The role of IL-33 and IL-1β in the development of persistent allergic rhinitis in overweight/obese children

Cover Page


Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription or Fee Access

Abstract

BACKGROUND: Few works were devoted to the study of the role of cytokines in children with allergic rhinitis (AR) with comorbid obesity.

AIMS: To study the level of cytokines interleukin (IL)1β, IL-33, IL-6, tumor necrosis factor (TNF)-α, and total IgE in the blood serum of overweight/obese children with intermittent and persistent AR.

MATERIALS AND METHODS: This cross-sectional observational study analyzed 69 children aged 7–10 years with AR in the remission period and was conducted from November 2020 to February 2021. All children went through a comprehensive examination for 3 days, including the definition of the serum concentrations IL-1β, IL-33, IL-6, TNF-α, and total IgE. Before blood sampling, children did not use nasal glucocorticosteroids, antileukotriene drugs for the last 4 weeks, and antihistamines for the last 7 days. Bioimpedansometry was used to assess the body weight by calculating the %FM (percentage of body fat mass).

RESULTS: The study included 44 children with AR and overweight/obesity (group I) and 25 children with AR and normal body weight (group II). The analysis of AR showed that in group I, intermittent AR was detected in 11 (25.0%) children (subgroup IA), whereas a persistent course was found in 33 children (75.0%) (subgroup IB). In group II, intermittent AR was detected in 13 (52.0%) children (subgroup IIA), whereas persistent AR in 12 children (48.0%) (subgroup IIB). The level of IL-1β in the blood serum was significantly higher in the subgroup IB than in subgroup IA (p=0.009). The concentration of IL-33 in children with persistent AR and obesity was significantly lower than that in children with intermittent AR and obesity (p=0.039). The level of IL-33 in the serum negatively correlated with %FM in group IA (r=-0.6673, p=0.035). The concentration of IL-1β negatively correlated with %FM in group IIB (r=-0,738, p=0,037). The levels of IL-6, TNF, and total IgE in obese children did not depend on the severity of AR.

CONCLUSIONS: The predictors of persistent AR in children with obesity are a decrease in the level of IL-33 and an increase in IL-1β in the blood serum. The negative correlation between the degree of obesity and IL-33 concentration in children with intermittent AR opens a window of opportunity for the personified management of children with AR and comorbid obesity.

Full Text

Restricted Access

About the authors

Anna E. Koroleva

Smolensk State Medical University

Author for correspondence.
Email: anna.ochkurenko@gmail.com
ORCID iD: 0000-0003-2655-1284
SPIN-code: 6007-1896

MD

Russian Federation, Smolensk

Vladimir V. Bekezin

Smolensk State Medical University

Email: smolenskbvv@yandex.ru
ORCID iD: 0000-0001-9141-5348
SPIN-code: 2518-3769

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

Russian Federation, Smolensk

Irina N. Sergeeva

Smolensk Regional Children’s Clinical Hospital

Email: serg.irina72@mail.ru
ORCID iD: 0000-0001-8863-1103
Russian Federation, Smolensk

Elena A. Volkova

Children’s Clinical Hospital

Email: VL-71@yandex.ru
Russian Federation, Smolensk

Raisa Ya. Meshkova

Smolensk State Medical University; Smolensk Clinical Hospital № 1

Email: meshkova.raisa@yandex.ru
ORCID iD: 0000-0002-7806-9484
SPIN-code: 8937-1230

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

Russian Federation, Smolensk; Smolensk

References

  1. Asher I, Montefort S, Björkstén B, et al. Worldwide time trends in the prevalence of symptoms of asthma, allergic rhinoconjunctivitis, and eczema in childhood: ISAAC Phases One and Three repeat multicountry cross-sectional surveys. Lancet. 2006;368(9537): 733–743. doi: 10.1016/S0140-6736(06)69283-0
  2. Liu Y, Sha J, Meng C, Zhu D. Mechanism of lower airway hyperresponsiveness induced by allergic rhinitis. J Immunol Res. 2022;2022:4351345. doi: 10.1155/2022/4351345
  3. Weinmayr G, Forastiere F, Büchele G, et al. Overweight/Obesity and respiratory and allergic disease in children: International study of asthma and allergies in childhood (ISAAC) phase two. PLoS One. 2014;9(12):e113996. doi: 10.1371/journal.pone.0113996
  4. Abarca-Gómez L, Abdeen ZA, Hamid ZA, et al. Worldwide trends in body-mass index, underweight, overweight, and obesity from 1975 to 2016: A pooled analysis of 2416 population-based measurement studies in 128·9 million children, adolescents, and adults. Lancet. 2017;390(10113):2627–2642. doi: 10.1016/S0140-6737(17)32129-3
  5. Peters U, Dixon AE, Forno E. Obesity and asthma. J Allergy Clin Immunol. 2018;141(4):1169–1179. doi: 10.1016/j.jaci.2018.02.004
  6. Umano GR, Pistone C, Tondina E, et al. Pediatric obesity and the immune system. Front. Pediatr. 2019;7:487. doi: 10.3389/fped.2019.00487
  7. Han MW, Kim SH, Oh I, et al. Obesity can contribute to severe persistent allergic rhinitis in children through leptin and interleukin-1β. Int Arch Allergy Immunol. 2021;182(6):546–552. doi: 10.1159/000512920
  8. Zeng Q, Luo X, Han M, et al. Leptin/Osteopontin axis regulated type 2t helper cell response in allergic rhinitis with obesity. EBio Medicine. 2018;(32):43–49. doi: 10.1016/j.ebiom.2018.05.037
  9. Zeyda M, Wernly B, Demyanets S, et al. Severe obesity increases adipose tissue expression of interleukin-33 and its receptor ST2, both predominantly detectable in endothelial cells of human adipose tissue. Int J Obes (Lond). 2013;37(5):658–665. doi: 10.1038/ijo.2012.118
  10. Wang EW, Jia XS, Ruan CW, Ge ZR. miR-487b mitigates chronic heart failure through inhibition of the IL-33/ST2 signaling pathway. Oncotarget. 2017;8(31):51688–51702. doi: 10.18632/oncotarget.18393
  11. Zhou J, Luo F, Han Y, et al. Obesity/overweight and risk of allergic rhinitis: A meta-analysis of observational studies. Allergy Eur J Allergy Clinl Immunol. 2020;75(5):1272–1275. doi: 10.1111/all14143
  12. Sybilski AJ, Raciborski F, Lipiec A, et al. Obesity -- A risk factor for asthma, but not for atopic dermatitis, allergic rhinitis and sensitization. Public Health Nutr. 2015;18(3):530–536. doi: 10.1017/S1368980014000676
  13. Kelishadi R, Roufarshbaf M, Soheili S, et al. Association of childhood obesity and the immune system: A systematic review of reviews. Childhood Obesity. 2017;13(4):332–346. doi: 10.1089/сhi.2016.0176
  14. Fang X, Henao-Mejia J, Henrickson SE. Obesity and immune status in children. Current Opinion Pediatrics. 2020;32(6):805–815. doi: 10.1097/МОР0000000000000953
  15. Vehapoglu A, Cakın ZE, Kahraman FU, et al. Is overweight/obesity a risk factor for atopic allergic disease in prepubertal children? A case-control study. J Pediatric Endocrinol Metabolism. 2021;34(6):727–732. doi: 10.1515/jpem-2021-0051
  16. Han YY, Forno E, Gogna M, Celedón JC. Obesity and rhinitis in a nationwide study of children and adults in the United States. J Allergy Clin Immunol. 2016;137(5):1460–1465. doi: 10.1016/j.jaci.2015.12.1307
  17. Liu W, Zeng Q, Zhou L, et al. Association of leptin with disease severity and inflammation indicators in Chinese obese children with allergic rhinitis. Pediatric Allergy Immunol. 2018;29(2):186–193. doi: 10.1111/pai.12856
  18. Yazdi AS, Ghoreschi K. The interleukin-1 family. Adv Exp Med Biology. 2016;(941):21–29. doi: 10.1007/978-94-024-0921-5_2
  19. Han MW, Kim SH, Oh I, et al. Serum IL-1β can be a biomarker in children with severe persistent allergic rhinitis. Allergy Asthma Clin Immunol. 201;15(1):58. doi: 10.1186/s13223-019-0368-8
  20. De Oliveira, Talvani A, Rocha-Vieira E. IL-33 in obesity: where do we go from here? Inflamm Res. 2019;68(3):185–194. doi: 10.1007/s00011-019-01214-2
  21. Hasan A, Al-Ghimlas F, Warsame S, et al. IL-33 is negatively associated with the BMI and confers a protective lipid/metabolic profile in non-diabetic but not diabetic subjects. BMC Immunol. 2014;15(1):19. doi: 10.1186/1471-2172-15-19
  22. 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
  23. Haenuki Y, Matsushita K, Futatsugi-Yumikura S, et al. A critical role of IL-33 in experimental allergic rhinitis. J Allergy Clin Immunol. 2012;130(1):184–194.e11. doi: 10.1016/j.jaci.2012.02.013
  24. Rogala B, Glück J. The role of interleukin-33 in rhinitis. Curr Allergy Asthma Rep. 2013;13(2):196–202. doi: 10.1007/s11882-013-0338-z
  25. Fan H, Qin TJ, Ye LS, et al. Expression of IL-25 and IL-33 and the count of EOS in peripheral blood of children with allergic rhinitis receiving immunotherapy. Lin Chung Er Bi. 2018;32(6):443–446. doi: 10.13201/j.issn.1001-1781.2018.06.011
  26. Sakashita M, Yoshimoto T, Hirota T, et al. Association of serum interleukin-33 level and the interleukin-33 genetic variant with Japanese cedar pollinosis. Clin Exp Allergy. 2008;38(12):1875–1881. doi: 10.1111/j.1365-2222.2008.03114.x

Supplementary files

Supplementary Files
Action
1. JATS XML
2. Fig. 1. %FM in subgroups of children with allergic rhinitis.

Download (246KB)
3. Fig. 2. Correlation analysis of the level of the studied cytokines with %FM in children with allergic rhinitis.Note: rxy ― Pearson’s correlation coefficient; rs ― Spearman’s correlation coefficient; R2 ― determination coefficient.

Download (827KB)

Copyright © Pharmarus Print Media, 2022



This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies