The role of fine suspended particles of atmospheric air in the formation of eosinophilic inflammation in T2-endotype of asthma

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Abstract

BACKGROUND: Allergens induce eosinophilic inflammation in the T2 endotype of asthma. However, much less is known about the role of non-specific factors (suspended particles in the atmospheric air-PM).

AIMS: To define eosinophilic inflammation on the basis of several biomarkers in the T2 endotype of asthma exposed to PM.

MATERIALS AND METHODS: We studied 150 patients with asthma, and 61 patients with T2 endotype of asthma (ages 18–65 years) were enrolled. Group 1 included 34 patients with allergic asthma, and group 2 included 27 patients with non-allergic asthma. Moreover, 30 healthy matched controls without asthma and other allergic diseases were enrolled in the study. Clinical examination and allergy testing were performed. Additionally, serum levels of IL-33, IL-25, IL-4, IL-5, IL-13, DPP4 (multiplex assay), and periostin (ELISA) were evaluated. The analyses of the average annual concentrations (Avr) and the maximal annual concentrations (MaxAvr) of PM2.5 and PM10 in Kazan were conducted using the database of the Center for Hygiene and Epidemiology in the Republic of Tatarstan, being averaged over the period from 2014 to 2020 years in monitoring points at residential areas. Statistical analyses were performed using R version 4.0.5. The study was funded by RFBR (Project no. 19-05-50094).

RESULTS: We detected increased blood eosinophil count and IL-5 levels in patients with asthma. High levels of total IgE (p=0.0001) that correlated with IL-4 levels were observed only in patients with allergic asthma (rS=0.38; p=0.045). Moreover, elevated IL-25 levels were found in patients with allergic asthma (p=0.009). No significant differences in IL-13 levels in patient with asthma were found. The regression analysis revealed that the PM2.5Avr increase by 1 mcg/m3 increases IL-33 and IL-25 levels, but the PM10Avr increase raises the IL-25 levels only in patients with non-allergic asthma. No significant increase in IL-25 and IL-33 levels under exposure to PM2.5Avr and PM 10Avr was detected in patients with allergic asthma.

CONCLUSIONS: The results of this study indicate the pivotal role of fine suspended particles in the development and maintenance of eosinophilic inflammation in patients with non-allergic asthma.

About the authors

Olesya V. Skorokhodkina

Kazan State Medical University

Email: olesya-27@rambler.ru
ORCID iD: 0000-0001-5793-5753
SPIN-code: 8649-6138

MD, Dr. Sci. (Med.), Professor

Russian Federation, Kazan

Milyausha R. Khakimova

Kazan State Medical University

Author for correspondence.
Email: mileushe7@gmail.com
ORCID iD: 0000-0002-3533-2596
SPIN-code: 1875-3934
Russian Federation, Kazan

Gyuzel A. Timerbulatova

Kazan State Medical University; Hygienic and Epidemiological Center in Republic of Tatarstan (Tatarstan)

Email: ragura@mail.ru
ORCID iD: 0000-0002-2479-2474
SPIN-code: 2402-8878
Russian Federation, Kazan; Kazan

Olga A. Bareycheva

Republican Clinical Hospital of the Republic of Tatarstan

Email: olga-alex21@mail.ru
ORCID iD: 0000-0002-1419-8746
SPIN-code: 8728-8883
Russian Federation, Kazan

Larisa Е. Saleeva

Republican Clinical Hospital of the Republic of Tatarstan

Email: saleeva.le@yandex.ru
ORCID iD: 0000-0003-3143-0436
SPIN-code: 7349-0840
Russian Federation, Kazan

Rezeda G. Sharipova

Republican Clinical Hospital of the Republic of Tatarstan

Email: rezeda-kazan@mail.ru
ORCID iD: 0000-0001-8273-5446
Russian Federation, Kazan

Anastasia V. Ablayeva

Kazan State Medical University

Email: wail2008@yandex.ru
ORCID iD: 0000-0001-5597-0694
SPIN-code: 3901-8348
Russian Federation, Kazan

Liliya M. Fatkhutdinova

Kazan State Medical University

Email: liliya.fatkhutdinova@gmail.com
ORCID iD: 0000-0001-9506-563X
SPIN-code: 9605-8332

MD, Dr. Sci. (Med.), Professor

Russian Federation, Kazan

References

  1. Global Initiative for Asthma [Internet]. Global Strategy for Asthma Management and Prevention. 2022. Available from: www. ginasthma.org. Accessed: 15.10.2022.
  2. Wenzel SE, Schwartz LB, Langmack EL, et al. Evidence that severe asthma can be divided pathologically into two inflammatory subtypes with distinct physiologic and clinical characteristics. Am J Respir Crit Care Med. 1999;160(3):1001–1008. doi: 10.1164/ajrccm.160.3.9812110
  3. Kuruvilla ME, Lee FE, Lee GB. Understanding asthma phenotypes, endotypes, and mechanisms of disease. Clin Rev Allergy Immunol. 2019;56(2):219–233. doi: 10.1007/s12016-018-8712-1
  4. Simpson JL, Scott R, Boyle MJ, Gibson PG. Inflammatory subtypes in asthma: Assessment and identification using induced sputum. Respirology. 2006;11(1):54–61. doi: 10.1111/j.1440-1843.2006.00784.x
  5. 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. (In Russ). doi: 10.18093/0869-0189-2018-28-3-341-358
  6. Nenasheva NM. Т2-high and T2-low bronchial asthma, endotype characteristics and biomarkers. Pulmonologiya. 2019;29(2):216–228. (In Russ). doi: 10.18093/0869-0189-2019-29-2-216-228
  7. Diamant Z, Vijverberg S, Alving K, et al. Toward clinically applicable biomarkers for asthma: An EAACI position paper. Allergy. 2019;74(10):1835–1851. doi: 10.1111/all.13806
  8. Hong H, Liao S, Chen F, et al. Role of IL-25, IL-33, and TSLP in triggering united airway diseases toward type 2 inflammation. Allergy. 2020;75(11):2794–2804. doi: 10.1111/all.14526
  9. Akdis CA, Arkwright PD, Brüggen MC, et al. Type 2 immunity in the skin and lungs. Allergy. 2020;75(7):1582–1605. doi: 10.1111/all.14318
  10. Arias-Pérez RD, Taborda NA, Gómez DM, et al. Inflammatory effects of particulate matter air pollution. Environ Sci Pollut Res Int. 2020;27(34):42390–42404. doi: 10.1007/s11356-020-10574-w
  11. Baldacci S, Maio S, Cerrai S, et al. Allergy and asthma: Effects of the exposure to particulate matter and biological allergens. Respir Med. 2015;109(9):1089–1104. doi: 10.1016/j.rmed.2015.05.017
  12. Revich BA. Fine suspended particulates in ambient air and their health effects in megalopolises. Problems of ecological monitoring and ecosystem modelling. 2018;29(3):53–78. (In Russ). doi: 10.21513/0207-2564-2018-3-53-78
  13. Lakey PS, Berkemeier T, Tong H, et al. Chemical exposure-response relationship between air pollutants and reactive oxygen species in the human respiratory tract. Sci Rep. 2016;6:32916. doi: 10.1038/srep32916
  14. Pfeffer PE, Mudway IS, Grigg J. Air pollution and asthma: Mechanisms of harm and considerations for clinical interventions. Chest. 2021;159(4):1346–1355. doi: 10.1016/j.chest.2020.10.053
  15. Anenberg SC, Haines S, Wang E, et al. Synergistic health effects of air pollution, temperature, and pollen exposure: A systematic review of epidemiological evidence. Environ Health. 2020;19(1):130. doi: 10.1186/s12940-020-00681-z
  16. Klinicheskie rekomendacii. Bronhial’naya astma. 2021. (In Russ). Available from: https://raaci.ru/dat/pdf/BA.pdf. Accessed: 20.10.2022.
  17. Ouédraogo AM, Crighton EJ, Sawada M, et al. Exploration of the spatial patterns and determinants of asthma prevalence and health services use in Ontario using a bayesian approach. PLoS ONE. 2018;13(12):e0208205. doi: 10.1371/journal.pone.0208205
  18. Fatkhutdinova LM, Tafeeva EA, Timerbulatova GA, Zalyalov RR. Health risks of air pollution with fine particulate matter. Kazan Medical Journal. 2021;102(6):862–876. doi: 10.17816/KMJ2021-862.
  19. Wallstrom G, Anderson KS, La Baer J. Biomarker discovery for heterogeneous diseases. Cancer Epidemiol Biomarkers Prev. 2013;22(5):747–755. doi: 10.1158/1055-9965.EPI-12-1236
  20. Engelkes M, Janssens HM, de Jongste JC, et al. Medication adherence and the risk of severe asthma exacerbations: A systematic review. Eur Respir J. 2015;45(2):396–407. doi: 10.1183/09031936.00075614
  21. Schwiebert LM, Beck LA, Stellato C, et al. Glucocorticosteroid inhibition of cytokine production: Relevance to antiallergic actions. J Allergy Clin Immunol. 1996;98(3):718. Corrected and republished from: J Allergy Clin Immunol. 1996;97(1 Pt 2):143–152. doi: 10.1016/s0091-6749(96)80214-4
  22. Williams DM. Clinical pharmacology of corticosteroids. Respir Care. 2018;63(6):655–670. doi: 10.4187/respcare.06314
  23. Doran E, Cai F, Holweg CT, et al. Interleukin-13 in asthma and other eosinophilic disorders. Front Med (Lausanne). 2017;4:139. doi: 10.3389/fmed.2017.00139
  24. Kimura H, Konno S, Makita H, et al. Serum periostin is associated with body mass index and allergic rhinitis in healthy and asthmatic subjects. Allergol Int. 2018;67(3):357–363. doi: 10.1016/j.alit.2017.11.006
  25. Solanki B, Prakash A, Rehan HS, Gupta LK. Effect of inhaled corticosteroids on serum periostin levels in adult patients with mild-moderate asthma. Allergy Asthma Proc. 2019;40(1):32–34. doi: 10.2500/aap.2019.40.4179
  26. Tan E, Varughese R, Semprini R, et al. Serum periostin levels in adults of Chinese descent: An observational study. Allergy Asthma Clin Immunol. 2018;14:87. doi: 10.1186/s13223-018-0312-3
  27. Emson C, Pham TH, Manetz S, Newbold P. Periostin and dipeptidyl peptidase-4: Potential biomarkers of interleukin 13 pathway activation in asthma and allergy. Immunol Allergy Clin North Am. 2018;38(4):611–628. doi: 10.1016/j.iac.2018.06.004
  28. Paplińska-Goryca M, Grabczak EM, Dąbrowska M, et al. Sputum interleukin-25 correlates with asthma severity: A preliminary study. Postepy Dermatol Alergol. 2018;35(5):462–469. doi: 10.5114/ada.2017.71428
  29. Xu M, Dong C. IL-25 in allergic inflammation. Immunol Rev. 2017;278(1):185–191. doi: 10.1111/imr.12558
  30. Tamachi T, Maezawa Y, Ikeda K, et al. IL-25 enhances allergic airway inflammation by amplifying a Th2 cell-dependent pathway in mice. J Allergy Clin Immunol. 2006;118(3):606–614. doi: 10.1016/j.jaci.2006.04.051

Supplementary files

Supplementary Files
Action
1. JATS XML
2. Fig. 1. Ambient air pollution in the residence of patients with asthma and controls: а, PM10Avr; b, PM10MaxAvr; c, PM2,5Avr; d, PM2,5MaxAvr.

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Copyright (c) 2022 Skorokhodkina O.V., Khakimova M.R., Timerbulatova G.A., Bareycheva O.A., Saleeva L.Е., Sharipova R.G., Ablayeva A.V., Fatkhutdinova L.M.

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