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Research Article Serum Levels of Epithelial-Derived Cytokines As Interleukin-25 and Thymic Stromal Lymphopoietin After a Single

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Research Article Serum Levels of Epithelial-Derived Cytokines As Interleukin-25 and Thymic Stromal Lymphopoietin After a Single Hindawi Canadian Respiratory Journal Volume 2019, Article ID 8607657, 7 pages https://doi.org/10.1155/2019/8607657 Research Article Serum Levels of Epithelial-Derived Cytokines as Interleukin-25 and Thymic Stromal Lymphopoietin after a Single Dose of Mepolizumab in Patients with Severe Non-Allergic Eosinophilic Asthma: A Short Report Virginija Kalinauskaite-Zukauske ,1 Andrius Januskevicius,2 Ieva Janulaityte,2 Skaidrius Miliauskas,1 and Kestutis Malakauskas1,2 1Department of Pulmonology, Lithuanian University of Health Sciences, Kaunas, LT-50161, Lithuania 2Laboratory of Pulmonology, Department of Pulmonology, Lithuanian University of Health Sciences, Kaunas, LT-50161, Lithuania Correspondence should be addressed to Virginija Kalinauskaite-Zukauske; [email protected] Received 4 July 2019; Revised 11 October 2019; Accepted 9 November 2019; Published 1 December 2019 Guest Editor: Paraskevi A. Katsaounou Copyright © 2019 Virginija Kalinauskaite-Zukauske et al. -is is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. -e bronchial epithelium has continuous contact with environmental agents initiating and maintaining airway type 2 in- flammation in asthma. However, there is a lack of data on whether reduced airway eosinophilic inflammation can affect the production of epithelial-derived mediators, such as interleukin-25 (IL-25) and thymic stromal lymphopoietin (TSLP). -e aim of this study was to investigate the changes in serum levels of IL-25 and TSLP after a single dose of mepolizumab, a humanized monoclonal antibody to interleukin-5 (IL-5), in patients with severe non-allergic eosinophilic asthma (SNEA). We examined 9 SNEA patients before and four weeks after administration of 100 mg mepolizumab subcutaneously. -e fractional exhaled nitric oxide (FeNO) level was analysed using an electrochemical assay (NIOX VERO , Circassia, UK). Serum IL-25 and TSLP levels were measured by ELISA. Four weeks after the single dose of mepolizumab, blood® eosinophil count significantly decreased from 9 9 0.55 ± 0.20 ×10 /l to 0.14 ± 0.04 ×10 /l (p � 0:01) and FEV1 increased from 2.1 ± 0.5 l (65.4 ± 8.8% of predicted) to 2.6 ± 0.4 l (76.4 ± 9.1% of predicted) (p � 0:04), while FeNO level has not changed (32.3 ± 8.4 vs 42.9 ± 12.6 ppb). Serum IL-25 level sig- nificantly decreased from 48.0 ± 17.2 pg/mL to 34.8 ± 17.1 pg/mL (p � 0:02) with same tendency in TSLP level: from 359.8 ± 71.3 pg/mL to 275.6 ± 47.8 pg/mL (p � 0:02). It has also been noticed a significant relation between changes in the blood eosinophil count and serum IL-25 level (r = 0.81, p � 0:008), as well as between changes in serum IL-25 and TSLP levels (r = 0.93, p � 0:004) after a single dose of mepolizumab. -us, anti-IL-5 treatment with mepolizumab might diminish the production of bronchial epithelial-derived cytokines IL-25 and TSLP in patients with SNEA which is potentially related to reduced eosinophilic inflammation. -is trial is registered in ClinicalTrial.gov with identifier NCT03388359. 1. Introduction steroids [1, 2]. All this leads to a significant loss of life quality and labour productivity, increased mortality risk [3, 4]. -e Asthma is a common, life-lasting airway disease, associated cost of severe asthma treatment represents a significant part with a high social and economic burden. About 3–8% of all of the total cost of all asthma cases [3, 4]. -erefore, severe asthma patients have severe asthma, suffering from frequent asthma is the most research-intensive areas of respiratory symptoms and recurrent exacerbations despite the com- medicine in the last decade. bined treatment with high-dose of inhaled steroids and long- Eosinophilic airway inflammation has a key position in acting bronchodilators, often supplemented with oral the pathogenesis of severe eosinophilic asthma [5, 6]. After 2 Canadian Respiratory Journal activation, eosinophils synthesize a row of cytokines, che- ≥0.30 ×109/l blood eosinophil count in the 12-month period mokines, growth factors, and other eosinophil-derived before the screening denying other possible common causes proinflammatory products, and all of them contribute to the of eosinophilia (e.g., helminths, allergies); no other reasons airway inflammation in asthma, including airway epithelial that could lead to poor control of asthma symptoms; cell damage, airway dysfunction, and remodeling [7–9]. In- documented at least 12-month treatment of high doses of terleukin- 5 (IL-5) is one of the main promoters of eosinophil inhaled steroids combined with long-acting beta-ago- production, maturation, and release from bone marrow. It nist ± long-acting antimuscarinic agent ± episodic use of oral also activates eosinophils and prolongs their survival in the steroids prior to inclusion in the study; and in the 12 months circulation, as well as providing an essential signal for their before the screening visit ≥2 exacerbations of asthma that migration into tissue [10]. However, the initial immune re- required treatment with systemic steroids. sponse to inhaled air pollutants or other external triggers -e study was open for non-smokers only. occurs already in the bronchial epithelium [11–16]. -erefore, Exclusion criteria included asthma exacerbation, active dysfunction of epithelial cells is becoming an increasingly airway infection, and use of oral steroids 1 month prior to the important part of the pathogenesis of asthma. -ere are data study; clinically significant permanent allergy symptoms; and that cytokines interleukin- 25 (IL-25) and thymic stromal treatment with targeted (biological) therapy (e.g., omalizu- lymphopoietin (TSLP) are some of the major airway type 2 mab, mepolizumab, and benralizumab) at the screening visit. inflammation regulators derived from the bronchial epithe- lium [14, 17]. -ese cytokines have been described as epi- 2.2. Study Design. At the screening visit, the inclusion/ex- thelial-derived alarmins that activate and potentiate the inner clusion criteria were assessed, and informed consent was immune cascade, including airway eosinophilic in- obtained. During the first study visit, FeNO level was flammation, in the presence of actual damage [14, 16–18]. analysed, FEV was measured, and blood samples were It is unknown whether anti-IL-5-directed treatment 1 collected for evaluation of blood eosinophil count and ep- affects only eosinophilic inflammation or also other medi- ithelial-derived mediators concentrations. After all the ators which are involved in airway type 2 inflammation. In procedures, mepolizumab 100 mg was injected sub- this study, we aimed at assessing the changes in serum levels cutaneously. -e second study visit was scheduled for 4 of epithelial-derived mediators as IL-25 and TSLP on weeks. -en, FeNO and FEV were re-evaluated, and blood mepolizumab, a humanized monoclonal antibody to IL-5, 1 samples were re-taken. Only patients without asthma ex- treatment in patients with severe non-allergic eosinophilic acerbation during this 4 weeks period were re-evaluated. -e asthma (SNEA). We designed to use a single dose of study design scheme is presented in Figure 1. mepolizumab to avoid asthma exacerbations that could influence the intensity of type 2 inflammation, whereas positive drug effect on reduction in blood eosinophils and 2.3. Pulmonary Function Testing. -e lung function was lung function improvement is observed already after the first evaluated for all study subjects by measuring baseline FEV1 dose [19, 20]. using an ultrasonic spirometer (Ganshorn Medizin Elec- tronic, Germany) and compared with the predicted value 2. Materials and Methods matched for age, body height, and sex according to the standard methodology. FEV1 was measured three times and 2.1. Subjects. -e study was conducted with the permission recorded only the highest of three reproducible of the Regional Biomedical Research Ethics Committee of measurements. the Lithuanian University of Health Sciences (BE-2-13) and after signing the informed consent forms. -e study was 2.4. FeNO Measurement. All study subjects underwent registered in the U.S. National Institutes of Health trial FeNO analysis with an online method using a single-breath registry ClinicalTrials.gov with identifier NCT03388359. exhalation and an electrochemical assay (NIOX VERO , -e study included patients with adult-onset SNEA (the Circassia, UK), according to ATS-ERS guidelines [21]. Pa-® inclusion criteria listed below). Non-allergic asthma was tients made an inspiration of eNO-free air via a mouthpiece chosen to eliminate allergens as an uncontrollable factor immediately followed by full exhalation at a constant rate which damage the epithelium and may significantly alter (50 mL/sec) for at least 10 seconds. -e mean of three cytokine levels and affect airway type 2 inflammation activity. readings at the end of the expiration (plateau phase) was -e participants were men and women between the ages taken as the representative value for each measurement. of 18 and 65 years, recruited from the Department of Pulmonology at Hospital of the Lithuanian University of Health Sciences Kaunas Clinics. 2.5. Skin Prick Test. All study subjects were screened for Inclusion criteria were as follows: asthma diagnosis for at allergies by the skin prick test at least 6 months prior to least 12 months; non-allergic phenotype, confirmed by the enrollment. Standardized allergen extracts (Stallergenes absence of allergy-specific symptoms (watery runny nose or S.A.,
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