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

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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.

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

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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.

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