Association between cigarette smoking and interleukin-17A expression in nasal tissues of patients with chronic rhinosinusitis and asthma

Chien-Chia Huang, Chun-Hua Wang, Chia-Hsiang Fu, Chi-Che Huang, Po-Hung Chang, Yi-Wei Chen, Chia-Chen Wu, Pei-Wen Wu, Ta-Jen Lee, Chien-Chia Huang, Chun-Hua Wang, Chia-Hsiang Fu, Chi-Che Huang, Po-Hung Chang, Yi-Wei Chen, Chia-Chen Wu, Pei-Wen Wu, Ta-Jen Lee

Abstract

Cigarette smoke plays a substantial role in the development of airway inflammatory diseases, including asthma and chronic rhinosinusitis (CRS). Interleukin (IL)-17A might contribute to cigarette smoke-related inflammation of the airway. This study aimed to investigate the association between cigarette smoking and IL-17A expression in the nasal tissues of patients with CRS and asthma.We prospectively recruited 24 patients (13 smokers, 11 nonsmokers) with CRS and asthma and 6 patients with asthma but without CRS (control group) in a tertiary medical center. Nasal mucosa was obtained as part of the nasal surgery. Protein and mRNA levels of IL-17A in the nasal tissues were determined by immunostaining and real-time polymerase chain reaction.The number of unexpected emergency clinic visits for acute asthma attacks were higher among smokers than among nonsmokers. Interleukin-17A protein and mRNA levels in the nasal tissues of smokers were greater compared to those in the nasal tissues of nonsmokers (P = 0.02 both) and control patients (P = 0.05 and 0.04, respectively).Cigarette smoking was associated with an increase in the number of unexpected emergency clinic visits due to acute asthma attack and in the expression of IL-17A in the nasal tissues of patients with airway inflammatory diseases.

Conflict of interest statement

The authors have no conflicts of interest to disclose.

Figures

Figure 1
Figure 1
Immunohistochemistry findings of evaluation of interleukin (IL)-17Aprotein expression in nasal tissues. The intensity of immunostaining was scored as weak: 70% (C, scored 5) based on the proportion of positively stained cells. The IL-17A expression levels in nasal tissues of smokers were higher compared to those in the nasal tissues of nonsmokers and control subjects (D). ∗Significance was considered at P < 0.05, analyzed by the Mann–Whitney U test. Cells were observed at a magnification of 200×. Open head, epithelium; closed head, endothelium; arrowhead, inflammatory cells; G, mucus gland. IL = interleukin.
Figure 2
Figure 2
Comparison of interleukin (IL)-12A (A), IL-4 (B), IL-5 (C), IL-13 (D), and IL-17A (E) mRNA levels in nasal tissues among smokers (n = 13), nonsmokers (n = 11), and control subjects (n = 6) based on the real-time polymerase chain reaction findings. The IL-17A mRNA levels in smokers were significantly higher compared to those in nonsmokers and control subjects (E). aAnalyzed by the Kruskal–Wallis test among the 3 groups. ∗Significance was considered at P < 0.05, analyzed by the Mann–Whitney U test. IL = interleukin.
Figure 3
Figure 3
Correlation between interleukin-17A mRNA expressions levels and various airway parameters. The mRNA expression levels of IL-17A were not correlated with the sino-nasal outcome test (SNOT)-22 (A), computed tomography (CT) (B), or asthma control test (ACT) (C) scores. However, they were well correlated with the predicted ratio of forced expiratory volume in 1s (FEV1) to forced vital capacity (FVC) (D). The data were analyzed by Spearman's correlation coefficient analysis. ∗Significance was considered at P < 0.05. ACT = asthma control test, CT = computed tomography, FEV1 = forced expiratory volume in 1s, FVC = forced vital capacity, SNOT-22 = sino-nasal outcome test-22.

References

    1. Bresciani M, Paradis L, Des Roches A, et al. Rhinosinusitis in severe asthma. J Allergy Clin Immunol 2001;107:73–80.
    1. Rosati MG, Peters AT. Relationships among allergic rhinitis, asthma, and chronic rhinosinusitis. Am J Rhinol Allergy 2016;30:44–7.
    1. Dixon AE, Kaminsky DA, Holbrook JT, et al. Allergic rhinitis and sinusitis in asthma: differential effects on symptoms and pulmonary function. Chest 2006;130:429–35.
    1. Feng CH, Miller MD, Simon RA. The united allergic airway: connections between allergic rhinitis, asthma, and chronic sinusitis. Am J Rhinol Allergy 2012;26:187–90.
    1. Ek A, Middelveld RJ, Bertilsson H, et al. Chronic rhinosinusitis in asthma is a negative predictor of quality of life: results from the Swedish GA(2) LEN survey. Allergy 2013;68:1314–21.
    1. Reh DD, Higgins TS, Smith TL. Impact of tobaccosmoke on chronicrhinosinusitis: a review of the literature. Int Forum Allergy Rhinol 2012;2:362–9.
    1. Jayes L, Haslam PL, Gratziou CG, et al. SmokeHaz: systematic reviews and meta-analyses of the effects of smoking on respiratory health. Chest 2016;150:164–79. S0012-3692(16)48547-8. doi: 10.1016/j.chest.2016.03.060.
    1. Thomson NC, Chaudhuri R, Livingston E. Asthma and cigarette smoking. Eur Respir J 2004;24:822–33.
    1. Thomson NC, Spears M. The influence of smoking on the treatment response in patients with asthma. Curr Opin Allergy Clin Immunol 2005;5:57–63.
    1. Chalmers GW, Macleod KJ, Little SA, et al. Influence of cigarette smoking on inhaled corticosteroid treatment in mild asthma. Thorax 2002;57:226–30.
    1. Chaudhuri R, Livingston E, McMahon AD, et al. Cigarette smoking impairs the therapeutic response to oral corticosteroids in chronic asthma. Am J RespirCrit Care Med 2003;168:1308–11.
    1. Hancox RJ, Gray AR, Poulton R, et al. The effect of cigarette smoking on lung function in young adults with asthma. Am J Respir Crit Care Med 2016;194:276–84.
    1. Sugiyama K, Matsuda T, Kondo H, et al. Postoperative olfaction in chronic sinusitis: smokers versus nonsmokers. Ann Otol Rhinol Laryngol 2002;111:1054–8.
    1. Briggs RD, Wright ST, Cordes S, et al. Smoking in chronic rhinosinusitis: a predictor of poor long-term outcome after endoscopic sinus surgery. Laryngoscope 2004;114:126–8.
    1. Das S, Khichi SS, Perakis H, et al. Effects of smoking on quality of life following sinus surgery: 4-year follow-up. Laryngoscope 2009;119:2284–7.
    1. Krzeski A, Galewicz A, Chmielewski R, et al. Influence of cigarette smoking on endoscopic sinus surgery long-term outcomes. Rhinology 2011;49:577–82.
    1. Lambrecht BN, Hammad H. The immunology of asthma. Nat Immunol 2015;16:45–56.
    1. Akdis CA, Bachert C, Cingi C, et al. Endotypes and phenotypes of chronic rhinosinusitis. J Allergy Clin Immunol 2013;131:1479–90.
    1. Newcomb DC, Peebles RS. Th17-mediated inflammation in asthma. Curr Opin Immunol 2013;25:10.
    1. Liu Y, Zeng M, Liu Z. Th17 response and its regulation in inflammatory upper airway diseases. Clin Exp Allergy 2015;45:602–12.
    1. Cao PP, Li HB, Wang BF, et al. Distinct immunopathologic characteristics of various types of chronic rhinosinusitis in adult Chinese. J Allergy Clin Immunol 2009;124:478–84.
    1. Chambers ES, Nanzer AM, Pfeffer PE, et al. Distinct endotypes of steroid-resistant asthma characterized by IL-17Ahigh and IFN-γhigh immunophenotypes: potential benefits of calcitriol. J Allergy Clin Immunol 2015;136:628–37.
    1. From the Global Strategy for Asthma Management and Prevention, Global Initiative for Asthma (GINA) 2014. Available from: .
    1. Fokkens WJ, Lund VJ, Mullol J, et al. EPOS 2012: European position paper on rhinosinusitis and nasal polyps 2012. A summary for otorhinolaryngologists. Rhinology 2012;50:1–2.
    1. Das S, Khichi SS, Perakis H, et al. Effects of smoking on quality of life following sinus surgery: 4-year follow-up. Laryngoscope 2009;119:2284–7.
    1. Teo KK, Ounpuu S, Hawken S, et al. Tobacco use and risk of myocardial infarction in 52 countries in the INTERHEART study: a case-control study. Lancet 2006;368:647–58.
    1. Lund VJ, Kennedy DW. Staging for rhinosinusitis. Otolaryngol Head Neck Surg 1997;117:S35–40.
    1. Lund VJ, Mackay IS. Staging in rhinosinusitus. Rhinology 1993;31:183–4.
    1. Hopkins C, Gillett S, Slack R, et al. Psychometric validity of the 22-item Sinonasal Outcome Test. Clin Otolaryngol 2009;34:447–54.
    1. Nathan RA, Sorkness CA, Kosinski M, et al. Development of the asthma control test: a survey for assessing asthma control. J Allergy Clin Immunol 2004;113:59–65.
    1. Van Crombruggen K, Zhang N, Gevaert P, et al. Pathogenesis of chronic rhinosinusitis: inflammation. J Allergy Clin Immunol 2011;128:728–32.
    1. Tan BK, Schleimer RP, Kern RC. Perspectives on the etiology of chronic rhinosinusitis. Curr Opin Otolaryngol Head Neck Surg 2010;18:21–6.
    1. Anderson GP. Endotyping asthma: new insights into key pathogenic mechanisms in a complex, heterogeneous disease. Lancet 2008;372:1107–19.
    1. Lotvall J, Akdis CA, Bacharier LB, et al. Asthma endotypes: a new approach to classification of disease entities within the asthma syndrome. J Allergy Clin Immunol 2011;127:355–60.
    1. Agache I, Akdis C, Jutel M, et al. Untangling asthma phenotypes and endotypes. Allergy 2012;67:835–46.
    1. Tomassen P, Vandeplas G, Van Zele T, et al. Inflammatory endotypes of chronic rhinosinusitis based on cluster analysis of biomarkers. J Allergy Clin Immunol 2016;137:1449–56.
    1. Akdis CA, Bachert C, Cingi C, et al. Endotypes and phenotypes of chronic rhinosinusitis: a PRACTALL document of the European Academy of Allergy and Clinical Immunology and the American Academy of Allergy, Asthma & Immunology. J Allergy Clin Immunol 2013;131:1479–90.
    1. Choy DF, Hart KM, Borthwick LA, et al. TH2 and TH17 inflammatory pathways are reciprocally regulated in asthma. Sci Transl Med 2015;7:301ra129.
    1. Newcomb DC, Boswell MG, Reiss S, et al. IL-17A inhibits airway reactivity induced by RSV infection during allergic airway inflammation. Thorax 2013;68:717–23.
    1. Brandt EB, Kovacic MB, Lee GB, et al. Diesel exhaust particle induction of IL-17A contributes to severe asthma. J Allergy Clin Immunol 2013;132:1194–204.
    1. van Voorhis M, Knopp S, Julliard W, et al. Exposure to atmospheric particulate matter enhances Th17 polarization through the aryl hydrocarbon receptor. PLoS One 2013;11:e82545.
    1. Chang Y, Al Alwan L, Risse PA, et al. Th17 cytokines induce human airway smooth muscle cell migration. J Allergy Clin Immunol 2011;127:1046–53.
    1. Chang Y, Al Alwan L, Risse PA, et al. Th17-associated cytokines promote human airway smooth muscle cell proliferation. FASEB J 2012;26:5152–60.
    1. Wen W, Liu W, Zhang L, et al. Increased neutrophilia in nasal polyps reduces the response to oral corticosteroid therapy. J Allergy Clin Immunol 2012;129:1522–8. (e5).
    1. Zheng Y, Zhao Y, Lv D, et al. Correlation between computed tomography staging and quality of life instruments in patients with chronic rhinosinusitis. Am J Rhinol Allergy 2010;24:e41–5.
    1. Huang CC, Wang CH, Fu CH, et al. The link between chronic rhinosinusitis and asthma: a questionnaire-based study. Medicine (Baltimore) 2016;95:e4294.
    1. McDougall CM, Blaylock MG, Douglas JG, et al. Nasal epithelial cells as surrogates for bronchial epithelial cells in airway inflammation studies. Am J Respir Cell Mol Biol 2008;39:560–8.
    1. Comer DM, Elborn JS, Ennis M. Comparison of nasal and bronchial epithelial cells obtained from patients with COPD. PLoS One 2012;7:e32924.

Source: PubMed

Sponsorer og samarbejdspartnere

Medicinske tilstande

Narkotikainterventioner

3
Abonner