Our intention was to review all material published to date regarding superantigens (SAgs) and allergy from an otorhinolaryngological viewpoint to understand this association more clearly.
Methods
We identified all materials published mentioning both SAg and allergic rhinitis (AR), chronic sinusitis, asthma, and atopic dermatitis (AD) that are indexed on PubMed, Google, or the ProQuest Central databases.
Results
Staphylococcus aureus is a significant bacterial pathogen in humans and has the ability to produce enterotoxins with superantigenic features. The inflammatory response in allergy seen in both B cell and T cell may be attributed to SAgs. Sufferers of both allergic asthma with rhinitis and AR alone produce serological evidence of immunoglobulin E formation to SAgs produced by S. aureus. Perennial AR sufferers carry S. aureus more frequently and the presence of the organism within the nasal cavity may exacerbate perennial AR. SAg produced by S. aureus potentially worsens the asthmatic inflammatory response within the airway and may lead to the airways becoming hyperresponsive, as well as possibly activating T cells if asthmatic control is poor. Staphylococcal SAgs potentially increase the risk of developing chronic rhinosinusitis with nasal polyposis, additionally being a marker for more severe disease. If SAgs bring about chronic inflammatory responses in the nose and sinuses, then T cells excreting interferon-gamma may be a crucial mediator. In allergic dermatitis, S. aureus could be a key player in exacerbation of the condition. Even in younger pediatric patients with allergic dermatitis, allergic hypersensitivity to SAgs is frequent and may be a factor explaining how severe the condition becomes.
Conclusion
Just as SAgs are known to feature in many allergic conditions, they play their part in AR, chronic rhinosinusitis, asthma, and AD. Further research is required before the relationship between SAgs and allergy can be adequately explained.
CruzAAPopovTPawankarRet al.
Common characteristics of upper and lower airways in rhinitis and asthma: ARIA update, in collaboration with GA(2)LEN.Allergy. 2007;
62(Suppl 84):1–41.
2.
TogiasA.Unique mechanistic features of allergic rhinitis.J Allergy Clin Immunol. 2000;
105(6 Pt 2):S599–S604.
3.
YawnBPYungingerJWWollanPCReedCESilversteinMDHarrisAG.Allergic rhinitis in Rochester, Minnesota residents with asthma: frequency and impact on healthcare utilization.J Allergy Clin Immunol1999;
103:54–59
4.
LiuJNShinYSYooHSet al.
The prevalence of serum specific IgE to superantigens in asthma and allergic rhinitis patients.Allergy Asthma Immunol Res. 2014;
6(3):263–266.
5.
BachertCZhangNHoltappelsGet al.
Presence of IL-5 protein and IgE antibodies to staphylococcal enterotoxins in nasal polyps is associated with comorbid asthma.J Allergy Clin Immunol. 2010;
126:962–968. 968.e1–968.e6.
6.
RossiREMonasteroloG.Prevalence of serum IgE antibodies to the Staphylococcus aureus enterotoxins (SAE, SEB, SEC, SED, TSST-1) in patients with persistent allergic rhinitis.Int Arch Allergy Immunol. 2004;
133:261–266.
7.
IkezawaZKomoriJIkezawaYet al.
A role of Staphylococcus aureus, interleukin-18, nerve growth factor and semaphorin 3A, an axon guidance molecule, in pathogenesis and treatment of atopic dermatitis.Allergy Asthma Immunol Res. 2010;
2:235–246.
8.
WhiteJHermanAPullenAMKuboRKapplerJWMarrackP.The Vβ-specific superantigen staphylococcal enterotoxin B: stimulation of mature T cells and clonal deletion in neonatal mice.Cell. 1989;
56(1):27–35.
PastacaldiCLewisPHowarthP.Staphylococci and staphylococcal superantigens in asthma and rhinitis: a systematic review and meta-analysis.Allergy. 2011;
66:549–555.
11.
AckleyBJSwanBALadwigGTuckerS.Evidence-Based Nursing Care Guidelines: Medical-Surgical Interventions.
St. Louis, MO:
Mosby Elsevier; 2008:7.
12.
McCormickJKYarwoodJMSchlievertPM.Toxic shock syndrome and bacterial superantigens: an update.Annu Rev Microbiol. 2001;
55:77–104.
13.
McCormickJPetersonMLSchlievertPM.Toxins and superantigens of group A streptococci. In: FischettiVANovickRPFerrettiJJPortnoyDARoodJI, eds. Gram-Positive Pathogens.
Washington, DC:
ASM Press; 2006:47–58.
14.
DingesMMOrwinPMSchlievertPM.Exotoxins of Staphylococcus aureus. Clin Microbiol Rev. 2000;
13:16–34.
15.
FraserJD.Clarifying the mechanism of superantigen toxicity.PLoS Biol. 2011;
9(9):e1001145.
16.
LinYCPetersonML.New insights into the prevention of staphylococcal infections and toxic shock syndrome.Expert Rev Clin Pharmacol. 2010;
3(6):753–767.
17.
HermanAKapplerJMarrackPPullenAM.Superantigens: mechanism of T-cell stimulation and role in immune responses.Annu Rev Immunol. 1991;
9:745–772.
18.
MiethkeTWahlCHeegKEchtenacherBKrammerPHWagnerH.T cell-mediated lethal shock triggered in mice by the superantigen staphylococcal enterotoxin B: critical role of tumor necrosis factor.J Exp Med. 1992;
175:91–98.
19.
DellabonaPPeccoudJKapplerJMarrackPBenoistCMathisD.Superantigens interact with MHC class II molecules outside of the antigen groove.Cell. 1990;
62:1115–1121.
20.
SethASternLOttenhoffTet al.
Binary and ternary complexes between T-cell receptor, class II MHC and superantigen in vitro.Nature. 1994;
369:324–327.
21.
TuffsSWHaeryfarSMMMcCormickJK.Manipulation of innate and adaptive immunity by staphylococcal superantigens. Pathogens. 2018;
7(2):53.
22.
HermannTMarianskyJLRomeroPFleischerBMac-DonaldHR.Activation of MHC class I-restricted CD8+ CTL by bicrobial T cell mitogens. Dependence upon MHC class II expression of the target cells and Vβ usage of the responder cells.J Immunol. 1990;
144:1181–1186.
23.
MouradWSchoolPDiazAGehaRChatilaT.The staphylococcal toxic shock syndrome toxin 1 triggers B cell proliferation and differentiation via major histocompatibility complex-unrestricted cognate T/B cell interaction.J Exp Med. 1989;
170:2011–2022.
24.
BergdollMSLee WongA. Staphylococcal intoxications. In: Reimann P, Cliver D, eds. Foodborne Infections and Intoxications. New York, NY: Elsevier; 2006:524–552.
25.
XuSXMcCormickJK.Staphylococcal superantigens in colonization and disease.Front Cell Infect Microbiol. 2012;
2:52.
26.
SpauldingARSalgado-PabónWKohlerPLHorswillARLeungDYSchlievertPM.Staphylococcal and streptococcal superantigen exotoxins.Clin Microbiol Rev. 2013;
26(3):422–447.
27.
DickGFDickGH.Landmark article Jan 26, 1924: the etiology of scarlet fever.J Am Med Assoc. 1983;
250(22):3096.
28.
ProftTFraserJD. Streptococcal superantigens: biological properties and potential role in disease. In: FerrettiJJStevensDLFischettiVA, eds. Streptococcus pyogenes: Basic Biology to Clinical Manifestations [Internet].
Oklahoma City:
University of Oklahoma Health Sciences Center; 2016:445–485.
CommonsRJSmeestersPRProftTFraserJDRobins-BrowneRCurtisN.Streptococcal superantigens: categorization and clinical associations.Trends Mol Med. 2014;
20(1):48–62.
31.
BhardwajNYoungJWNisanianAJBaggersJSteinmanRM.Small amounts of superantigen, when presented on dendritic cells are sufficient to initiate T cell responses.J Exp Med. 1993;
178:633–642.
32.
MiethkeTWahlCRegeleDGausHHeegKWagnerH.Superantigen mediated shock: a cytokine release syndrome.Immunobiol1993;
189:270–284.
33.
BohachGAFastDJNelsonRDSchlievertPM.Staphylococcal and streptococcal pyrogenic toxins involved in toxic shock syndrome and related illnesses.Crit Rev Microbiol. 1990;
17:251–272.
34.
PoindexterNJSchlievertPM.Suppression of immunoglobulin secreting cells from human peripheral blood by toxic-shock-syndrome toxin-1.J Infect Dis. 1986;
153:772–779.
35.
FastDJSchlievertPMNelsonRD.Nonpurulent response to toxic shock syndrome toxin 1-producing Staphylococcus aureus. Relationship to toxin-stimulated production of tumor necrosis factor. J Immunol. 1988;
140:949–953.
36.
LuoWYuHCaoZSchoebTRMarronMDybvigK.Association of Mycoplasma arthritidis mitogen with lethal toxicity but not with arthritis in mice.Infect Immun. 2008;
76(11):4989–4998.
37.
BlackmanMAWoodlandDL.In vivo effects of superantigens.Life Sci. 1995;
57(19):1717–1735.
38.
MontefortSEllulPMontefortMCaruanaSAgius MuscatH.Increasing prevalence of asthma, allergic rhinitis but not eczema in 5- to 8-yr-old Maltese children (ISAAC).Pediatr Allergy Immunol. 2009;
20:67–71.
39.
FanCHYangTSTangSMWangQZhangZ.Diagnostic significance of serum allergen detection in diagnosis of allergic rhinitis and bronchial asthma. Zhonghua Yi Xue Za Zhi. 2008;
88:3422–3424.
40.
BrozekJLBaena-CagnaniCEBoniniSet al.
Methodology for development of the allergic rhinitis and its impact on asthma guideline 2008 update.Allergy. 2008;
63:38–46.
41.
SchubertMS.Superantigens and allergic disease. In: PawankarRHolgateSTRosenwasserLJ, eds. Allergy Frontiers: Classification and Pathomechanisms.
Tokyo, Japan:
Springer; 2009:59–77.
42.
HamelmannERolinck-WerninghausCWahnUKoppMV.Treatment with a combination of anti-IgE and specific immunotherapy for allergic rhinitis and asthma.Arb Paul Ehrlich Inst Bundesinstitut Impfstoffe Biomed Arzneim Langen Hess. 2009;
96:303–313.
43.
HellingsPWHensGMeytsIet al.
Aggravation of bronchial eosinophilia in mice by nasal and bronchial exposure to Staphylococcus aureus enterotoxin B.Clin Exp Allergy. 2006;
36:1063–1071.
44.
OkanoMHattoryHYoshinoTet al.
Nasal exposure to staphylococcal enterotoxins enhances the development of allergic rhinitis in mice.Clin Exp Allergy. 2005;
35:506–514.
45.
OehlingAFernandez-BenitezMResanoA.The antigenic potentiation of inhalant allergens by bacterial compounds in bronchial asthma.J Investig Allergol Clin Immunol. 1997;
7:266–269.
ShiomoriTYoshıdaSMiyamotoHMakishimaK.Relationship of nasal carriage of Staphylococcus aureus to pathogenesis of perennial allergic rhinitis.J Allergy Clin Immunol. 2000;
105:449–454.
49.
BachertCGevaertPZhangNvan ZeleTPerez-NovoC.Role of staphylococcal superantigens in airway disease.Chem Immunol Allergy. 2007;
93:214–236.
50.
Riechelmann, EssigADeutschleTRauARothermelBWeschtaM.Nasal carriage of Staphylococcus aureus in house dust mite allergic patients and healthy controls.Allergy. 2005;
60:1418–1423.
51.
MoonIJHongSLKimDYLeeCHRheeCSMinYG.Blocking interleukin-17 attenuates enhanced inflammation by staphylococcal enterotoxin B in murine allergic rhinitis model.Acta Otolaryngol. 2012;
132(Suppl 1):S6–S12.
52.
YangPCWangCSAnZY.A murine model of ulcerative colitis: induced with sinusitis-derived superantigen and food allergen.BMC Gastroenterol. 2005;
5:6.
53.
FakhriSChristodoulopoulosPTulicMet al.
Role of microbial toxins in the induction of glucocorticoid receptor beta expression in an explant model of rhinosinusitis.J Otolaryngol. 2003;
32(6):388–393.
54.
SutherlandERMartinRJ.Airway inflammation in chronic obstructive pulmonary disease: comparisons with asthma.J Allergy Clin Immunol. 2003;
112:819–827.
55.
EliasJ.The relationship between asthma and COPD: lessons from transgenic mice.Chest. 2004;
126(Suppl):111S–116S.
56.
Global Initiative for Chronic Obstructive Lung Disease. Global Strategy for the Diagnosis, Management and Prevention of COPD. http://goldcopd.org/. Accessed September 1, 2018. Published 2016.
57.
BachertCGevaertPHowarthPHoltappelsGVan CauwenbergePJohanssonSGO.IgE to Staphylococcus aureus enterotoxins in serum is related to severity of asthma.J Allergy Clin Immunol. 2003;
111:1131–1132.
58.
HaukPJWenzelSETrumbleAESzeflerSJLeungDY.Increased T-cell receptor vbeta8+ T cells in bronchoalveolar lavage fluid of subjects with poorly controlled asthma: a potential role for microbial superantigens.J Allergy Clin Immunol. 1999;
104:37–45.
59.
LosolPKimSHHwangEKShinYSParkHS.IL-5 promoter polymorphism enhances IgE responses to staphylococcal superantigens in adult asthmatics.Allergy Asthma Immunol Res. 2013;
5:106–109.
60.
RohdeGGavaertPHoltappelsGet al.
Increased IgE-antibodies to Staphylococcus aureus enterotoxins in patients with COPD.Respir Med. 2004;
98:858–864.
61.
FilhoEJMelloFCLupiOBicaBEPapiJAFrançaAT.Staphylococcal superantigen-specific IgE antibodies: degree of sensitization and association with severity of asthma.J Bras Pneumol. 2016;
42(5):356–361.
62.
KerzelSRogoschTStrueckerBMaierRFKabeschMZemlinM.Unlike in children with allergic asthma, IgE transcripts from preschool children with atopic dermatitis display signs of superantigen-driven activation.J Immunol. 2016;
196(12):4885–4892.
63.
TomassenPJarvisDNewsonRet al.
Staphylococcus aureus enterotoxin-specific IgE is associated with asthma in the general population: a GA(2)LEN study.Allergy. 2013:
68(10):1289–1297.
64.
KryskoOMaesTPlantingaMet al.
The adjuvant-like activity of staphylococcal enterotoxin B in a murine asthma model is independent of IL-1R signaling.Allergy. 2013;
68(4):446–453.
65.
BachertCvan SteenKZhangNet al.
Specific IgE against Staphylococcus aureus enterotoxins: an independent risk factor for asthma.J Allergy Clin Immunol. 2012;
130(2):376–381.e8.
66.
KowalskiMLCieślakMPérez-NovoCAMakowskaJSBachertC.Clinical and immunological determinants of severe/refractory asthma (SRA): association with staphylococcal superantigen-specific IgE antibodies.Allergy. 2011;
66(1):32–38.
67.
Pérez NovoCAJedrzejczak-CzechowiczMLewandowska-PolakAet al.
T cell inflammatory response, Foxp3 and TNFRS18-L regulation of peripheral blood mononuclear cells from patients with nasal polyps-asthma after staphylococcal superantigen stimulation.Clin Exp Allergy. 2010;
40(9):1323–1332.
68.
LeeJYKimHMYeYMet al.
Role of staphylococcal superantigen-specific IgE antibodies in aspirin-intolerant asthma.Allergy Asthma Proc. 2006;
27(5):341–346.
69.
LiuTKongWYangPWangB.A possible association of staphylococcus enterotoxin B-induced asthma and sinusitis.J Huazhong Univ Sci Technolog Med Sci. 2006;
26(1):63–67.
70.
SuhYJYoonSHSampsonAPet al.
Specific immunoglobulin E for staphylococcal enterotoxins in nasal polyps from patients with aspirin-intolerant asthma.Clin Exp Allergy. 2004;
34(8):1270–1275.
71.
SmartJMKempAS.Increased Th1 and Th2 allergen-induced cytokine responses in children with atopic disease.Clin Exp Allergy. 2002;
32(5):796–802.
72.
Van ZeleTGevaertPWateletJBet al.
Staphylococcus aureus colonization and IgE antibody formation to enterotoxins is increased in nasal polyposis.J Allergy Clin Immunol. 2004;
114(4):981–983.
73.
BernsteinJMAllenCRichGet al.
Further observations on the role of Staphylococcus auerus exotoxins and IgE in the pathogenesis of nasal polyposis.Laryngoscope. 2011;
121:647–655.
74.
FengCHMillerMDSimonRA.The united allergic airway: connections between allergic rhinitis, asthma, and chronic sinusitis.Am J Rhinol Allergy. 2012;
26(3):187–190.
75.
OuJWangJXuYet al.
Staphylococcus aureus superantigens are associated with chronic rhinosinusitis with nasal polyps: a meta-analysis.Eur Arch Otorhinolaryngol. 2014;
271(10):2729–2736.
76.
ThunbergUHugossonSMoneckeSEhrichtRSöderquistB.Molecular characteristics of Staphylococcus aureus associated with chronic rhinosinusitis.APMIS. 2015;
123(1):37–44.
77.
Van ZeleTVaneechoutteMHoltappelsGGevaertPvanCauwenbergePBachertC.Detection of enterotoxin DNA in Staphylococcus aureus strains obtained from the middle meatus in controls and nasal polyp patients.Am J Rhinol. 2008;
22(3):223–227.
78.
KernRCConleyDBWalshWet al.
Perspectives on the etiology of chronic rhinosinusitis: an immune barrier hypothesis.Am J Rhinol. 2008;
22(6):549–559.
79.
WangMShiPChenBet al.
The role of superantigens in chronic rhinosinusitis with nasal polyps.ORL J Otorhinolaryngol Relat Spec. 2008;
70(2):97–103.
80.
SeiberlingKAConleyDBTripathiAet al.
Superantigens and chronic rhinosinusitis: detection of staphylococcal exotoxins in nasal polyps.Laryngoscope. 2005;
115(9):1580–1585.
81.
BernsteinJMBallowMSchlievertPMRichGAllenCDryjaD.A superantigen hypothesis for the pathogenesis of chronic hyperplastic sinusitis with massive nasal polyposis.Am J Rhinol. 2003;
17(6):321–326.
82.
ChengKJXuYYZhouMLZhouSHWangSQ.Role of local allergic inflammation and Staphylococcus aureus enterotoxins in Chinese patients with chronic rhinosinusitis with nasal polyps.J Laryngol Otol. 2017;
131(8):707–713.
83.
ChenJBJamesLKDaviesAMet al.
Antibodies and superantibodies in patients with chronic rhinosinusitis with nasal polyps.J Allergy Clin Immunol. 2017;
139(4):1195–1204e11.
84.
MruwatRKivitySLandsbergRYedgarSLangierS.Phospholipase A2-dependent release of inflammatory cytokines by superantigen-stimulated nasal polyps of patients with chronic rhinosinusitis.Am J Rhinol Allergy. 2015;
29(5):e122–e128.
85.
ClarkDWWenaasALuongACitardiMJFakhriS.Staphylococcus aureus prevalence in allergic fungal rhinosinusitis vs other subsets of chronic rhinosinusitis with nasal polyps.Int Forum Allergy Rhinol. 2013;
3(2):89–93.
86.
FakhriSTulicMChristodoulopoulosPet al.
Microbial superantigens induce glucocorticoid receptor beta and steroid resistance in a nasal explant model.Laryngoscope. 2004;
114(5):887–892.
ChoKSKimCSLeeHSSeoSKParkHYRohHJ.Role of interferon-γ-producing T cells in the pathogenesis of chronic rhinosinusitis with nasal polyps associated with staphylococcal superantigen.J Otolaryngol Head Neck Surg. 2010;
39(5):600–605.
89.
el-FikyLMKhamisNMostafa BelDAdlyAM.Staphylococcal infection and toxin production in chronic rhinosinusitis.Am J Rhinol Allergy. 2009:
23(3):264–267.
90.
WangMShiPYueZet al.
Superantigens and the expression of T-cell receptor repertoire in chronic rhinosinusitis with nasal polyps.Acta Otolaryngol. 2008:
128(8):901–908.
91.
WangMMShiPZhangHPJianJFZhangDL.Relationship between Staphylococcal superantigens and the dominant expression of T-cell receptor V beta gene in chronic rhinosinusitis with nasal polyp. Zhonghua Er Bi Yan Hou Tou Jing Wai Ke Za Zhi. 2006:
41(11):830–834.
92.
FanYPXuGZuoKJet al.
Detection of specific IgE of anti-Staphylococcus aureus enterotoxins in nasal polyps and analysis theoretically about the superantigen hypothesis. Zhonghua Er Bi Yan Hou Tou Jing Wai Ke Za Zhi. 2006;
41(11):825–829.
93.
DouglasRBruhnMTanLWOoiEPsaltisAWormaldPJ.Response of peripheral blood lymphocytes to fungal extracts and staphylococcal superantigen B in chronic rhinosinusitis.Laryngoscope. 2007;
117(3):411–414.
94.
WangMZhangDZhangHpWangZChenXJianJf.A primary study about the correlation between superantigens produced by Staphylococcus aureus and chronic rhinosinusitis with nasal polyps. Lin Chuang Er Bi Yan Hou Ke Za Zhi. 2006;
20(20):914–916.
95.
DammMQuanteGRosenbohmJRieckmannR.Proinflammatory effects of Staphylococcus aureus exotoxin B on nasal epithelial cells.Otolaryngol Head Neck Surg. 2006;
134(2):245–249.
96.
TripathiAKernRConleyDBet al.
Staphylococcal exotoxins and nasal polyposis: analysis of systemic and local responses.Am J Rhinol. 2005:
19(4):327–333.
97.
TripathiAConleyDBGrammerLCet al.
Immunoglobulin E to staphylococcal and streptococcal toxins in patients with chronic sinusitis/nasal polyposis.Laryngoscope. 2004;
114(10):1822–1826.
98.
BoguniewiczMLeungDY.Atopic dermatitis: a disease of altered skin barrier and immune dysregulation.Immunol Rev. 2011;
242:233–246.
99.
Guttman-YasskyENogralesKEKruegerJG.Contrasting pathogenesis of atopic dermatitis and psoriasis. I. Clinical and pathologic concepts.J Allergy Clin Immunol. 2011;
127:1110–1118.
100.
SpergelJMPallerAS.Atopic dermatitis and the atopic march.J Allergy Clin Immunol. 2003;
112:118–127.
101.
KotzinBLLeungDYKapplerJMarrackP.Superantigens and their potential role in human disease.Adv Immunol. 1993;
54:99–166.
102.
BoguniewiczMLeungDY.Recent insights into atopic dermatitis and implications for management of infectious complications.J Allergy Clin Immunol. 2010;
125:4–15.
103.
LeungDYHarbeckRBinaPet al.
Presence of IgE antibodies to staphylococcal exotoxins on the skin of patients with atopic dermatitis. Evidence for a new group of allergens.J Clin Invest. 1993;
92:1374–1380.
104.
LinYTWangCTChaoPSet al.
Skin-homing CD4+ Foxp3+ T cells exert Th2-like function after staphylococcal superantigen stimulation in atopic dermatitis patients.Clin Exp Allergy. 2011;
41(4):516–525.
105.
ShinSYChoiGSLeeKHKimSWChoJSParkHS.IgE response to staphylococcal enterotoxins in adenoid tissues from atopic children.Laryngoscope. 2009;
119(1):171–175.
106.
Semic-JusufagicABachertCGevaertPet al.
Staphylococcus aureus sensitization and allergic disease in early childhood: population-based birth cohort study.J Allergy Clin Immunol. 2007;
119(4):930–936.
107.
NissenDPedersenLJSkovPSet al.
IgE-binding components of staphylococcal enterotoxins in patients with atopic dermatitis.Ann Allergy Asthma Immunol. 1997;
79(5):403–408.
108.
de WitJTottéJEEvan BuchemFJMPasmansSGMA.The prevalence of antibody responses against Staphylococcus aureus antigens in patients with atopic dermatitis: a systematic review and meta-analysis. Br J Dermatol. 2018;
178:1263–1271.
109.
NowrouzianFLLinaGHodilleEet al.
Superantigens and adhesins of infant gut commensal Staphylococcus aureus strains and association with subsequent development of atopic eczema.Br J Dermatol. 2017;
176(2):439–445.
110.
OrfaliRLSatoMNSantosVGet al.
Staphylococcal enterotoxin B induces specific IgG4 and IgE antibody serum levels in atopic dermatitis.Int J Dermatol. 2015;
54(8):898–904.
111.
RojoAAguinagaAMoneckeSYusteJRGastaminzaGEspañaA.Staphylococcus aureus genomic pattern and atopic dermatitis: may factors other than superantigens be involved?Eur J Clin Microbiol Infect Dis. 2014;
33(4):651–658.
112.
NadaHAGomaaNIElakhrasAWasfyRBakerRA.Skin colonization by superantigen-producing Staphylococcus aureus in Egyptian patients with atopic dermatitis and its relation to disease severity and serum interleukin-4 level.Int J Infect Dis. 2012;
16(1):e29–e33.
113.
KozmanAYaoYBinaPet al.
Encoding a superantigen by Staphylococcus aureus does not affect clinical characteristics of infected atopic dermatitis lesions.Br J Dermatol. 2010;
163(6):1308–1311.
114.
OngPYFerdmanRMChurchJA.Late-onset of IgE sensitization to microbial allergens in young children with atopic dermatitis.Br J Dermatol. 2010;
162(1):159–161.
115.
LeungDYHanifinJMPariserDMet al.
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. 2009:
161(2):435–443.
116.
OngPYPatelMFerdmanRMDunawayTChurchJA.Association of staphylococcal superantigen-specific immunoglobulin e with mild and moderate atopic dermatitis.J Pediatr. 2008:
153(6):803–806.
117.
SchlievertPMCaseLCStrandbergKLAbramsBBLeungDY.Superantigen profile of Staphylococcus aureus isolates from patients with steroid-resistant atopic dermatitis.Clin Infect Dis. 2008;
46(10):1562–1567.
118.
FukushimaHHiranoTShibayamaNet al.
The role of immune response to Staphylococcus aureus superantigens and disease severity in relation to the sensitivity to tacrolimus in atopic dermatitis.Int Arch Allergy Immunol. 2006;
141(3):281–289.
119.
KimKHHanJHChungJHChoKHEunHC.Role of staphylococcal superantigen in atopic dermatitis: influence on keratinocytes.J Korean Med Sci. 2006;
21(2):315–323.
120.
OuLSGolevaEHallCLeungDY.T regulatory cells in atopic dermatitis and subversion of their activity by superantigens.J Allergy Clin Immunol. 2004;
113(4):756–763.
121.
LinYTWangCTHsuCTet al.
Differential susceptibility to staphylococcal superantigen (SsAg)-induced apoptosis of CD4+ T cells from atopic dermatitis patients and healthy subjects: the inhibitory effect of IL-4 on SsAg-induced apoptosis.J Immunol. 2003;
171(2):1102–1108.
122.
NomuraIKatsunumaTTomikawaMet al.
Hypoproteinemia in severe childhood atopic dermatitis: a serious complication.Pediatr Allergy Immunol. 2002;
13(4):287–294.
123.
MatsuiKNishikawaASutoHTsuboiROgawaH.Comparative study of Staphylococcus aureus isolated from lesional and non-lesional skin of atopic dermatitis patients.Microbiol Immunol. 2000;
44(11):945–947.
124.
LinYTShauWYWangLFet al.
Comparison of serum specific IgE antibodies to staphylococcal enterotoxins between atopic children with and without atopic dermatitis.Allergy. 2000;
55(7):641–646.
125.
ZollnerTMWichelhausTAHartungAet al.
Colonization with superantigen-producing Staphylococcus aureus is associated with increased severity of atopic dermatitis.Clin Exp Allergy. 2000;
30(7):994–1000.
126.
BunikowskiRMielkeMESkarabisHet al.
Evidence for a disease-promoting effect of Staphylococcus aureus-derived exotoxins in atopic dermatitis.J Allergy Clin Immunol. 2000;
105(4):814–819.
127.
CampbellDEKempAS.Production of antibodies to staphylococcal superantigens in atopic dermatitis.Arch Dis Child. 1998;
79(5):400–404.
128.
StricklandIHaukPJTrumbleAEPickerLJLeungDY.Evidence for superantigen involvement in skin homing of T cells in atopic dermatitis.J Invest Dermatol. 1999;
112(2):249–253.
129.
BunikowskiRMielkeMSkarabisHet al.
Prevalence and role of serum IgE antibodies to the Staphylococcus aureus-derived superantigens SEA and SEB in children with atopic dermatitis.J Allergy Clin Immunol. 1999;
103(1 Pt 1):119–124.
130.
TorresMJGonzalezFJCorzoJLet al.
Circulating CLA+ lymphocytes from children with atopic dermatitis contain an increased percentage of cells bearing staphylococcal-related T-cell receptor variable segments.Clin Exp Allergy. 1998;
28(10):1264–1272.
131.
CampbellDEKempAS.Proliferation and production of interferon-gamma (IFN-gamma) and IL-4 in response to Staphylococcus aureus and staphylococcal superantigen in childhood atopic dermatitis.Clin Exp Immunol. 1997;
107(2):392–397.
132.
YudateTYamadaHTezukaT.Role of staphylococcal enterotoxins in pathogenesis of atopic dermatitis: growth and expression of T cell receptor V beta of peripheral blood mononuclear cells stimulated by enterotoxins A and B.J Dermatol Sci. 1996;
13(1):63–70.
133.
TanakaMAibaSTakahashiKTagamiH.Reduced proliferative responses of peripheral blood mononuclear cells specifically to Candida albicans antigen in patients with atopic dermatitis–comparison with their normal reactivity to bacterial superantigens.Arch Dermatol Res. 1996;
288(9):495–499.
134.
HoferMFLesterMRSchlievertPMLeungDY.Upregulation of IgE synthesis by staphylococcal toxic shock syndrome toxin-1 in peripheral blood mononuclear cells from patients with atopic dermatitis.Clin Exp Allergy. 1995;
25(12):1218–1227.
135.
LesterMRHoferMFRenzHTrumbleAEGelfandEWLeungDY.Modulatory effects of staphylococcal superantigen TSST-1 on IgE synthesis in atopic dermatitis.Clin Immunol Immunopathol. 1995;
77(3):332–338.
