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• W2132775166 abstract "Allergic fungal rhinosinusitis (AFRS) is a noninvasive form of fungal disease mostly caused by Aspergillus species.1Schubert M.S. Allergic fungal sinusitis: pathophysiology, diagnosis and management.Med Mycol. 2009; 47: S324-30Crossref PubMed Scopus (43) Google Scholar Patients with AFRS commonly present with chronic rhinosinusitis with nasal polyps (CRSwNP), inhalant atopy with specific IgE antibodies present in serum against Aspergillus species, elevated total serum IgE, and sinus-obstructing viscoelastic eosinophil-rich material called “allergic mucin,” containing sparse numbers of fungal hyphae.1Schubert M.S. Allergic fungal sinusitis: pathophysiology, diagnosis and management.Med Mycol. 2009; 47: S324-30Crossref PubMed Scopus (43) Google Scholar This constellation of findings is shared with allergic bronchopulmonary aspergillosis. Characteristic computed tomography findings including complete opacification of at least 1 paranasal sinus, a typical heterogeneity of the signal within involved sinuses, and the expansion and attenuation/erosion of the bone with displacement of adjacent anatomic compartments can be seen in AFRS (see Fig E1 in this article’s Online Repository at www.jacionline.org).1Schubert M.S. Allergic fungal sinusitis: pathophysiology, diagnosis and management.Med Mycol. 2009; 47: S324-30Crossref PubMed Scopus (43) Google ScholarThere is no doubt that fungi can function as allergens and induce an allergic IgE-mediated reaction; allergic disease should generally be considered a superimposed problem that contributes with a variable but relatively mild impact on the inflammation seen in most patients with CRS.2Fokkens W.J. Lund V.J. Mullol J. Bachert C. Alobid I. Baroody F. et al.European position paper on rhinosinusitis and nasal polyps 2012.Rhinol Suppl. 2012; 23: 1-298Google Scholar In that line of thinking, Aspergillus species may induce the formation of specific IgE antibodies to fungal allergens; however, the exorbitant elevations in serum total IgE level that is typical for AFRS cannot be explained. We therefore hypothesized that another stimulus with superantigenic properties is involved in aspergillus-related airway disease with high IgE production.3Bachert C. Zhang N. Holtappels G. De Lobel L. van Cauwenberge P. Liu S. et al.Presence of IL-5 protein and IgE-antibodies to staphylococcal enterotoxins in nasal polyps is associated with co-morbid asthma.J Allergy Clin Immunol. 2010; 126: 962-968Abstract Full Text Full Text PDF PubMed Scopus (284) Google ScholarSuperantigens from Staphylococcus aureus are possible candidates for such an effect and have been demonstrated to be involved in upper and lower airway disease, preferentially amplifying TH2-biased inflammatory reactions in CRS with nasal polyps and asthma, and inducing a local mucosal production of high concentrations of polyclonal IgE and IgG antibodies.4Bachert C. van Steen K. Zhang N. Holtappels G. Cattaert T. Maus B. et al.Specific IgE against Staphylococcus aureus enterotoxins: an independent risk factor for asthma.J Allergy Clin Immunol. 2012; 130: 376-381Abstract Full Text Full Text PDF PubMed Scopus (133) Google Scholar The mechanisms in AFRS could be similar, with Aspergillus preparing the ground for the impact of superantigens by breaking the epithelial barrier and initiating a TH2 bias. S aureus could profit from the disturbed barrier and the weakened innate response of the sinus mucosa, partially created by this TH2-bias, leading to the alternative activation of macrophages with a decrease in phagocytotic and intracellular killing properties for the germs, and symbioses with Aspergillus species to elicit a polyclonal B- and T-cell activation.5Krysko O. Holtappels G. Zhang N. Kubica M. Deswarte K. Derycke L. et al.Alternatively activated macrophages and impaired phagocytosis of S. aureus in chronic rhinosinusitis.Allergy. 2011; 66: 396-403Crossref PubMed Scopus (122) Google Scholar A recent retrospective review showed that S aureus was significantly more prevalent in the AFRS group compared with other subsets of CRSwNP.6Clark D.W. Wenaas A. Luong A. Citardi M.J. Fakhri S. Staphylococcus aureus prevalence in allergic fungal rhinosinusitis vs other subsets of chronic rhinosinusitis with nasal polyps.Int Forum Allergy Rhinol. 2012 Oct 4; https://doi.org/10.1002/alr.21090Crossref PubMed Scopus (27) Google ScholarHere we investigated serum samples of AFRS (n = 17), CRSwNP (n = 13), and healthy control (n = 12) patients, sampled in Riyadh, Saudi Arabia, with AFRS being abundant in this region. AFRS was diagnosed according to the clinical criteria of Schubert.7Schubert M.S. Allergic fungal sinusitis: pathophysiology, diagnosis and management.Med Mycol. 2009; 47: S324-30Crossref PubMed Scopus (99) Google Scholar Aspergillus fumigatus was found in the nasal samples of patients with AFRS, but not in CRSwNP subjects or controls; concentrations of serum total IgE, specific IgE antibodies to the classical S aureus superantigens (SE-IgE), specific IgE antibodies to Aspergillus species (m3-IgE), and eosinophil cationic protein were measured by using the CAP system (Phadia, Uppsala, Sweden) as detailed earlier.6Clark D.W. Wenaas A. Luong A. Citardi M.J. Fakhri S. Staphylococcus aureus prevalence in allergic fungal rhinosinusitis vs other subsets of chronic rhinosinusitis with nasal polyps.Int Forum Allergy Rhinol. 2012 Oct 4; https://doi.org/10.1002/alr.21090Crossref PubMed Scopus (27) Google Scholar We furthermore studied formalin-fixed tissue removed from the sinuses in 3 subjects with AFRS by in situ hybridization (PNA-FISH) by using panfungal and S aureus–specific probes as detailed before.8Corriveau M.N. Zhang N. Holtappels G. Van Roy N. Bachert C. Detection of Staphylococcus aureus in nasal tissue with peptide nucleic acid – fluorescence in situ hybridization.Am J Rhinol Allergy. 2009; 23: 461-465Crossref PubMed Scopus (97) Google ScholarIn 13 of 17 sera from subjects with AFRS, but not in control or CRSwNP subjects, specific IgE to A fumigatus (m3-IgE) could be detected (median and interquartile range, 8.7 kU/L [2.3-12.9 kU/L]); total IgE level was strongly elevated above normal values in patients with AFRS (median [interquartile range], 1220 [226-3287] kU/L). Sixteen of 17 subjects with AFRS also expressed SE-IgE in serum (3.5 [0.6-7.2] kU/L). There was a significant and strong correlation of SE-IgE with total IgE (r = 0.78; P < .002), whereas m3-IgE did not correlate with total IgE (r = 0.31; P = .37). However, the co-expression of A fumigatus–specific IgE antibodies in AFRS did amplify the total IgE concentrations significantly versus CRSwNP. Serum eosinophil cationic protein tended to be higher in patients with AFRS than in control patients (21.7 vs 9.3 μg/L), but differences did not reach statistical significance. For all results, please see Table I.Table ISerum total and specific IgE concentrations (median = IQR) of patients with AFRS versus non-AFRS CRSwNP and control subjectsCRSwNPAFRSControlP valueAFRS vs CRSwNPAFRS vs controlSamples, n131712IgE (kU/L)<.005<.0001 Median220.01220.036.7 IQR96.6-448.0226.8-3287.517.7-63.0ECP (μg/L)NSNS Median10.221.79.3 IQR6.1-29.49.9-49.04.9-31.8SE-IgE (kUA/L)NS<.004 n10/1316/173/12 Median0.43.50.5 IQR0.3-0.720.64-7.20.24-0.93m3-IgE (kUA/L)<.0001<.0001 n0/1313/170/12 Median8.7 IQR2.3-12.9ECP, Eosinophil cationic protein; IQR, interquartile range; NS, not significant. Open table in a new tab In all 3 tissue samples, we could discover biofilms adherent to the epithelium, carrying fungus and S aureus together. A representative confocal microscopy, showing the staining with the fungal probe (Aspergillus species has been demonstrated in the same patients by culture), the probe for S aureus, and the three-dimensional reconstruction of the combination of both is depicted in Fig 1.On the basis of our findings of S aureus coexisting with Aspergillus species within the sinuses, and the presence of SE-IgE in the sera of nearly all subjects with AFRS, significantly correlating with the total IgE (in contrast to m3-IgE, which does not correlate with total IgE), we hypothesize that S aureus may play a crucial role in AFRS. We estimate that S aureus synergizes with or makes use of Aspergillus species in creating a TH2 tissue signature, and adds its superantigenic activities to the disease, resulting in the high total IgE concentrations typically found in AFRS.9Chakrabarti A. Denning D.W. Ferguson B.J. Ponikau J. Buzina W. Kita H. et al.Fungal rhinosinusitis: a categorization and definitional schema addressing current controversies.Laryngoscope. 2009; 119: 1809-1918Crossref PubMed Scopus (280) Google Scholar In this way, Aspergillus species and S aureus benefit from each other’s potential to overcome the mucosal barrier, bias the immune system, and cause the fulminant characteristics of AFRS.This hypothesis is supported by the published literature demonstrating a role for S aureus superantigens in upper airway disease, specifically in adult nasal polyp disease unrelated to AFRS.4Bachert C. van Steen K. Zhang N. Holtappels G. Cattaert T. Maus B. et al.Specific IgE against Staphylococcus aureus enterotoxins: an independent risk factor for asthma.J Allergy Clin Immunol. 2012; 130: 376-381Abstract Full Text Full Text PDF PubMed Scopus (133) Google Scholar The presence of SE-IgE in 10 of the 13 patients with CRSwNP and a total IgE concentration of 220 kU/L in this investigation is in line with former findings.3Bachert C. Zhang N. Holtappels G. De Lobel L. van Cauwenberge P. Liu S. et al.Presence of IL-5 protein and IgE-antibodies to staphylococcal enterotoxins in nasal polyps is associated with co-morbid asthma.J Allergy Clin Immunol. 2010; 126: 962-968Abstract Full Text Full Text PDF PubMed Scopus (284) Google Scholar, 10Gevaert P. Calus L. Van Zele T. Blomme K. De Ruyck N. Bauters W. et al.Omalizumab is effective in allergic and non-allergic patients with nasal polyposis and co-morbid asthma.J Allergy Clin Immunol. 2012 Sep 26; (pii:S0091–6749(12)01294-8. doi:)10.1016/j.jaci.2012.07.047Google Scholar Also, in CRSwNP, we reported a TH2 signature of the mucosal inflammation, which is amplified by S aureus enterotoxins resulting in high total IgE tissue and serum concentrations and an increase in the degree of eosinophilic inflammation. The involvement of S aureus and its superantigenic activities in AFRS and possibly allergic bronchopulmonary aspergillosis does open a new insight into the pathophysiology of this disease, may have an impact on our diagnostic tools in aspergillus-related airway disease, and finally may result in new therapeutic options including anti-IgE strategies.10Gevaert P. Calus L. Van Zele T. Blomme K. De Ruyck N. Bauters W. et al.Omalizumab is effective in allergic and non-allergic patients with nasal polyposis and co-morbid asthma.J Allergy Clin Immunol. 2012 Sep 26; (pii:S0091–6749(12)01294-8. doi:)10.1016/j.jaci.2012.07.047Google ScholarThe role of S aureus in the disease needs to be demonstrated by the local presence of S aureus–derived enterotoxins and S aureus–specific interventions in comparison to antifungal therapeutic approaches. The contribution of the polyclonal IgE antibodies in patients with AFRS needs to be studied by making use of anti-IgE strategies. Allergic fungal rhinosinusitis (AFRS) is a noninvasive form of fungal disease mostly caused by Aspergillus species.1Schubert M.S. Allergic fungal sinusitis: pathophysiology, diagnosis and management.Med Mycol. 2009; 47: S324-30Crossref PubMed Scopus (43) Google Scholar Patients with AFRS commonly present with chronic rhinosinusitis with nasal polyps (CRSwNP), inhalant atopy with specific IgE antibodies present in serum against Aspergillus species, elevated total serum IgE, and sinus-obstructing viscoelastic eosinophil-rich material called “allergic mucin,” containing sparse numbers of fungal hyphae.1Schubert M.S. Allergic fungal sinusitis: pathophysiology, diagnosis and management.Med Mycol. 2009; 47: S324-30Crossref PubMed Scopus (43) Google Scholar This constellation of findings is shared with allergic bronchopulmonary aspergillosis. Characteristic computed tomography findings including complete opacification of at least 1 paranasal sinus, a typical heterogeneity of the signal within involved sinuses, and the expansion and attenuation/erosion of the bone with displacement of adjacent anatomic compartments can be seen in AFRS (see Fig E1 in this article’s Online Repository at www.jacionline.org).1Schubert M.S. Allergic fungal sinusitis: pathophysiology, diagnosis and management.Med Mycol. 2009; 47: S324-30Crossref PubMed Scopus (43) Google Scholar There is no doubt that fungi can function as allergens and induce an allergic IgE-mediated reaction; allergic disease should generally be considered a superimposed problem that contributes with a variable but relatively mild impact on the inflammation seen in most patients with CRS.2Fokkens W.J. Lund V.J. Mullol J. Bachert C. Alobid I. Baroody F. et al.European position paper on rhinosinusitis and nasal polyps 2012.Rhinol Suppl. 2012; 23: 1-298Google Scholar In that line of thinking, Aspergillus species may induce the formation of specific IgE antibodies to fungal allergens; however, the exorbitant elevations in serum total IgE level that is typical for AFRS cannot be explained. We therefore hypothesized that another stimulus with superantigenic properties is involved in aspergillus-related airway disease with high IgE production.3Bachert C. Zhang N. Holtappels G. De Lobel L. van Cauwenberge P. Liu S. et al.Presence of IL-5 protein and IgE-antibodies to staphylococcal enterotoxins in nasal polyps is associated with co-morbid asthma.J Allergy Clin Immunol. 2010; 126: 962-968Abstract Full Text Full Text PDF PubMed Scopus (284) Google Scholar Superantigens from Staphylococcus aureus are possible candidates for such an effect and have been demonstrated to be involved in upper and lower airway disease, preferentially amplifying TH2-biased inflammatory reactions in CRS with nasal polyps and asthma, and inducing a local mucosal production of high concentrations of polyclonal IgE and IgG antibodies.4Bachert C. van Steen K. Zhang N. Holtappels G. Cattaert T. Maus B. et al.Specific IgE against Staphylococcus aureus enterotoxins: an independent risk factor for asthma.J Allergy Clin Immunol. 2012; 130: 376-381Abstract Full Text Full Text PDF PubMed Scopus (133) Google Scholar The mechanisms in AFRS could be similar, with Aspergillus preparing the ground for the impact of superantigens by breaking the epithelial barrier and initiating a TH2 bias. S aureus could profit from the disturbed barrier and the weakened innate response of the sinus mucosa, partially created by this TH2-bias, leading to the alternative activation of macrophages with a decrease in phagocytotic and intracellular killing properties for the germs, and symbioses with Aspergillus species to elicit a polyclonal B- and T-cell activation.5Krysko O. Holtappels G. Zhang N. Kubica M. Deswarte K. Derycke L. et al.Alternatively activated macrophages and impaired phagocytosis of S. aureus in chronic rhinosinusitis.Allergy. 2011; 66: 396-403Crossref PubMed Scopus (122) Google Scholar A recent retrospective review showed that S aureus was significantly more prevalent in the AFRS group compared with other subsets of CRSwNP.6Clark D.W. Wenaas A. Luong A. Citardi M.J. Fakhri S. Staphylococcus aureus prevalence in allergic fungal rhinosinusitis vs other subsets of chronic rhinosinusitis with nasal polyps.Int Forum Allergy Rhinol. 2012 Oct 4; https://doi.org/10.1002/alr.21090Crossref PubMed Scopus (27) Google Scholar Here we investigated serum samples of AFRS (n = 17), CRSwNP (n = 13), and healthy control (n = 12) patients, sampled in Riyadh, Saudi Arabia, with AFRS being abundant in this region. AFRS was diagnosed according to the clinical criteria of Schubert.7Schubert M.S. Allergic fungal sinusitis: pathophysiology, diagnosis and management.Med Mycol. 2009; 47: S324-30Crossref PubMed Scopus (99) Google Scholar Aspergillus fumigatus was found in the nasal samples of patients with AFRS, but not in CRSwNP subjects or controls; concentrations of serum total IgE, specific IgE antibodies to the classical S aureus superantigens (SE-IgE), specific IgE antibodies to Aspergillus species (m3-IgE), and eosinophil cationic protein were measured by using the CAP system (Phadia, Uppsala, Sweden) as detailed earlier.6Clark D.W. Wenaas A. Luong A. Citardi M.J. Fakhri S. Staphylococcus aureus prevalence in allergic fungal rhinosinusitis vs other subsets of chronic rhinosinusitis with nasal polyps.Int Forum Allergy Rhinol. 2012 Oct 4; https://doi.org/10.1002/alr.21090Crossref PubMed Scopus (27) Google Scholar We furthermore studied formalin-fixed tissue removed from the sinuses in 3 subjects with AFRS by in situ hybridization (PNA-FISH) by using panfungal and S aureus–specific probes as detailed before.8Corriveau M.N. Zhang N. Holtappels G. Van Roy N. Bachert C. Detection of Staphylococcus aureus in nasal tissue with peptide nucleic acid – fluorescence in situ hybridization.Am J Rhinol Allergy. 2009; 23: 461-465Crossref PubMed Scopus (97) Google Scholar In 13 of 17 sera from subjects with AFRS, but not in control or CRSwNP subjects, specific IgE to A fumigatus (m3-IgE) could be detected (median and interquartile range, 8.7 kU/L [2.3-12.9 kU/L]); total IgE level was strongly elevated above normal values in patients with AFRS (median [interquartile range], 1220 [226-3287] kU/L). Sixteen of 17 subjects with AFRS also expressed SE-IgE in serum (3.5 [0.6-7.2] kU/L). There was a significant and strong correlation of SE-IgE with total IgE (r = 0.78; P < .002), whereas m3-IgE did not correlate with total IgE (r = 0.31; P = .37). However, the co-expression of A fumigatus–specific IgE antibodies in AFRS did amplify the total IgE concentrations significantly versus CRSwNP. Serum eosinophil cationic protein tended to be higher in patients with AFRS than in control patients (21.7 vs 9.3 μg/L), but differences did not reach statistical significance. For all results, please see Table I. ECP, Eosinophil cationic protein; IQR, interquartile range; NS, not significant. In all 3 tissue samples, we could discover biofilms adherent to the epithelium, carrying fungus and S aureus together. A representative confocal microscopy, showing the staining with the fungal probe (Aspergillus species has been demonstrated in the same patients by culture), the probe for S aureus, and the three-dimensional reconstruction of the combination of both is depicted in Fig 1. On the basis of our findings of S aureus coexisting with Aspergillus species within the sinuses, and the presence of SE-IgE in the sera of nearly all subjects with AFRS, significantly correlating with the total IgE (in contrast to m3-IgE, which does not correlate with total IgE), we hypothesize that S aureus may play a crucial role in AFRS. We estimate that S aureus synergizes with or makes use of Aspergillus species in creating a TH2 tissue signature, and adds its superantigenic activities to the disease, resulting in the high total IgE concentrations typically found in AFRS.9Chakrabarti A. Denning D.W. Ferguson B.J. Ponikau J. Buzina W. Kita H. et al.Fungal rhinosinusitis: a categorization and definitional schema addressing current controversies.Laryngoscope. 2009; 119: 1809-1918Crossref PubMed Scopus (280) Google Scholar In this way, Aspergillus species and S aureus benefit from each other’s potential to overcome the mucosal barrier, bias the immune system, and cause the fulminant characteristics of AFRS. This hypothesis is supported by the published literature demonstrating a role for S aureus superantigens in upper airway disease, specifically in adult nasal polyp disease unrelated to AFRS.4Bachert C. van Steen K. Zhang N. Holtappels G. Cattaert T. Maus B. et al.Specific IgE against Staphylococcus aureus enterotoxins: an independent risk factor for asthma.J Allergy Clin Immunol. 2012; 130: 376-381Abstract Full Text Full Text PDF PubMed Scopus (133) Google Scholar The presence of SE-IgE in 10 of the 13 patients with CRSwNP and a total IgE concentration of 220 kU/L in this investigation is in line with former findings.3Bachert C. Zhang N. Holtappels G. De Lobel L. van Cauwenberge P. Liu S. et al.Presence of IL-5 protein and IgE-antibodies to staphylococcal enterotoxins in nasal polyps is associated with co-morbid asthma.J Allergy Clin Immunol. 2010; 126: 962-968Abstract Full Text Full Text PDF PubMed Scopus (284) Google Scholar, 10Gevaert P. Calus L. Van Zele T. Blomme K. De Ruyck N. Bauters W. et al.Omalizumab is effective in allergic and non-allergic patients with nasal polyposis and co-morbid asthma.J Allergy Clin Immunol. 2012 Sep 26; (pii:S0091–6749(12)01294-8. doi:)10.1016/j.jaci.2012.07.047Google Scholar Also, in CRSwNP, we reported a TH2 signature of the mucosal inflammation, which is amplified by S aureus enterotoxins resulting in high total IgE tissue and serum concentrations and an increase in the degree of eosinophilic inflammation. The involvement of S aureus and its superantigenic activities in AFRS and possibly allergic bronchopulmonary aspergillosis does open a new insight into the pathophysiology of this disease, may have an impact on our diagnostic tools in aspergillus-related airway disease, and finally may result in new therapeutic options including anti-IgE strategies.10Gevaert P. Calus L. Van Zele T. Blomme K. De Ruyck N. Bauters W. et al.Omalizumab is effective in allergic and non-allergic patients with nasal polyposis and co-morbid asthma.J Allergy Clin Immunol. 2012 Sep 26; (pii:S0091–6749(12)01294-8. doi:)10.1016/j.jaci.2012.07.047Google Scholar The role of S aureus in the disease needs to be demonstrated by the local presence of S aureus–derived enterotoxins and S aureus–specific interventions in comparison to antifungal therapeutic approaches. The contribution of the polyclonal IgE antibodies in patients with AFRS needs to be studied by making use of anti-IgE strategies. Appendix" @default.
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• W2132775166 title "Allergic fungal rhinosinusitis—more than a fungal disease?" @default.
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