Abstract
This prospective observational study examined whether Staphylococcus aureus (SA) nasal colonization and staphylococcal enterotoxin (SE)-specific IgE sensitization synergistically affect clinical outcomes of adults with late-onset asthma (onset age ≥ 40 years). Nasal swabs were taken to evaluate SA colonization. Serum SE-IgE level was measured. Subjects were classified into 4 groups according to SA colonization and SE-IgE sensitization positivity. Among 181 patients with late-onset asthma recruited, the proportions of SA/SE (‒/‒), SA/SE (+ /‒), SA/SE (‒/ +), and SA/SE (+ / +) were 33.7%, 15.5%, 28.2%, and 22.6%, respectively. Severe asthma was more frequent in the SA/SE (+ / +) group than in the SA/SE (‒/‒) group (41.5% vs. 13.1%). The relationship of SA/SE (+ / +) with severe asthma was significant in multivariate logistic regression (vs. SA/SE (‒/‒); adjusted odds ratio: 4.36; 95% confidence intervals: 1.50‒12.73; p = 0.007), whereas SA/SE (+ /‒) or SA/SE (‒/ +) was not. In conclusion, SA nasal colonization and SE-IgE sensitization may synergistically affect disease severity in late-onset asthmatics.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Pietrocola G, Nobile G, Rindi S, Speziale P (2017) Staphylococcus aureus manipulates innate immunity through own and host-expressed proteases. Front Cell Infect Microbiol 7:166
Zhang N, Holtappels G, Gevaert P, Patou J, Dhaliwal B, Gould H, Bachert C (2011) Mucosal tissue polyclonal IgE is functional in response to allergen and SEB. Allergy 66(1):141–148
Bachert C, Gevaert P, Howarth P, Holtappels G, van Cauwenberge P, Johansson SG (2003) IgE to Staphylococcus aureus enterotoxins in serum is related to severity of asthma. J Allergy Clin Immunol 111(5):1131–1132
Stentzel S, Teufelberger A, Nordengrun M et al (2017) Staphylococcal serine protease-like proteins are pacemakers of allergic airway reactions to Staphylococcus aureus. J Allergy Clin Immunol 139(2):492-500 e498
Teufelberger AR, Nordengrun M, Braun H et al (2018) The IL-33/ST2 axis is crucial in type 2 airway responses induced by Staphylococcus aureus-derived serine protease-like protein D. J Allergy Clin Immunol 141(2):549-559 e547
Song WJ, Sintobin I, Sohn KH et al (2016) Staphylococcal enterotoxin IgE sensitization in late-onset severe eosinophilic asthma in the elderly. Clin Exp Allergy 46(3):411–421
Bachert C, van Steen K, Zhang N, Holtappels G, Cattaert T, Maus B, Buhl R, Taube C, Korn S, Kowalski M, Bousquet J, Howarth P (2012) Specific IgE against Staphylococcus aureus enterotoxins: an independent risk factor for asthma. J Allergy Clin Immunol 130(2):376-381 e378
Won HK, Song WJ, Moon Sd, Sohn KH, Kim JY, Kim BK, Park HW, Bachert C, Cho SH (2022) Staphylococcal enterotoxin-Specific IgE sensitization: a potential predictor of fixed airflow obstruction in elderly asthma. Allergy Asthma Immunol Res 15:160–173
Davis MF, Peng RD, McCormack MC, Matsui EC (2015) Staphylococcus aureus colonization is associated with wheeze and asthma among US children and young adults. Journal of Allergy and Clinical Immunology 135(3):811-813.e815
Sorensen M, Wickman M, Sollid JU, Furberg AS, Klingenberg C (2016) Allergic disease and Staphylococcus aureus carriage in adolescents in the Arctic region of Norway. Pediatr Allergy Immunol 27(7):728–735
Kim YC, Won HK, Lee JW, Sohn KH, Kim MH, Kim TB, Chang YS, Lee BJ, Cho SH, Bachert C, Song WJ (2019) Staphylococcus aureus nasal colonization and asthma in adults: systematic review and meta-analysis. J Allergy Clin Immunol 7(2):606-615.e609
Sørensen M, Klingenberg C, Wickman M, Sollid JUE, Furberg AS, Bachert C, Bousquet J (2017) Staphylococcus aureus enterotoxin sensitization is associated with allergic poly-sensitization and allergic multimorbidity in adolescents. Allergy 72(10):1548–1555
Park HK, Yoo SJ, Kim TS, Kim BK, Jang S, Kim SY, Lee K (2022) Differences between Staphylococcus aureus nasal carriage and IgE-sensitization to Staphylococcus aureus enterotoxin on risk factors and effects in adult population. Allergy Asthma Clin Immunol 18(1):6
Chung KF, Wenzel SE, Brozek JL et al (2014) International ERS/ATS guidelines on definition, evaluation and treatment of severe asthma. Eur Respir J 43(2):343–373
Hayes SM, Biggs TC, Goldie SP, Harries PG, Walls AF, Allan RN, Pender SL, Salib RJ (2020) Staphylococcus aureus internalization in mast cells in nasal polyps: characterization of interactions and potential mechanisms. J Allergy Clin Immunol 145(1):147–159
Huvenne W, Callebaut I, Plantinga M, Vanoirbeek JA, Krysko O, Bullens DM, Gevaert P, Van Cauwenberge P, Lambrecht BN, Ceuppens JL, Bachert C, Hellings PW (2010) Staphylococcus aureus enterotoxin B facilitates allergic sensitization in experimental asthma. Clin Exp Allergy 40(7):1079–1090
Flora M, Perna F, Abbadessa S, Garziano F, Maffucci R, Maniscalco M, Mollica M, Pelaia C, Tremante E, Maffei M (2021) Basophil activation test for Staphylococcus aureus enterotoxins in severe asthmatic patients. Clin Exp Allergy 51(4):536–545
Altrichter S, Hawro T, Liedtke M, Holtappels G, Bachert C, Skov P, Maurer M (2018) In chronic spontaneous urticaria, IgE against staphylococcal enterotoxins is common and functional. Allergy 73(7):1497–1504
Funding
This research was supported by a National Research Foundation of Korea (NRF) grant funded by the Korean Government (NRF-2018R1D1A1B07049440) and by a Veterans Health Service Medical Center Research Grant, Republic of Korea (grant number: VHSMC 21002, 22036, and 23009).
Author information
Authors and Affiliations
Contributions
HKW and WJS: contributed to the study conception and design. Material preparation, data collection and analysis were performed by HKW, YY, JL, NK, JHL, JPC, TBK, SHC and WJS. The first draft of the manuscript was written by HKW and WJS and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors have no relevant financial or non-financial interests to disclose.
Ethical Approval
This study was performed in line with the principles of the Declaration of Helsinki. Approval was granted by the Ethics Committee of Asan Medical Center and Veterans Health Service Medical Center.
Informed Consent
Informed consent was obtained from all individual participants included in the study.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Won, HK., Yoo, Y., Lee, J. et al. Clinical Relevance of Staphylococcus aureus Nasal Colonization and Staphylococcal Enterotoxin-Specific IgE Sensitization in Late-Onset Asthma. Lung 201, 303–308 (2023). https://doi.org/10.1007/s00408-023-00624-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00408-023-00624-8