e6 CrossRefPubMedPubMedCentral
26.
go back to reference Ong PY, Ohtake T, Brandt C, Strickland I, Boguniewicz M, Ganz T, Gallo RL, Leung DY (2002) Endogenous antimicrobial peptides and skin infections in atopic dermatitis. N Engl J Med 347:1151–1160CrossRefPubMed Ong PY, Ohtake T, Brandt C, Strickland I, Boguniewicz M, Ganz T, Gallo RL, Leung DY (2002) Endogenous antimicrobial peptides and skin infections in atopic dermatitis. N Engl J Med 347:1151–1160CrossRefPubMed
27.
go back to reference Kim BS, Siracusa MC, Saenz SA, Noti M, Monticelli LA, Sonnenberg GF, Hepworth MR, Van Voorhees AS, Comeau MR, Artis D. (2013) TSLP elicits IL-33-independent innate lymphoid cell responses to promote skin inflammation. Sci Transl Med 5:170ra16 Kim BS, Siracusa MC, Saenz SA, Noti M, Monticelli LA, Sonnenberg GF, Hepworth MR, Van Voorhees AS, Comeau MR, Artis D. (2013) TSLP elicits IL-33-independent innate lymphoid cell responses to promote skin inflammation. Sci Transl Med 5:170ra16
28.
go back to reference Spits H, Artis D, Colonna M, Diefenbach A, Di Santo JP, Eberl G, Koyasu S, Locksley RM, McKenzie AN, Mebius RE, Powrie F, Vivier E (2013) Innate lymphoid cells—a proposal for uniform nomenclature. Nat Rev Immunol 13:145–149CrossRefPubMed Spits H, Artis D, Colonna M, Diefenbach A, Di Santo JP, Eberl G, Koyasu S, Locksley RM, McKenzie AN, Mebius RE, Powrie F, Vivier E (2013) Innate lymphoid cells—a proposal for uniform nomenclature. Nat Rev Immunol 13:145–149CrossRefPubMed
29.
go back to reference Savinko T, Matikainen S, Saarialho-Kere U, Lehto M, Wang G, Lehtimäki S, Karisola P, Reunala T, Wolff H, Lauerma A, Alenius H (2012) IL-33 and ST2 in atopic dermatitis: expression profiles and modulation by triggering factors. J Invest Dermatol 132:1392–1400CrossRefPubMed Savinko T, Matikainen S, Saarialho-Kere U, Lehto M, Wang G, Lehtimäki S, Karisola P, Reunala T, Wolff H, Lauerma A, Alenius H (2012) IL-33 and ST2 in atopic dermatitis: expression profiles and modulation by triggering factors. J Invest Dermatol 132:1392–1400CrossRefPubMed
30.
go back to reference Hvid M, Vestergaard C, Kemp K, Christensen GB, Deleuran B, Deleuran M (2011) IL-25 in atopic dermatitis: a possible link between inflammation and skin barrier dysfunction? J Invest Dermatol 131:150–157CrossRefPubMed Hvid M, Vestergaard C, Kemp K, Christensen GB, Deleuran B, Deleuran M (2011) IL-25 in atopic dermatitis: a possible link between inflammation and skin barrier dysfunction? J Invest Dermatol 131:150–157CrossRefPubMed
31.
go back to reference Kim BE, Bin L, Ye YM, Ramamoorthy P, Leung DY (2013) IL-25 enhances HSV-1 replication by inhibiting filaggrin expression, and acts synergistically with Th2 cytokines to enhance HSV-1 replication. J Invest Dermatol 133:2678–2685CrossRefPubMedPubMedCentral Kim BE, Bin L, Ye YM, Ramamoorthy P, Leung DY (2013) IL-25 enhances HSV-1 replication by inhibiting filaggrin expression, and acts synergistically with Th2 cytokines to enhance HSV-1 replication. J Invest Dermatol 133:2678–2685CrossRefPubMedPubMedCentral
32.
go back to reference Alase A, Seltmann J, Werfel T, Wittmann M (2012) Interleukin-33 modulates the expression of human β-defensin 2 in human primary keratinocytes and may influence the susceptibility to bacterial superinfection in acute atopic dermatitis. Br J Dermatol 167:1386–1389CrossRefPubMed Alase A, Seltmann J, Werfel T, Wittmann M (2012) Interleukin-33 modulates the expression of human β-defensin 2 in human primary keratinocytes and may influence the susceptibility to bacterial superinfection in acute atopic dermatitis. Br J Dermatol 167:1386–1389CrossRefPubMed
33.
go back to reference Hayakawa K, Hirahara K, Fukuda T, Okazaki M, Shiohara T (2009) Risk factors for severe impetiginized atopic dermatitis in Japan and assessment of its microbiological features. Clin Exp Dermatol 34:e63–e65CrossRefPubMed Hayakawa K, Hirahara K, Fukuda T, Okazaki M, Shiohara T (2009) Risk factors for severe impetiginized atopic dermatitis in Japan and assessment of its microbiological features. Clin Exp Dermatol 34:e63–e65CrossRefPubMed
34.
go back to reference Benenson S, Zimhony O, Dahan D, Solomon M, Raveh D, Schlesinger Y, Yinnon AM (2005) Atopic dermatitis—a risk factor for invasive Staphylococcus aureus infections: two cases and review. Am J Med 118:1048–1051CrossRefPubMed Benenson S, Zimhony O, Dahan D, Solomon M, Raveh D, Schlesinger Y, Yinnon AM (2005) Atopic dermatitis—a risk factor for invasive Staphylococcus aureus infections: two cases and review. Am J Med 118:1048–1051CrossRefPubMed
35.
go back to reference Wolk K, Mitsui H, Witte K, Gellrich S, Gulati N, Humme D, Witte E, Gonsior M, Beyer M, Kadin ME, Volk HD, Krueger JG, Sterry W, Sabat R (2014) Deficient cutaneous antibacterial competence in cutaneous T-cell lymphomas: role of Th2-mediated biased Th17 function. Clin Cancer Res 20:5507–5516CrossRefPubMed Wolk K, Mitsui H, Witte K, Gellrich S, Gulati N, Humme D, Witte E, Gonsior M, Beyer M, Kadin ME, Volk HD, Krueger JG, Sterry W, Sabat R (2014) Deficient cutaneous antibacterial competence in cutaneous T-cell lymphomas: role of Th2-mediated biased Th17 function. Clin Cancer Res 20:5507–5516CrossRefPubMed
36.
go back to reference Staumont-Sallé D, Fleury S, Lazzari A, Molendi-Coste O, Hornez N, Lavogiez C, Kanda A, Wartelle J, Fries A, Pennino D, Mionnet C, Prawitt J, Bouchaert E, Delaporte E, Glaichenhaus N, Staels B, Julia V, Dombrowicz D (2014) CX3CL1 (fractalkine) and its receptor CX3CR1 regulate atopic dermatitis by controlling effector T cell retention in inflamed skin. J Exp Med 211:1185–1196CrossRefPubMedPubMedCentral Staumont-Sallé D, Fleury S, Lazzari A, Molendi-Coste O, Hornez N, Lavogiez C, Kanda A, Wartelle J, Fries A, Pennino D, Mionnet C, Prawitt J, Bouchaert E, Delaporte E, Glaichenhaus N, Staels B, Julia V, Dombrowicz D (2014) CX3CL1 (fractalkine) and its receptor CX3CR1 regulate atopic dermatitis by controlling effector T cell retention in inflamed skin. J Exp Med 211:1185–1196CrossRefPubMedPubMedCentral
37.
go back to reference Echigo T, Hasegawa M, Shimada Y, Takehara K, Sato S (2004) Expression of fractalkine and its receptor, CX3CR1, in atopic dermatitis: possible contribution to skin inflammation. J Allergy Clin Immunol 113:940–948CrossRefPubMed Echigo T, Hasegawa M, Shimada Y, Takehara K, Sato S (2004) Expression of fractalkine and its receptor, CX3CR1, in atopic dermatitis: possible contribution to skin inflammation. J Allergy Clin Immunol 113:940–948CrossRefPubMed
38.
go back to reference Leung DY, Hanifin JM, Pariser DM, Barber KA, Langley RG, Schlievert PM, Abrams B, Hultsch T (2009) Effects of pimecrolimus cream 1% in the treatment of patients with atopic dermatitis who demonstrate a clinical insensitivity to topical corticosteroids: a randomized, multicentre vehicle-controlled trial. Br J Dermatol 161(2):435–443CrossRefPubMed Leung DY, Hanifin JM, Pariser DM, Barber KA, Langley RG, Schlievert PM, Abrams B, Hultsch T (2009) Effects of pimecrolimus cream 1% in the treatment of patients with atopic dermatitis who demonstrate a clinical insensitivity to topical corticosteroids: a randomized, multicentre vehicle-controlled trial. Br J Dermatol 161(2):435–443CrossRefPubMed
39.
go back to reference Schlievert PM, Strandberg KL, Lin YC, Peterson ML, Leung DYM (2010) Secreted virulence factor comparison between methicillin-resistant and methicillin-sensitive Staphylococcus aureus, and its relevance to atopic dermatitis. J Allergy Clin Immunol 125:39–49CrossRefPubMedPubMedCentral Schlievert PM, Strandberg KL, Lin YC, Peterson ML, Leung DYM (2010) Secreted virulence factor comparison between methicillin-resistant and methicillin-sensitive Staphylococcus aureus, and its relevance to atopic dermatitis. J Allergy Clin Immunol 125:39–49CrossRefPubMedPubMedCentral
40.
go back to reference Warner JA, McGirt LY, Beck LA (2009) Biomarkers of Th2 polarity are predictive of staphylococcal colonization in subjects with atopic dermatitis. Br J Dermatol 160:183–185CrossRefPubMed Warner JA, McGirt LY, Beck LA (2009) Biomarkers of Th2 polarity are predictive of staphylococcal colonization in subjects with atopic dermatitis. Br J Dermatol 160:183–185CrossRefPubMed
41.
go back to reference Jagadeesan S, Kurien G, Divakaran MV, Sadanandan SM, Sobhanakumari K, Sarin A (2014) Methicillin-resistant Staphylococcus aureus colonization and disease severity in atopic dermatitis: a cross-sectional study from South India. Indian J Dermatol Venereol Leprol 80:229–234CrossRefPubMed Jagadeesan S, Kurien G, Divakaran MV, Sadanandan SM, Sobhanakumari K, Sarin A (2014) Methicillin-resistant Staphylococcus aureus colonization and disease severity in atopic dermatitis: a cross-sectional study from South India. Indian J Dermatol Venereol Leprol 80:229–234CrossRefPubMed
42.
go back to reference Lo WT, Wang SR, Tseng MH, Huang CF, Chen SJ, Wang CC (2010) Comparative molecular analysis of meticillin-resistant Staphylococcus aureus isolates from children with atopic dermatitis and healthy subjects in Taiwan. Br J Dermatol 162:1110–1116CrossRefPubMed Lo WT, Wang SR, Tseng MH, Huang CF, Chen SJ, Wang CC (2010) Comparative molecular analysis of meticillin-resistant Staphylococcus aureus isolates from children with atopic dermatitis and healthy subjects in Taiwan. Br J Dermatol 162:1110–1116CrossRefPubMed
43.
go back to reference Ong PY (2014) Recurrent MRSA infections in atopic dermatitis. J Allergy Clin Immunol Pract 2:396–399CrossRefPubMed Ong PY (2014) Recurrent MRSA infections in atopic dermatitis. J Allergy Clin Immunol Pract 2:396–399CrossRefPubMed
44.
go back to reference Leung DYM (2005) Superantigens, steroid insensitivity and innate immunity in atopic eczema. Acta Derm Venereol Suppl (Stockh) 215:11–15CrossRef Leung DYM (2005) Superantigens, steroid insensitivity and innate immunity in atopic eczema. Acta Derm Venereol Suppl (Stockh) 215:11–15CrossRef
45.
go back to reference Sonkoly E, Muller A, Lauerma AI, Pivarcsi A, Soto H, Kemeny L, Alenius H, Dieu-Nosjean MC, Meller S, Rieker J, Steinhoff M, Hoffmann TK, Ruzicka T, Zlotnik A, Homey B (2006) IL-31: a new link between T cells and pruritus in atopic skin inflammation. J Allergy Clin Immunol 117:411–417CrossRefPubMed Sonkoly E, Muller A, Lauerma AI, Pivarcsi A, Soto H, Kemeny L, Alenius H, Dieu-Nosjean MC, Meller S, Rieker J, Steinhoff M, Hoffmann TK, Ruzicka T, Zlotnik A, Homey B (2006) IL-31: a new link between T cells and pruritus in atopic skin inflammation. J Allergy Clin Immunol 117:411–417CrossRefPubMed
46.
go back to reference Cornelissen C, Marquardt Y, Czaja K, Wenzel J, Frank J, Lüscher-Firzlaff J, Lüscher B, Baron JM (2012) IL-31 regulates differentiation and filaggrin expression in human organotypic skin models. J Allergy Clin Immunol 129:426–433, e1-8 CrossRefPubMed Cornelissen C, Marquardt Y, Czaja K, Wenzel J, Frank J, Lüscher-Firzlaff J, Lüscher B, Baron JM (2012) IL-31 regulates differentiation and filaggrin expression in human organotypic skin models. J Allergy Clin Immunol 129:426–433, e1-8 CrossRefPubMed
47.
go back to reference van Drongelen V, Haisma EM, Out-Luiting JJ, Nibbering PH, El Ghalbzouri A (2014) Reduced filaggrin expression is accompanied by increased Staphylococcus aureus colonization of epidermal skin models. Clin Exp Allergy 44:1515–1524CrossRefPubMed van Drongelen V, Haisma EM, Out-Luiting JJ, Nibbering PH, El Ghalbzouri A (2014) Reduced filaggrin expression is accompanied by increased Staphylococcus aureus colonization of epidermal skin models. Clin Exp Allergy 44:1515–1524CrossRefPubMed
48.
go back to reference Breuer K, Wittmann M, Kempe K, Kapp A, Mai U, Dittrich-Breiholz O, Kracht M, Mrabet-Dahbi S, Werfel T (2005) Alpha-toxin is produced by skin colonizing Staphylococcus aureus and induces a T helper type 1 response in atopic dermatitis. Clin Exp Allergy 35:1088–1095CrossRefPubMed Breuer K, Wittmann M, Kempe K, Kapp A, Mai U, Dittrich-Breiholz O, Kracht M, Mrabet-Dahbi S, Werfel T (2005) Alpha-toxin is produced by skin colonizing Staphylococcus aureus and induces a T helper type 1 response in atopic dermatitis. Clin Exp Allergy 35:1088–1095CrossRefPubMed
49.
go back to reference Ezepchuk YV, Leung DYM, Middleton MH, Bina P, Reiser R, Norris DA (1996) Staphylococcal toxins and protein A differentially induce cytotoxicity and release of tumor necrosis factor-alpha from human keratinocytes. J Invest Dermatol 107:603–609CrossRefPubMed Ezepchuk YV, Leung DYM, Middleton MH, Bina P, Reiser R, Norris DA (1996) Staphylococcal toxins and protein A differentially induce cytotoxicity and release of tumor necrosis factor-alpha from human keratinocytes. J Invest Dermatol 107:603–609CrossRefPubMed
50.
go back to reference Brauweiler AM, Bin L, Kim BE, Oyoshi MK, Geha RS, Goleva E, Leung DY (2013) Filaggrin-dependent secretion of sphingomyelinase protects against staphylococcal α-toxin-induced keratinocyte death. J Allergy Clin Immunol 131:421–427CrossRefPubMed Brauweiler AM, Bin L, Kim BE, Oyoshi MK, Geha RS, Goleva E, Leung DY (2013) Filaggrin-dependent secretion of sphingomyelinase protects against staphylococcal α-toxin-induced keratinocyte death. J Allergy Clin Immunol 131:421–427CrossRefPubMed
51.
go back to reference Brauweiler AM, Goleva E, Leung DY (2014) Th2 cytokines increase Staphylococcus aureus alpha toxin-induced keratinocyte death through the signal transducer and activator of transcription 6 (STAT6). J Invest Dermatol 134:2114–2121CrossRefPubMedPubMedCentral Brauweiler AM, Goleva E, Leung DY (2014) Th2 cytokines increase Staphylococcus aureus alpha toxin-induced keratinocyte death through the signal transducer and activator of transcription 6 (STAT6). J Invest Dermatol 134:2114–2121CrossRefPubMedPubMedCentral
52.
53.
go back to reference Kaesler S, Volz T, Skabytska Y, Köberle M, Hein U, Chen KM, Guenova E, Wölbing F, Röcken M, Biedermann T (2014) Toll-like receptor 2 ligands promote chronic atopic dermatitis through IL-4-mediated suppression of IL-10. J Allergy Clin Immunol 134:92–99CrossRefPubMed Kaesler S, Volz T, Skabytska Y, Köberle M, Hein U, Chen KM, Guenova E, Wölbing F, Röcken M, Biedermann T (2014) Toll-like receptor 2 ligands promote chronic atopic dermatitis through IL-4-mediated suppression of IL-10. J Allergy Clin Immunol 134:92–99CrossRefPubMed
54.
go back to reference Vu AT, Baba T, Chen X, Le TA, Kinoshita H, Xie Y, Kamijo S, Hiramatsu K, Ikeda S, Ogawa H, Okumura K, Takai T (2010) Staphylococcus aureus membrane and diacylated lipopeptide induce thymic stromal lymphopoietin in keratinocytes through the Toll-like receptor 2-Toll-like receptor 6 pathway. J Allergy Clin Immunol 126:985–993, 993.e1-3 CrossRefPubMed Vu AT, Baba T, Chen X, Le TA, Kinoshita H, Xie Y, Kamijo S, Hiramatsu K, Ikeda S, Ogawa H, Okumura K, Takai T (2010) Staphylococcus aureus membrane and diacylated lipopeptide induce thymic stromal lymphopoietin in keratinocytes through the Toll-like receptor 2-Toll-like receptor 6 pathway. J Allergy Clin Immunol 126:985–993, 993.e1-3 CrossRefPubMed
55.
go back to reference Grice EA, Kong HH, Renaud G, Young AC, Comparative Sequencing Program NISC, Bouffard GG, Blakesley RW, Wolfsberg TG, Turner ML, Segre JA (2008) A diversity profile of the human skin microbiota. Genome Res 18:1043–1050CrossRefPubMedPubMedCentral Grice EA, Kong HH, Renaud G, Young AC, Comparative Sequencing Program NISC, Bouffard GG, Blakesley RW, Wolfsberg TG, Turner ML, Segre JA (2008) A diversity profile of the human skin microbiota. Genome Res 18:1043–1050CrossRefPubMedPubMedCentral
56.
go back to reference Kong HH, Oh J, Deming C, Conlan S, Grice EA, Beatson MA, Nomicos E, Polley EC, Komarow HD, Program NSCCS, Murray PR, Turner ML, Segre JA (2012) Temporal shifts in the skin microbiome associated with disease flares and treatment in children with atopic dermatitis. Genome Res 22:850–859CrossRefPubMedPubMedCentral Kong HH, Oh J, Deming C, Conlan S, Grice EA, Beatson MA, Nomicos E, Polley EC, Komarow HD, Program NSCCS, Murray PR, Turner ML, Segre JA (2012) Temporal shifts in the skin microbiome associated with disease flares and treatment in children with atopic dermatitis. Genome Res 22:850–859CrossRefPubMedPubMedCentral
58.
go back to reference Beck LA, Boguniewicz M, Hata T, Schneider LC, Hanifin J, Gallo R, Paller AS, Lieff S, Reese J, Zaccaro D, Milgrom H, Barnes KC, Leung DY (2009) Phenotype of atopic dermatitis subjects with a history of eczema herpeticum. J Allergy Clin Immunol 124(2):260–269CrossRefPubMedPubMedCentral Beck LA, Boguniewicz M, Hata T, Schneider LC, Hanifin J, Gallo R, Paller AS, Lieff S, Reese J, Zaccaro D, Milgrom H, Barnes KC, Leung DY (2009) Phenotype of atopic dermatitis subjects with a history of eczema herpeticum. J Allergy Clin Immunol 124(2):260–269CrossRefPubMedPubMedCentral
59.
go back to reference Wollenberg A, Zoch C, Wetzel S, Plewig G, Przybilla B (2003) Predisposing factors and clinical features of eczema herpeticum: a retrospective analysis of 100 cases. J Am Acad Dermatol 49:198–205CrossRefPubMed Wollenberg A, Zoch C, Wetzel S, Plewig G, Przybilla B (2003) Predisposing factors and clinical features of eczema herpeticum: a retrospective analysis of 100 cases. J Am Acad Dermatol 49:198–205CrossRefPubMed
60.
go back to reference Howell MD, Wollenberg A, Gallo RL, Flaig M, Streib JE, Wong C, Pavicic T, Boguniewicz M, Leung DY (2006) Cathelicidin deficiency predisposes to eczema herpeticum. J Allergy Clin Immunol 117(4):836–841CrossRefPubMedPubMedCentral Howell MD, Wollenberg A, Gallo RL, Flaig M, Streib JE, Wong C, Pavicic T, Boguniewicz M, Leung DY (2006) Cathelicidin deficiency predisposes to eczema herpeticum. J Allergy Clin Immunol 117(4):836–841CrossRefPubMedPubMedCentral
61.
go back to reference Howell MD, Gallo RL, Boguniewicz M, Jones JF, Wong C, Streib JE, Leung DY (2006) Cytokine milieu of atopic dermatitis skin subverts the innate immune response to vaccinia virus. Immunity 24(3):341–348CrossRefPubMed Howell MD, Gallo RL, Boguniewicz M, Jones JF, Wong C, Streib JE, Leung DY (2006) Cytokine milieu of atopic dermatitis skin subverts the innate immune response to vaccinia virus. Immunity 24(3):341–348CrossRefPubMed
62.
go back to reference Gao PS, Rafaels NM, Mu D, Hand T, Murray T, Boguniewicz M, Hata T, Schneider L, Hanifin JM, Gallo RL, Gao L, Beaty TH, Beck LA, Leung DY, Barnes KC (2010) Genetic variants in thymic stromal lymphopoietin are associated with atopic dermatitis and eczema herpeticum. J Allergy Clin Immunol 25:1403–1407, e4 CrossRef Gao PS, Rafaels NM, Mu D, Hand T, Murray T, Boguniewicz M, Hata T, Schneider L, Hanifin JM, Gallo RL, Gao L, Beaty TH, Beck LA, Leung DY, Barnes KC (2010) Genetic variants in thymic stromal lymphopoietin are associated with atopic dermatitis and eczema herpeticum. J Allergy Clin Immunol 25:1403–1407, e4 CrossRef
63.
go back to reference Howell MD, Gao P, Kim BE, Lesley LJ, Streib JE, Taylor PA, Zaccaro DJ, Boguniewicz M, Beck LA, Hanifin JM, Schneider LC, Hata TR, Gallo RL, Kaplan MH, Barnes KC, Leung DY (2011) The signal transducer and activator of transcription 6 gene (STAT6) increases the propensity of patients with atopic dermatitis toward disseminated viral skin infections. J Allergy Clin Immunol 128:1006–1014CrossRefPubMedPubMedCentral Howell MD, Gao P, Kim BE, Lesley LJ, Streib JE, Taylor PA, Zaccaro DJ, Boguniewicz M, Beck LA, Hanifin JM, Schneider LC, Hata TR, Gallo RL, Kaplan MH, Barnes KC, Leung DY (2011) The signal transducer and activator of transcription 6 gene (STAT6) increases the propensity of patients with atopic dermatitis toward disseminated viral skin infections. J Allergy Clin Immunol 128:1006–1014CrossRefPubMedPubMedCentral
64.
go back to reference Leung DY, Gao PS, Grigoryev DN, Rafaels NM, Streib JE, Howell MD, Taylor PA, Boguniewicz M, Canniff J, Armstrong B, Zaccaro DJ, Schneider LC, Hata TR, Hanifin JM, Beck LA, Weinberg A, Barnes KC (2011) Human atopic dermatitis complicated by eczema herpeticum is associated with abnormalities in IFN-γ response. J Allergy Clin Immuno 127:965–973, e1-5 CrossRef Leung DY, Gao PS, Grigoryev DN, Rafaels NM, Streib JE, Howell MD, Taylor PA, Boguniewicz M, Canniff J, Armstrong B, Zaccaro DJ, Schneider LC, Hata TR, Hanifin JM, Beck LA, Weinberg A, Barnes KC (2011) Human atopic dermatitis complicated by eczema herpeticum is associated with abnormalities in IFN-γ response. J Allergy Clin Immuno 127:965–973, e1-5 CrossRef
65.
go back to reference Gao PS, Leung DY, Rafaels NM, Boguniewicz M, Hand T, Gao L, Hata TR, Schneider LC, Hanifin JM, Beaty TH, Beck LA, Weinberg A, Barnes KC (2012) Genetic variants in interferon regulatory factor 2 (IRF2) are associated with atopic dermatitis and eczema herpeticum. J Invest Dermatol 132:650–657 Gao PS, Leung DY, Rafaels NM, Boguniewicz M, Hand T, Gao L, Hata TR, Schneider LC, Hanifin JM, Beaty TH, Beck LA, Weinberg A, Barnes KC (2012) Genetic variants in interferon regulatory factor 2 (IRF2) are associated with atopic dermatitis and eczema herpeticum. J Invest Dermatol 132:650–657
66.
go back to reference Bin L, Edwards MG, Heiser R, Streib JE, Richers B, Hall CF, Leung DY (2014) Identification of novel gene signatures in patients with atopic dermatitis complicated by eczema herpeticum. J Allergy Clin Immunol 134:848–855CrossRefPubMedPubMedCentral Bin L, Edwards MG, Heiser R, Streib JE, Richers B, Hall CF, Leung DY (2014) Identification of novel gene signatures in patients with atopic dermatitis complicated by eczema herpeticum. J Allergy Clin Immunol 134:848–855CrossRefPubMedPubMedCentral
67.
go back to reference Bin L, Kim BE, Brauweiler A, Goleva E, Streib J, Ji Y, Schlievert PM, Leung DY (2012) Staphylococcus aureus α-toxin modulates skin host response to viral infection. J Allergy Clin Immunol 130:683–691, e2 CrossRefPubMedPubMedCentral Bin L, Kim BE, Brauweiler A, Goleva E, Streib J, Ji Y, Schlievert PM, Leung DY (2012) Staphylococcus aureus α-toxin modulates skin host response to viral infection. J Allergy Clin Immunol 130:683–691, e2 CrossRefPubMedPubMedCentral
68.
go back to reference Wilke GA, Bubeck WJ (2010) Role of a disintegrin and metalloprotease 10 in Staphylococcus aureus alpha-hemolysin-mediated cellular injury. Proc Natl Acad Sci U S A 107:13473–13478CrossRefPubMedPubMedCentral Wilke GA, Bubeck WJ (2010) Role of a disintegrin and metalloprotease 10 in Staphylococcus aureus alpha-hemolysin-mediated cellular injury. Proc Natl Acad Sci U S A 107:13473–13478CrossRefPubMedPubMedCentral
69.
go back to reference Petersen BW, Damon IK, Pertowski CA, Meaney-Delman D, Guarnizo JT, Beigi RH, Edwards KM, Fisher MC, Frey SE, Lynfield R, Willoughby RE (2015) Clinical guidance for smallpox vaccine use in a postevent vaccination program. MMWR Recomm Rep 64:1–26CrossRefPubMed Petersen BW, Damon IK, Pertowski CA, Meaney-Delman D, Guarnizo JT, Beigi RH, Edwards KM, Fisher MC, Frey SE, Lynfield R, Willoughby RE (2015) Clinical guidance for smallpox vaccine use in a postevent vaccination program. MMWR Recomm Rep 64:1–26CrossRefPubMed
70.
go back to reference Grigoryev DN, Howell MD, Watkins T, Chen YC, Cheadle C, Boguniewicz M, Barnes KC, Leung DY (2010) Vaccinia virus-specific molecular signature in atopic dermatitis skin. J Allergy Clin Immunol 125:153–159, e28CrossRefPubMedPubMedCentral Grigoryev DN, Howell MD, Watkins T, Chen YC, Cheadle C, Boguniewicz M, Barnes KC, Leung DY (2010) Vaccinia virus-specific molecular signature in atopic dermatitis skin. J Allergy Clin Immunol 125:153–159, e28CrossRefPubMedPubMedCentral
71.
go back to reference Patera AC, Pesnicak L, Bertin J, Cohen JI (2002) Interleukin 17 modulates the immune response to vaccinia virus infection. Virology 299(1):56–63CrossRefPubMed Patera AC, Pesnicak L, Bertin J, Cohen JI (2002) Interleukin 17 modulates the immune response to vaccinia virus infection. Virology 299(1):56–63CrossRefPubMed
72.
go back to reference Oyoshi MK, Murphy GF, Geha RS (2009) Filaggrin-deficient mice exhibit TH17-dominated skin inflammation and permissiveness to epicutaneous sensitization with protein antigen. J Allergy Clin Immunol 124(3):485–493CrossRefPubMedPubMedCentral Oyoshi MK, Murphy GF, Geha RS (2009) Filaggrin-deficient mice exhibit TH17-dominated skin inflammation and permissiveness to epicutaneous sensitization with protein antigen. J Allergy Clin Immunol 124(3):485–493CrossRefPubMedPubMedCentral
73.
go back to reference Oyoshi MK, Elkhal A, Kumar L, Scott JE, Koduru S, He R, Leung DY, Howell MD, Oettgen HC, Murphy GF, Geha RS (2009) Vaccinia virus inoculation in sites of allergic skin inflammation elicits a vigorous cutaneous IL-17 response. Proc Natl Acad Sci U S A 106(35):14954–14959CrossRefPubMedPubMedCentral Oyoshi MK, Elkhal A, Kumar L, Scott JE, Koduru S, He R, Leung DY, Howell MD, Oettgen HC, Murphy GF, Geha RS (2009) Vaccinia virus inoculation in sites of allergic skin inflammation elicits a vigorous cutaneous IL-17 response. Proc Natl Acad Sci U S A 106(35):14954–14959CrossRefPubMedPubMedCentral
74.
go back to reference Oyoshi MK, Beaupré J, Venturelli N, Lewis CN, Iwakura Y, Geha RS. (2015) Filaggrin deficiency promotes the dissemination of cutaneously inoculated vaccinia virus. J Allergy Clin Immunol 135(6):1511–1518.e6 Oyoshi MK, Beaupré J, Venturelli N, Lewis CN, Iwakura Y, Geha RS. (2015) Filaggrin deficiency promotes the dissemination of cutaneously inoculated vaccinia virus. J Allergy Clin Immunol 135(6):1511–1518.e6
75.
go back to reference Mathes EF, Oza V, Frieden IJ, Cordoro KM, Yagi S, Howard R, Kristal L, Ginocchio CC, Schaffer J, Maguiness S, Bayliss S, Lara-Corrales I, Garcia-Romero MT, Kelly D, Salas M, Oberste MS, Nix WA, Glaser C, Antaya R (2013) “Eczema coxsackium" and unusual cutaneous findings in an enterovirus outbreak. Pediatrics 132:e149–e157CrossRefPubMedPubMedCentral Mathes EF, Oza V, Frieden IJ, Cordoro KM, Yagi S, Howard R, Kristal L, Ginocchio CC, Schaffer J, Maguiness S, Bayliss S, Lara-Corrales I, Garcia-Romero MT, Kelly D, Salas M, Oberste MS, Nix WA, Glaser C, Antaya R (2013) “Eczema coxsackium" and unusual cutaneous findings in an enterovirus outbreak. Pediatrics 132:e149–e157CrossRefPubMedPubMedCentral
76.
go back to reference Johnson VK, Hayman JL, McCarthy CA, Cardona ID (2014) Successful treatment of eczema coxsackium with wet wrap therapy and low-dose topical corticosteroid. J Allergy Clin Immunol Pract 2:803–804CrossRefPubMed Johnson VK, Hayman JL, McCarthy CA, Cardona ID (2014) Successful treatment of eczema coxsackium with wet wrap therapy and low-dose topical corticosteroid. J Allergy Clin Immunol Pract 2:803–804CrossRefPubMed
77.
go back to reference Harris PN, Wang AD, Yin M, Lee CK, Archuleta S (2014) Atypical hand, foot, and mouth disease: eczema coxsackium can also occur in adults. Lancet Infect Dis 14:1043CrossRefPubMed Harris PN, Wang AD, Yin M, Lee CK, Archuleta S (2014) Atypical hand, foot, and mouth disease: eczema coxsackium can also occur in adults. Lancet Infect Dis 14:1043CrossRefPubMed
Metadata
Title
Bacterial and Viral Infections in Atopic Dermatitis: a Comprehensive Review
Authors
Peck Y. Ong
Donald Y. M. Leung
Publication date
01-12-2016
Publisher
Springer US
Published in
Clinical Reviews in Allergy & Immunology / Issue 3/2016
Print ISSN: 1080-0549
Electronic ISSN: 1559-0267
DOI
https://doi.org/10.1007/s12016-016-8548-5

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