Periostin as a marker of eosinophilic inflammation in patients with asthma and chronic obstructive pulmonary disease

Abstract

BACKGROUND: Asthma and chronic obstructive pulmonary disease are common chronic respiratory diseases. Given their heterogeneity, the study of periostin is a relevant area for establishing the endotypes of airway inflammation and determining further therapy tactics.

AIM: To evaluate periostin levels and determine its significance as a marker of eosinophilic inflammation in patients with asthma and chronic obstructive pulmonary disease.

MATERIALS AND METHODS: The study included 59 patients with asthma and 33 patients with chronic obstructive pulmonary disease. The control group consisted of 37 apparently healthy people, comparable in age and sex, without allergic and bronchial obstructive diseases in anamnesis. The anamnesis data, the number of peripheral blood eosinophils and induced sputum, indices of external respiratory function were evaluated. Levels of specific immunoglobulin E to allergens, periostin level were determined in blood serum by immunoenzyme method. The obtained data were processed using STATISTICA 13 and SPSS Statistic 27 software systems.

RESULTS: The maximum serum periostin concentration 22.5 (17–38) ng/ml was recorded in the patients with asthma, which was significantly higher than in the chronic obstructive pulmonary disease group [16 (12–21) ng/ml; p = 0.006] and control group [20.1 (14.6–24.8) ng/ml; p = 0.044]. The level of periostin in induced sputum in the patients with asthma was significantly higher than in the chronic obstructive pulmonary disease group — 0.05 (0.03–0.6) ng/ml vs 0.03 (0.02–0.04) ng/ml (p = 0.008). The study revealed the correlation between serum periostin level and eosinophil level (r = 0.406; p < 0.05) and with forced expiratory volume in the first second after bronchodilator test (r = 0.366; p < 0.05) as well as with forced expiratory volume in the first second divided by forced vital capacity after bronchodilator test (r = 0.572; p < 0.05).

CONCLUSIONS: Periostin is a promising marker of eosinophilic inflammation in patients with asthma, which can be considered as an indicator of fixed bronchial obstruction and a molecule linking T2-inflammation and airway remodelling. In a group of chronic obstructive pulmonary disease patients, the use of periostin for diagnostic and prognostic purposes requires further investigation and larger studies.

Keywords

periostin / asthma / chronic obstructive pulmonary disease

References

[1] Avdeev SN, Emelyanov AV, Aisanov ZR, et al. Problems and opportunities to improve diagnosis of asthma and chronic obstructive pulmonary disease in Russia: resolution of advisory board. Terapevticheskii Arkhiv. 2022;94(4):524–529. EDN: ZSVKEK doi: 10.26442/00403660.2022.04.201487

[2] Авдеев С.Н., Емельянов А.В., Айсанов З.Р., и др. Проблемы и возможности для повышения диагностики бронхиальной астмы и хронической обструктивной болезни легких в России: заключение совета экспертов // Терапевтический архив. 2022. Т. 94, № 4. С. 524–529. EDN: ZSVKEK doi: 10.26442/00403660.2022.04.201487

[3] Bystritskaya EV, Bilichenko TN. The morbidity, disability, and mortality associated with respiratory diseases in the Russian Federation (2015–2019). Pulmonologiya. 2021;31(5):551–561. EDN: KXDQEV doi: 10.18093/0869-0189-2021-31-5-551-561

[4] Быстрицкая Е.В., Биличенко Т.Н. Заболеваемость, инвалидность и смертность от болезней органов дыхания в Российской Федерации (2015–2019) // Пульмонология. 2021. Т. 31, № 5. С. 551–561. EDN: KXDQEV doi: 10.18093/0869-0189-2021-31-5-551-561

[5] Adeloye D, Chua S, Lee C, et al. Global and regional estimates of COPD prevalence: Systematic review and meta-analysis. J Glob Health. 2015;5(2):020415. doi: 10.7189/jogh.05-020415

[6] Adeloye D., Chua S., Lee C., et al. Global and regional estimates of COPD prevalence: Systematic review and meta-analysis // J Glob Health. 2015. Vol. 5, N. 2. P. 020415. doi: 10.7189/jogh.05-020415

[7] GBD 2013 Mortality and Causes of Death Collaborators. Global, regional, and national age-sex specific all-cause and cause-specific mortality for 240 causes of death, 1990–2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet. 2015;385(9963):117–171. doi: 10.1016/S0140-6736(14)61682-2

[8] GBD 2013 Mortality and Causes of Death Collaborators. Global, regional, and national age-sex specific all-cause and cause-specific mortality for 240 causes of death, 1990–2013: a systematic analysis for the Global Burden of Disease Study 2013 // Lancet. 2015. Vol. 385, N. 9963. P. 117–171. doi: 10.1016/S0140-6736(14)61682-2

[9] Lopez A, Shibuya K, Rao C, et al. Obstructive pulmonary disease: current burden and future projections. Eur Respir J. 2006;27(2):397–412. doi: 10.1183/09031936.06.00025805

[10] Lopez A., Shibuya K., Rao C., et al. Obstructive pulmonary disease: current burden and future projections // Eur Respir J. 2006. Vol. 27, N. 2. P. 397–412. doi: 10.1183/09031936.06.00025805

[11] WHO. Projections of mortality and causes of death, 2015 and 2030 [Internet]. Available from: https://bigdataanalyticsnews.com/projections-of-mortality-and-causes-of-death-2015-and-2030/. Accessed: 11 Jan 2022.

[12] WHO. Projections of mortality and causes of death, 2015 and 2030. Режим доступа: https://bigdataanalyticsnews.com/projections-of-mortality-and-causes-of-death-2015-and-2030/. Дата обращения: 11.01.2022.

[13] Avdeev SN, Nenasheva NM, Zhudenkov KV, et al. Prevalence, morbidity, phenotypes and other characteristics of severe bronchial asthma in Russian Federation. Pulmonologiya. 2018;28(3):341–358. EDN: XWCRRZ doi: 10.18093/0869-0189-2018-28-3-341-358

[14] Авдеев С.Н., Ненашева Н.М., Жуденков К.В., и др. Распространенность, заболеваемость, фенотипы и другие характеристики тяжелой бронхиальной астмы в Российской Федерации // Пульмонология. 2018. Т. 28, № 3. С. 341–358. EDN: XWCRRZ doi: 10.18093/0869-0189-2018-28-3-341-358

[15] Clinical recommendations “Bronchial asthma” 2021 [Internet]. Available from: https://cr.minzdrav.gov.ru/recomend/359_2. Accessed: 4 Feb 2022. (In Russ.)

[16] Клинические рекомендации «Бронхиальная астма» 2021 г. [Электронный ресурс]. Режим доступа: https://cr.minzdrav.gov.ru/recomend/359_2. Дата обращения: 04.02.2022.

[17] Ono J, Takai M, Kamei A, et al. Pathological roles and clinical usefulness of periostin in type 2 inflammation and pulmonary fibrosis. Biomolecules. 2021;11(8):1084. doi: 10.3390/biom11081084

[18] Ono J., Takai M., Kamei A., et al. Pathological roles and clinical usefulness of periostin in type 2 inflammation and pulmonary fibrosis // Biomolecules. 2021. Vol. 11, N. 8. P. 1084. doi: 10.3390/biom11081084

[19] Okamoto M, Izuhara K, Ohta S, et al. Ability of periostin as a new biomarker of idiopathic pulmonary fibrosis. Adv Exp Med Bio. 2019;1132:79–87. doi: 10.1007/978-981-13-6657-4_9

[20] Okamoto M., Izuhara K., Ohta S., et al. Ability of periostin as a new biomarker of idiopathic pulmonary fibrosis // Adv Exp Med Bio. 2019. Vol. 1132. P. 79–87. doi: 10.1007/978-981-13-6657-4_9

[21] Yoshihara T, Nanri Y, Nunomura S, et al. Periostin plays a critical role in the cell cycle in lung fibroblasts. Respir Res. 2020;21(1):38–50. doi: 10.1186/s12931-020-1299-0

[22] Yoshihara T., Nanri Y., Nunomura S., et al. Periostin plays a critical role in the cell cycle in lung fibroblasts // Respir Res. 2020. Vol. 21, N. 1. P. 38–50. doi: 10.1186/s12931-020-1299-0

[23] Bhatt S, Agusti A, Bafadhel M, et al. Phenotypes, etiotypes, and endotypes of exacerbations of chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2023;208(10):1026–1041. doi: 10.1164/rccm.202209-1748SO.

[24] Bhatt S., Agusti A., Bafadhel M., et al. Phenotypes, etiotypes, and endotypes of exacerbations of chronic obstructive pulmonary disease // Am J Respir Crit Care Med. 2023. Vol. 208, N. 10. P. 1026–1041. doi: 10.1164/rccm.202209-1748SO

[25] The Global Strategy for Asthma Management and Prevention, Global Initiative for Asthma (GINA) 2023 [Internet]. Available from: https://www.kineed.org/wp-content/uploads/2023/06/GINA-2023-Full-Report-2023-WMS.pdf. Accessed: 19 May 2023.

[26] The Global Strategy for Asthma Management and Prevention, Global Initiative for Asthma (GINA) 2023 [Электронный ресурс]. Режим доступа: https://www.kineed.org/wp-content/uploads/2023/06/GINA-2023-Full-Report-2023-WMS.pdf. Дата обращения: 19.05.2023.

[27] The Global Initiative for Chronic Obstructive Lung Disease (GOLD) 2023 [Internet]. Available from: https://goldcopd.org/2023-gold-report-2/ Accessed: 16 Sep 2023.

[28] The Global Initiative for Chronic Obstructive Lung Disease (GOLD) 2023 [Электронный ресурс]. Режим доступа: https://goldcopd.org/2023-gold-report-2/. Дата обращения: 16.09.2023.

[29] Clinical recommendations “Chronic obstructive lung disease” 2021 [Internet]. Available from: https://cr.minzdrav.gov.ru/recomend/603_2. Accessed: 23 June 2022. (In Russ.)

[30] Клинические рекомендации «Хроническая обструктивная болезнь легких» 2021 г. [Электронный ресурс]. Режим доступа: https://cr.minzdrav.gov.ru/recomend/603_2. Дата обращения: 23.06.2022.

[31] Masalskiy SS, Kalmykova АS, Ukhanova ОP. Comprehensive assessment of serum periostin – a new marker for uncontrolled asthma in children Russian Journal of Allergy. 2018;15(1):55–57. EDN: YNKNGX

[32] Масальский С.С., Калмыкова А.С., Уханова О.П. Комплексная оценка сывороточного периостина – нового маркера при неконтролируемой БА у детей // Российский аллергологический журнал. 2018. Т. 15, № 1. С. 55–57. EDN: YNKNGX

[33] Izuhara K, Nunomura S, Nanri Y, et al. Periostin in inflammation and allergy. Cell Mol Life Sci. 2017;74(23):4293–4303. doi: 10.1007/s00018-017-2648-0

[34] Izuhara K., Nunomura S., Nanri Y., et al. Periostin in inflammation and allergy // Cell Mol Life Sci. 2017. Vol. 74, No. 23. P. 4293–4303. doi: 10.1007/s00018-017-2648-0

[35] Takayama G, Arima K, Kanaji T, et al. Periostin: a novel component of subepithelial fibrosis of bronchial asthma downstream of IL-4 and IL-13 signals. J Allergy Clin Immunol. 2006;118(1):98–104. doi: 10.1016/j.jaci.2006.02.046

[36] Takayama G., Arima K., Kanaji T., et al. Periostin: a novel component of subepithelial fibrosis of bronchial asthma downstream of IL-4 and IL-13 signals // J Allergy Clin Immunol. 2006. Vol. 118, N. 1. P. 98–104. doi: 10.1016/j.jaci.2006.02.046

[37] Shakhova NV. Periostin as a biomarker of bronchial asthma. Current Pediatrics. 2019;18(5):339–345. EDN: ZIXBFC doi: 10.15690/vsp.v18i5.2056

[38] Шахова Н.В. Периостин — биомаркер бронхиальной астмы // Вопросы современной педиатрии. 2019. Т. 18, № 5. С. 339–345. EDN: ZIXBFC doi: 10.15690/vsp.v18i5.2056

[39] Ono J, Takai M, Kamei A, et al. Periostin forms a functional complex with IgA in human serum. Allergol Int. 2020;69(1):111–120. doi: 10.1016/j.alit.2019.05.014

[40] Ono J., Takai M., Kamei A., et al. Periostin forms a functional complex with IgA in human serum // Allergol Int. 2020. Vol. 69, N. 1. P. 111–120. doi: 10.1016/j.alit.2019.05.014

[41] Scheerens H, Arron JR, Zheng Y, et al. The effects of lebrikizumab in patients with mild asthma following whole lung allergen challenge. Clin Exp Allergy. 2014;4(1):38–46. doi: 10.1111/cea.12220

[42] Scheerens H., Arron J.R., Zheng Y., et al. The effects of lebrikizumab in patients with mild asthma following whole lung allergen challenge // Clin Exp Allergy. 2014. Vol. 4, N. 1. P. 38–46. doi: 10.1111/cea.12220

[43] Naik PK, Bozyk PD, Bentley JK, et al. Periostin promotes fibrosis and predicts progression in patients with idiopathic pulmonary fibrosis. Am J Physiol Lung Cell Mol Physiol. 2012;303(12):1046–1056. doi: 10.1152/ajplung.00139.2012

[44] Naik P.K., Bozyk P.D., Bentley J.K., et al. Periostin promotes fibrosis and predicts progression in patients with idiopathic pulmonary fibrosis // Am J Physiol Lung Cell Mol Physiol. 2012. Vol. 303, N. 12. P. 1046–1056. doi: 10.1152/ajplung.00139.2012

[45] Jia G, Erickson RW, Choy DF, et al. Periostin is a systemic biomarker of eosinophilic airway inflammation in asthmatic patients. J Allergy Clin Immunol. 2012;130(3):647–654.e10. doi: 10.1016/j.jaci.2012.06.025

[46] Jia G., Erickson R.W., Choy D.F., et al. Periostin is a systemic biomarker of eosinophilic airway inflammation in asthmatic patients // J Allergy Clin Immunol. 2012. Vol. 130, N. 3. P. 647–654.e10. doi: 10.1016/j.jaci.2012.06.025

[47] Kato G, Takahashi K, Izuhara K, et al. Markers that can reflect asthmatic activity before and after reduction of inhaled corticosteroids: a pilot study. Biomark Insights. 2013;8:97–105. doi: 10.4137/BMI.S12537

[48] Kato G., Takahashi K., Izuhara K., et al. Markers that can reflect asthmatic activity before and after reduction of inhaled corticosteroids: a pilot study // Biomark Insights. 2013. Vol. 8. P. 97–105. doi: 10.4137/BMI.S12537

[49] Casale TB. Biologics and biomarkers for asthma, urticaria, and nasal polyposis. J Allergy Clin Immunol. 2017;139(5):1411–1421. doi: 10.1016/j.jaci.2017.03.006

[50] Casale T.B. Biologics and biomarkers for asthma, urticaria, and nasal polyposis // J Allergy Clin Immunol. 2017. Vol. 139, N. 5. P. 1411–1421. doi: 10.1016/j.jaci.2017.03.006

[51] Akar-Ghibril N, Casale T, Custovic A, et al. Allergic endotypes and phenotypes of asthma. J Allergy Clin Immunol Pract. 2020;8(2):429–440. doi: 10.1016/j.jaip.2019.11.008

[52] Akar-Ghibril N., Casale T., Custovic A., et al. Allergic endotypes and phenotypes of asthma // J Allergy Clin Immunol Pract. 2020. Vol. 8, N. 2. P. 429–440. doi: 10.1016/j.jaip.2019.11.008

[53] Izuhara K, Nunomura S, Nanri Y, et al. Periostin: An emerging biomarker for allergic diseases. Allergy. 2019;74(11):2116–2128. doi: 10.1111/all.13814

[54] Izuhara K., Nunomura S., Nanri Y., et al. Periostin: An emerging biomarker for allergic diseases // Allergy. 2019. Vol. 74, N. 11. P. 2116–2128. doi: 10.1111/all.13814

[55] Wu G, Meng X, Zheng P, et al. Elevated serum levels of periostin in patients with allergic bronchopulmonary aspergillosis. Mycoses. 2019;62(9):780–789. doi: 10.1111/myc.12957

[56] Wu G., Meng X., Zheng P., et al. Elevated serum levels of periostin in patients with allergic bronchopulmonary aspergillosis // Mycoses. 2019. Vol. 62, N. 9. P. 780–789. doi: 10.1111/myc.12957

[57] Kozlova Y, Frolova E, Uchevatkina A, et al. Diagnostic markers of allergic bronchopulmonary aspergillosis in patients with severe asthma. Mycoses. 2020;63(6):596–603. doi: 10.1111/myc.13083

[58] Kozlova Y., Frolova E., Uchevatkina A., et al. Diagnostic markers of allergic bronchopulmonary aspergillosis in patients with severe asthma // Mycoses. 2020. Vol. 63, N. 6. P. 596–603. doi: 10.1111/myc.13083

[59] Nejman-Gryz P, Górska K, Krenke K, et al. Periostin concentration in exhaled breath condensate in children with mild asthma. J Asthma. 2021;58(1):60–68. doi: 10.1080/02770903.2019.1659312

[60] Nejman-Gryz P., Górska K., Krenke K., et al. Periostin concentration in exhaled breath condensate in children with mild asthma // J Asthma. 2021. Vol. 58, N. 1. P. 60–68. doi: 10.1080/02770903.2019.1659312

[61] O’Connell P, Gaston B, Bonfield T, et al. Periostin levels in children without respiratory disease. Pediatr Pulmonol. 2019;54(2):200–204. doi: 10.1002/ppul.24206

[62] O’Connell P., Gaston B., Bonfield T., et al. Periostin levels in children without respiratory disease // Pediatr Pulmonol. 2019. Vol. 54, N. 2. P. 200–204. doi: 10.1002/ppul.24206

[63] Baranov DZ, Trofimov VI, Lapin SV, et al. Evaluation of periostin in case of bronchoostructive diseases. Therapy. 2021;7(8)(50):22–29. EDN: QEOLUD doi: 10.18565/therapy.2021.8.22-29

[64] Баранов Д.З., Трофимов В.И., Лапин С.В., и др. Определение периостина при бронхообструктивных заболеваниях // Терапия. 2021. Т. 7, № 8(50). С. 22–29. EDN: QEOLUD doi: 10.18565/therapy.2021.8.22-29

[65] Masalskiy SS, Kalmykova AS, Ukhanova OP, et al. Use serum periostin as marker of worsening pediatric allergic asthma. Allergology and Immunology in Paediatrics. 2018;4(55):37–48. EDN: YZXRAD doi: 10.24411/2500-1175-2018-00021

[66] Масальский С.С., Калмыкова А.С., Уханова О.П., и др. Использование сывороточного периостина в качестве маркера обострений астмы у детей // Аллергология и иммунология в педиатрии. 2018. Т. 4, № 55. С. 37–48. EDN: YZXRAD doi: 10.24411/2500-1175-2018-00021

[67] Scichilone N, Crimi C, Benfante A, et al. Higher serum levels of periostin and the risk of exacerbations in moderate asthmatics. Asthma Res Pract. 2016;2(1):1. doi: 10.1186/s40733-015-0019-x

[68] Scichilone N., Crimi C., Benfante A., et al. Higher serum levels of periostin and the risk of exacerbations in moderate asthmatics // Asthma Res Pract. 2016. Vol. 2, N. 1. P. 1. doi: 10.1186/s40733-015-0019-x

[69] Shirai T, Hirai K, Gon Y, et al. Combined assessment of serum periostin and YKL-40 May identify asthma-COPD overlap. J Allergy Clin Immunol Pract. 2019;7(1):134–145.e1. doi: 10.1016/j.jaip.2018.06.015

[70] Shirai T., Hirai K., Gon Y., et al. Combined assessment of serum periostin and YKL-40 may identify asthma-COPD overlap // J Allergy Clin Immunol Pract. 2019. Vol. 7, N. 1. P. 134–145.e1. doi: 10.1016/j.jaip.2018.06.015

[71] Liu Y, Zhang S, Chen R, et al. Meta-analysis of randomized controlled trials for the efficacy and safety of anti-interleukin-13 therapy with lebrikizumab in patients with uncontrolled asthma. Allergy Asthma Proc. 2018;39(5):332–337. doi: 10.2500/aap.2018.39.4149

[72] Liu Y., Zhang S., Chen R., et al. Meta-analysis of randomized controlled trials for the efficacy and safety of anti-interleukin-13 therapy with lebrikizumab in patients with uncontrolled asthma // Allergy Asthma Proc. 2018. Vol. 39, N. 5. P. 332–337. doi: 10.2500/aap.2018.39.4149

[73] Gottlow M, Svensson DJ, Lipkovich I, et al. Application of structured statistical analyses to identify a biomarker predictive of enhanced tralokinumab efficacy in phase III clinical trials for severe, uncontrolled asthma. BMC Pulm Med. 2019;19(1):129. doi: 10.1186/s12890-019-0889-4

[74] Gottlow M., Svensson D.J., Lipkovich I., et al. Application of structured statistical analyses to identify a biomarker predictive of enhanced tralokinumab efficacy in phase III clinical trials for severe, uncontrolled asthma // BMC Pulm Med. 2019. Vol. 19, N. 1. P. 129. doi: 10.1186/s12890-019-0889-4

[75] Abramson MJ, Schattner RL, Sulaiman ND, et al. Accuracy of asthma and COPD diagnosis in Australian general practice: a mixed methods study. Prim Care Respir J. 2012;21(2):167–173. doi: 10.4104/pcrj.2011.00103

[76] Abramson M.J., Schattner R.L., Sulaiman N.D., et al. Accuracy of asthma and COPD diagnosis in Australian general practice: a mixed methods study // Prim Care Respir J. 2012. Vol. 21, N. 2. P. 167–173. doi: 10.4104/pcrj.2011.00103

[77] Trofimov VI, Baranov DZ. Clinical and functional peculiarities at patients with bronchial asthma, chronic obstructive pulmonary disease and overlap of asthma-chronic obstructive pulmonary disease. Nefrologiya. 2020;24(4):80–86. EDN: HBKWSH doi: 10.36485/1561-6274-2020-24-4-80-86

[78] Трофимов В.И., Баранов Д.З. Клинические и функциональные особенности больных бронхиальной астмой, хронической обструктивной болезнью лёгких и сочетанием бронхиальной астмы и хронической обструктивной болезни лёгких // Нефрология. 2020. Т. 24, № 4. С. 80–86. EDN: HBKWSH doi: 10.36485/1561-6274-2020-24-4-80-86

[79] Mansur AH, Srivastava S, Sahal A. Disconnect of type 2 biomarkers in severe asthma; dominated by FeNO as a predictor of exacerbations and periostin as predictor of reduced lung function. Respir Med. 2018;143:31–38. doi: 10.1016/j.rmed.2018.08.005

[80] Mansur A.H., Srivastava S., Sahal A. Disconnect of type 2 biomarkers in severe asthma; dominated by FeNO as a predictor of exacerbations and periostin as predictor of reduced lung function // Respir Med. 2018. Vol. 143. P. 31–38. doi: 10.1016/j.rmed.2018.08.005

[81] Takahashi K, Meguro K, Kawashima H, et al. Serum periostin levels serve as a biomarker for both eosinophilic airway inflammation and fixed airflow limitation in well-controlled asthmatics. J Asthma. 2019;56(3):236–243. doi: 10.1080/02770903.2018.1455855

[82] Takahashi K., Meguro K., Kawashima H., et al. Serum periostin levels serve as a biomarker for both eosinophilic airway inflammation and fixed airflow limitation in well-controlled asthmatics // J Asthma. 2019. Vol. 56, N. 3. P. 236–243. doi: 10.1080/02770903.2018.1455855

[83] Matsumoto H. Roles of periostin in asthma. Adv Exp Med Biol. 2019;1132:145–159. doi: 10.1007/978-981-13-6657-4_15

[84] Matsumoto H. Roles of periostin in asthma // Adv Exp Med Biol. 2019. Vol. 1132. P. 145–159. doi: 10.1007/978-981-13-6657-4_15

[85] Johansson MW, Annis DS, Mosher DF. α(M)β(2) integrin-mediated adhesion and motility of IL-5-stimulated eosinophils on periostin. Am J Respir Cell Mol Biol. 2013;48(4):503–510. doi: 10.1165/rcmb.2012-0150OC

[86] Johansson M.W., Annis D.S., Mosher D.F. α(M)β(2) integrin-mediated adhesion and motility of IL-5-stimulated eosinophils on periostin // Am J Respir Cell Mol Biol. 2013. Vol. 48, N. 4. P. 503–510. doi: 10.1165/rcmb.2012-0150OC

[87] Nejman-Gryz P, Górska K, Paplińska-Goryca M, et al. Periostin and thymic stromal lymphopoietin – potential crosstalk in obstructive airway diseases. J Clin Med. 2020;9(11):3667. doi: 10.3390/jcm9113667

[88] Nejman-Gryz P., Górska K., Paplińska-Goryca M., et al. Periostin and thymic stromal lymphopoietin – potential crosstalk in obstructive airway diseases // J Clin Med. 2020. Vol. 9, N. 11. P. 3667. doi: 10.3390/jcm9113667

[89] Park HY, Lee H, Koh W-J, et al. Association of blood eosinophils and plasma periostin with FEV1 response after 3-month inhaled corticosteroid and long-acting beta2-agonist treatment in stable COPD patients. Int J Chron Obstruct Pulmol Dis. 2015;11:23–30. doi: 10.2147/COPD.S94797

[90] Park H.Y., Lee H., Koh W.-J., et al. Association of blood eosinophils and plasma periostin with FEV1 response after 3-month inhaled corticosteroid and long-acting beta2-agonist treatment in stable COPD patients // Int J Chron Obstruct Pulmol Dis. 2015. Vol. 11. P. 23–30. doi: 10.2147/COPD.S94797

[91] Carpaij OA, Muntinghe FOW, Wagenaar MB, et al. Serum periostin does not reflect type 2-driven inflammation in COPD. Respir Res. 2018;19(1):112. doi: 10.1186/s12931-018-0818-8

[92] Carpaij O.A., Muntinghe F.O.W., Wagenaar M.B., et al. Serum periostin does not reflect type 2-driven inflammation in COPD // Respir Res. 2018. Vol. 19, N. 1. P. 112. doi: 10.1186/s12931-018-0818-8

[93] Morra L, Rechsteiner M, Casagrande S, et al. Characterization of periostin isoform pattern in non-small cell lung cancer. Lung Cancer. 2012;76(2):183–190. doi: 10.1016/j.lungcan.2011.10.013

[94] Morra L., Rechsteiner M., Casagrande S., et al. Characterization of periostin isoform pattern in non-small cell lung cancer // Lung Cancer. 2012. Vol. 76, N. 2. P. 183–190. doi: 10.1016/j.lungcan.2011.10.013

RIGHTS & PERMISSIONS

Eco-Vector