Background: The association between staphylococcal enterotoxins and atopic dermatitis (AD) is well characterized. We aim to evaluate the association between sensitization to staphylococcal enterotoxin A (SEA) and/or B (SEB) and the development of allergic airway disease. Methods: Two hundred and seventy-four patients were grouped into allergic rhinitis (AR) and/or bronchial asthma (BA) only, AD only and AR/BA+AD. The AR/BA only group was further divided into AR only, AR and airway hyperresponsiveness (AR+AHR) and BA. The allergen-specific and total immunoglobulin E (IgE) antibodies were determined by the CAP system. The associations of sensitization to SEA/SEB with allergic airway disease were analyzed by logistic regression analysis. Results: The overall rate of sensitization to SEA/SEB was 25.7%, whereas the rate of the AD only group (45.5%) was significantly higher than that of the AR/BA only group (24.5%, χ2 = 8.1). After sensitization to SEA/SEB, the geometric mean total IgE levels were significantly elevated in patients with AR+AHR and BA, but not in those with AR only. BA patients had higher geometric mean values of SEA- and SEB-specific IgE than AR only and AR+AHR patients. Logistic regression revealed that AR/BA only was more associated with sensitization to SEA/SEB (odds ratio 6.57) than AD only and AR/BA+AD (odds ratio 2.44 and 1.72). Conclusions: Atopic status after sensitization to SEA/SEB was more closely associated with BA than with other airway allergy, implying that SEA/SEB may play a role in exacerbating airway allergy and increasing the risk of allergic airway disease. Our study suggests that staphylococcal enterotoxins play a prominent role in the pathogenesis of allergic airway disease as well as AD.

1.
Fleischer B: Superantigens. Acta Pathol Microbiol Immunol Scand 1994;102:3–12.
2.
Bachert C, Gevaert P, van Cauwenberge P: Staphylococcus aureus enterotoxins: a key in airway disease? Allergy 2002;57:480–487.
3.
Clementsen P, Jensen CB, Jarlov JO, Hannoun C, Soborg M, Norn S: Influenza A virus enhances Staphylococcus aureus-induced basophil histamine release in normal individuals and patients with intrinsic asthma. Allergy 1989;44:39–44.
4.
Oehling A, Aguila de la Coba R, Fernandez M, Leyva J, Sanz ML, Resano A: Potentiation of histamine release against inhalant allergens (Dermatophagoides pteronyssinus) with bacterial antigens in bronchial asthma. J Invest Allergol Clin Immunol 1997;7:211–216.
5.
Hauk PJ, Wenzel SE, Trumble AE, Szefler SJ, Leung DY: Increased T-cell receptor Vβ8+ 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.
6.
Herz U, Ruckert R, Wollenhaupt K, Tschernig T, Neuhaus-Steinmetz U, Pabst R, Renz H: Airway exposure to bacterial superantigen (SEB) induces lymphocyte-dependent airway inflammation associated with increased airway responsiveness – A model for non-allergic asthma. Eur J Immunol 1999;29:1021–1031.
7.
Shiomori T, Yoshida S, Miyamoto H, Makishima K: Relationship of nasal carriage of Staphylococcus aureus to pathogenesis of perennial allergic rhinitis. J Allergy Clin Immunol 2000;105:449–454.
8.
Alho OP, Karttunen TJ, Karttunen R, Tuokko H, Koskela M, Suramo I, Uhari M: Subjects with allergic rhinitis show signs of more severely impaired paranasal sinus functioning during viral colds than nonallergic subjects. Allergy 2003;58:767–771.
9.
Rossi RE, Monasterolo G: Prevalence of serum IgE antibodies to the Staphylococcus aureus enterotoxins (SEA, SEB, SEC, SED, TSST-1) in patients with persistent allergic rhinitis. Int Arch Allergy Immunol 2004;133:261–266.
10.
Bachert C, Gevaert P, Howarth P, Holtappels G, van Cauwenberge P, Johansson SG: IgE to Staphylococcal aureus enterotoxins in serum is related to severity of asthma. J Allergy Clin Immunol 2003;111:1131–1132.
11.
Howarth PH: Allergic and nonallergic rhinitis; in Adkinson NF Jr, Yunginger JW, Busse WW, Bochner BS, Holgate ST, Simons FER (eds): Middleton’s Allergy: Principles and Practice, ed 6. Philadelphia, Mosby, 2003, pp 1391–1410.
12.
National Asthma Education and Prevention Program. Expert Panel Report: Guidelines for the Diagnosis and Management of Asthma Update on Selected Topics – 2002. J Allergy Clin Immunol 2002;110:S141–S219.
13.
Johansson SG, Hourihane JO, Bousquet J, Bruijnzeel-Koomen C, Dreborg S, Haahtela T, Kowalski ML, Mygind N, Ring J, van Cauwenberge P, van Hage-Hamsten M, Wuthrich B, EAACI (the European Academy of Allergology and Cinical Immunology) nomenclature task force: A revised nomenclature for allergy. An EAACI position statement from the EAACI nomenclature task force. Allergy 2001;56:813–824.
14.
Cfzapo RO, Casaburi R, Coates AL, Enright PL, Hankinson JL, Irvin CG, MacIntyre NR, McKay RT, Wanger JS: Guidelines for methacholine and exercise challenge testing – 1999. Am J Resp Crit Care Med 2000;161:309–329.
15.
Leung DY, Harbeck R, Bina P, Reiser RF, Yang E, Norris DA, Hanifin JM, Sampson HA: 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.
16.
Bunikowski R, Mielke M, Skarabis H, Herz U, Bergmann RL, Wahn U, Renz H: 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;103:119–124.
17.
Nomura I, Tanaka K, Tomita H, Katsunuma T, Ohya Y, Ikeda N, Takeda T, Saito H, Akasawa A: Evaluation of the staphylococcal exotoxins and their specific IgE in childhood atopic dermatitis. J Allergy Clin Immunol 1999;104:441–446.
18.
Tada J, Toi Y, Akiyama H, Arata J, Kato H: Presence of specific IgE antibodies to staphylococcal enterotoxins in patients with atopic dermatitis. Eur J Dermatol 1996;6:552–554.
19.
Okano M, Takishita T, Yamamoto T, Hattori H, Yamashita Y, Nishioka S, Ogawa T, Nishizaki K: Presence and characterization of sensitization to staphylococcal enterotoxins in patients with allergic rhinitis. Am J Rhinol 2001;15:417–421.
20.
Neuber K, Steinrucke K, Ring J: Staphylococcal enterotoxin B affects in vitro IgE synthesis, interferon-gamma, interleukin-4 and interleukin-5 production in atopic eczema. Int Arch Allergy Immunol 1995;107:179–182.
21.
Kristiansen SV, Pascual V, Lipsky PE: Staphylococcal protein A induces biased production of Ig by VH3-expressing B lymphocytes. J Immunol 1994;153:2974–2982.
22.
Hofer MF, Harbeck RJ, Schlievert PM, Leung DY: Staphylococcal toxins augment specific IgE responses by atopic patients exposed to allergen. J Invest Dermatol 1999;112:171–176.
23.
Braun-Fahrlander C, Riedler J, Herz U, Eder W, Waser M, Grize L, Maisch S, Carr D, Gerlach F, Bufe A, Lauener RP, Schierl R, Renz H, Nowak D, von Mutius E, Allergy and Endotoxin Study Team: Environmental exposure to endotoxin and its relation to asthma in school-age children. N Engl J Med 2002;347:869–877.
24.
Matsui K, Nishikawa A: Lipoteichoic acid from Staphylococcus aureus enhances allergen-specific immunoglobulin E production in mice. Clin Exp Allergy 2003;33:842–848.
25.
Cazzola M, Matera MG, Rossi F: Bronchial hyperresponsiveness and bacterial respiratory infections. Clin Ther 1991;13:157–171.
26.
Breuer K, Wittmann M, Bosche B, Kapp A, Werfel T: Severe atopic dermatitis is associated with sensitization to staphylococcal enterotoxin B (SEB). Allergy 2000;55:551–555.
27.
Lin YT, Shau WY, Wang LF, Yang YH, Hwang YW, Tsai MJ, Tsao PN, Chiang BL: Comparison of serum specific IgE to staphylococcal enterotoxins between atopic children with and without atopic dermatitis. Allergy 2000;55:641–646.
28.
Sears MR, Burrows B, Flannery EM, Herbison GP, Hewitt CJ, Holdaway MD: Relation between airway responsiveness and serum IgE in children with asthma and in apparently normal children. N Engl J Med 1991;325:1067–1071.
29.
Ramsdale EH, Morris MM, Roberts RS, Hargreave FE: Asymptomatic bronchial hyperresponsiveness in rhinitis. J Allergy Clin Immunol 1985;75:573–577.
30.
Linneberg A, Nielsen NH, Frolund L, Madsen F, Dirksen A, Jorgensen T, Copenhagen Allergy Study: The link between allergic rhinitis and asthma: a prospective population-based study. The Copenhagen Allergy Study. Allergy 2002;57:1048–1052.
31.
Boulay ME, Boulet LP: The relationships between atopy, rhinitis and asthma: pathophysiological considerations. Curr Opin Allergy Immunol 2003;3:51–55.
32.
Platts-Mills TAE, Rakes G, Heymann PW: The relevance of allergen exposure to the development of asthma in childhood. J Allergy Clin Immunol 2000;105:S503–S508.
33.
Celedon JC, Soto-Quiros ME, Hanson LA, Weiss ST: The relationship among markers of allergy, asthma, allergic rhinitis, and eczema in Costa Rica. Pediatr Allergy Immunol 2002;13:91–97.
34.
Scalabrin DM, Bavbek S, Perzanowski MS, Wilson BB, Platts-Mills TA, Wheatley LM: Use of specific IgE in assessing the relevance of fungal and dust mite allergens to atopic dermatitis: a comparison with asthmatic and nonasthmatic control subjects. J Allergy Clin Immunol 1999;104:1273–1279.
35.
Sunyer J, Anto JM, Castellsague J, Soriano JB, Roca J: Total serum IgE is associated with asthma independently of specific IgE levels: the Spanish Group of the European Study of Asthma. Eur Respir J 1996;9:1880–1884.
Copyright / Drug Dosage / Disclaimer
Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.
You do not currently have access to this content.