Adolescent smoking as risk factor of decrease in adaptation resources of neutrophil metabolism in oral cavity and progressive recurrent bronchitis

View or download the full article: 
PDF icon health-risk-analysis-2024-3-13.pdf
UDC: 
616.155.34:616.311+616.234-002-02:613.84-053.6
DOI: 
10.21668/health.risk/2024.3.13.eng
Authors: 

O.I. Pikuza1, A.M. Zakirova1, Kh.M. Vakhitov1, E.V. Volanyuk2, E.L. Rashitova3, A.A. Pikuza1

Organization: 

1Kazan State Medical University, 49 Butlerova St., Kazan, 420012, Russian Federation
2Kazan State Medical Academy – Branch Campus of the Federal State Budgetary Educational Institution of Further Professional Education «Russian Medical Academy of Continuous Professional Education», 11 Mushtari St., Kazan, 420012, Russian Federation
3Dmitry Rogachev National Medical Research Center of Pediatric Hematology, Oncology and Immunology, 1 Samory Mashela St., Moscow, 117198, Russian Federation

Abstract: 

High prevalence of smoking among children and its early onset is an urgent problem in modern pediatrics. For proper health risk quantification, it is extremely important to understand and parameterize relationships between effects of adverse factors and physiological processes in the body, including the cellular level.

The aim of this study was to analyze how tobacco smoking influences maladaptive changes in the mucosal immunity system of the oral cavity in adolescents and to assess kinetic trends in the clinical course of recurrent bronchitis (RB) in long-term outlook.
The study included 92 patients with RB aged 16.8 ± 3.1 years. Two groups were created of them; the observation group was made of 64 patients, who admitted smoking as a habit, and the reference group included 28 people without nicotine addiction. The control group was made of 23 adolescents of the same age without any signs of the analyzed disease.

Oral neutrophils (N) were selected as basic research material. N oxygen metabolism was registered by luminol-dependent chemiluminescence (LDCL) in spontaneous (sLDCL) and induced (iLDCL) variants. Functional N probing was performed using opsonized zymosan (Σ) and and peptidoglycan from S. aureus strain Cowan. Concentrations of antibodies (AT) to glycolipid (GLP) (Re-mutant Salmonella Minnesota), Candida albicans and S. аureus were determined by ELISA tests.

The analyses made it possible to detect a close relationship between levels of ROS generation by neutrophilic granulocytes and the immune components of anti-endotoxic immunity. Immune changes were not established to be universal in the groups of examined patients and were shown to reflect the specificity of destabilizing effects produced by tobacco smoke. A direct moderate correlation was established in the observation group between sLDCL indicators and the concentration of anti-candidosis antibodies (r = +0.59, p = 0.0382), which reflects the level of bacterial stimulation involving dysbiotic shifts in gut microbiota. A direct correlation was detected between levels of biocidal parameters of neutorphil granulocytes and anti-glycolipid levels (r = +0.64 p = 0.417).

Integral assessment of specific humoral immunity to glycolipid and the phagocytic link of the mucosal protection in the oral cavity reflects the degree of endogenous intoxication and kinetic trends in the RB clinical course in adolescents in subsequent years of life. These relationships may provide solid rounds for ‘exposure – response’ stage in the risk assessment procedure for assessing risks of respiratory diseases in smoking adolescents.

Keywords: 
adolescents, smoking, recurrent bronchitis, mucosal immunity, oral neutrophilic granulocytes, endotoxin aggression, anti-endotoxic immunity, prediction
Pikuza O.I., Zakirova A.M., Vakhitov Kh.M., Volanyuk E.V., Rashitova E.L., Pikuza A.A. Adolescent smoking as risk factor of decrease in adaptation resources of neutrophil metabolism in oral cavity and progressive recurrent bronchitis. Health Risk Analysis, 2024, no. 3, pp. 123–131. DOI: 10.21668/health.risk/2024.3.13.eng
References: 
  1. Baranov A.A., Albitskiy V.Yu. State of health of children in Russia, priorities of its preservation and improving. Ka-zanskii meditsinskii zhurnal, 2018, vol. 99, no. 4, pp. 698–705. DOI: 10.17816/KMJ2018-698 (in Russian).
  2. Dumler A.A., Uteva N.A. Rasprostranennost' veip-assotsiirovannoi travmy legkikh sredi studentov meditsinskogo vuza [Prevalence of vape-associated lung injury among medical students]. Zdorov'e natsii v XXI veke, 2022, no. 1, pp. 23 (in Russian).
  3. Vafin A.Yu., Vizel A.A., Sherputovsky V.G., Lysenko G.V., Kolgin R.A., Vizel I.Yu., Shaymuratov R.I., Amirov N.B. Respiratory diseases in tatarstan: perennial epidemiological analysis. Vestnik sovremennoi klinicheskoi meditsiny, 2016, vol. 9, no. 1, pp. 24–31. DOI: 10.20969/vskm.2016.9(1).24-31 (in Russian).
  4. Wawrzyniak A., Lipińska-Opałka A., Kalicki B., Kloc M. The effect of passive exposure to tobacco smoke on the immune response in children with asthma. Subst. Use Misuse, 2021, vol. 56, no. 3, pp. 424-430. DOI: 10.1080/10826084.2020.1869263
  5. Zubairova L.D., Zubairov D.M. Kurenie kak faktor riska serdechno-sosudistykh zabolevanii [Smoking as a risk factor of cardiovascular diseases]. Kazanskii meditsinskii zhurnal, 2006, vol. 87, no. 5, pp. 369–374 (in Russian).
  6. Abakhainova M.A. Vliyanie elektronnykh sigaret na sostoyanie slizistoi polosti rta [The influence of electronic cigarettes on the condition of the oral mucosa]. Fundamental'nye aspekty psikhicheskogo zdorov'ya, 2018, no. 2, pp. 22–25 (in Russian).
  7. Mizinov D.S., Kryukov Y.Y. Upotreblenie nikotinsoderzhashchikh veshchestv sredi studencheskoi molodezhi [Use of nicotine-containing substances among students]. Byulleten' meditsinskikh internet-konferentsii, 2020, vol. 10, no. 9, pp. 243 (in Russian).
  8. Galikhanova Yu.I., Shklyaev A.E., Pantyukhina A.S., Dudarev V.M., Kazarin D.D. Impact of electronic cigarettes on acid forming and motor functions of the stomach. Vestnik sovremennoi klinicheskoi meditsiny, 2023, vol. 16, no. 6, pp. 14–18 DOI: 10.20969/VSKM.2023.16(6).14-18 (in Russian).
  9. Mendelevich V.D. Benefits and harm of electronic cigarettes through the prism of different therapeutic methodologies. Vestnik sovremennoi klinicheskoi meditsiny, 2015, vol. 8, no. 2, pp. 61–73 (in Russian).
  10. Popova N.M., Korobeinikov M.S., Alekseeva N.A. Rasprostranennost' kureniya sigaret, kal'yanov i elektronnykh sig-aret sredi studentov Izhevskoi meditsinskoi akademii [Prevalence of smoking cigarettes, hookahs and electronic cigarettes among students of the Izhevsk Medical Academy]. Vestnik nauki, 2019, vol. 2, no. 4 (13), pp. 97–100 (in Russian).
  11. Gelashvili O.A., Khisamov R.R., Shalneva I.R. Physical development of children and adolescents. Modern problems of science and education, 2018, no. 3, pp. 123 Available at: https://science-education.ru/ru/article/view?id=27656 (April 12, 2024) (in Russian).
  12. Shklyaev A.E., Galikhanova Yu.I., Pantyukhina A.S., Gorbunov Yu.V. Kachestvo zhizni pol'zovatelei elektronnykh sigaret [Quality of life of e-cigarette users]. Terapiya, 2023, vol. 9, no. 3S, pp. 464–465. DOI: 10.18565/therapy.2023.3suppl.464-465 (in Russian).
  13. Ovsyannikov D.Yu., Boytsova E.V., Furman E.G., Mazunina E.S. Protracted bacterial bronchitis in children – the «new» «old» disease. Pediatriya, 2017, vol. 96, no. 2, pp. 136–144 (in Russian).
  14. Andryukov B.G., Bogdanova V.D., Lyapun I.N. Phenotypic heterogeneity of neutrophils: new antimicrobic character-istics and diagnostic technologies. Gematologiya i transfuziologiya, 2019, vol. 64, no. 2, pp. 211–221. DOI: 10.35754/0234-5730-2019-64-2-211-221 (in Russian).
  15. Wang J., Hossain M., Thanabalasuriar A., Gunzer М., Meininger С., Kubes P. Visualizing the function and fate of neutrophils in sterile injury and repair. Science, 2017, vol. 358, no. 6359, pp. 111–116. DOI: 10.1126/science.aam9690
  16. Jones H.R., Robb C.T., Perretti M., Rossi A.G. The role of neutrophils in inflammation resolution. Semin. Immunol., 2016, vol. 28, no. 2, pp. 137–145. DOI: 10.1016/j.smim.2016.03.007
  17. Kaur M., Singh D. Neutrophil chemotaxis caused by chronic obstructive pulmonary disease alveolar macrophages: the role of CXCL8 and the receptors CXCR1/CXCR2. J. Pharmacol. Exp. Ther., 2013, vol. 347, no. 1, pp. 173–180. DOI: 10.1124/jpet.112.201855
  18. Dolgushin I.I., Mezentseva E.A., Savochkina A.Yu., Kuznetsova E.K. Neutrophil as a multifunctional relay in immune system. Infektsiya i immunitet, 2019, vol. 9, no. 1, pp. 9–38. DOI: 10.15789/2220-7619-2019-1-9-38 (in Russian).
  19. Andryukov B.G., Somova L.M., Drobot E.I., Matosova E.V. Defensive strategy of neutrophilic granulocytes against pathogenic bacteria. Zdorov'e, meditsinskaya ekologiya. Nauka, 2017, no. 1 (68), pp. 4–18. DOI: 10.5281/zenodo.345606 (in Rus-sian).
  20. Pikuza O.I., Fayzullina R.A., Zakirova A.M., Suleymanova Z.Y., Rashitova E.L., Volyanyuk E.V. Bactericidal capacity of oral neutrophils as a marker for clinical course of inflammatory -respiratory diseases in children. Kazanskii meditsinskii zhurnal, 2020, vol. 101, no. 5, pp. 740–748. DOI: 10.17816/KMJ2020-740 (in Russian).
  21. Pikuza O.I., Zakirova A.M., Volyanyuk E.V., Filatov V.S., Pikuza A.V., Zakirov A.M. Functional potential of coloni-zation defense of buccal epitheliocytes as an indicator of the clinical course of respiratory tract diseases. Prakticheskaya meditsina, 2023, vol. 21, no. 1, pp. 75–79. DOI: 10.32000/2072-1757-2023-1-75-79 (in Russian).
  22. Shishkova Yu.S., Babikova M.S., Golovin N.S., Filimonova O.I. Factors of colonization resistance of oral mucous membranes in individuals using dental orthopedic constructions: peculiarities of biofilm-forming activity of microorganisms. Ural'skii meditsinskii zhurnal, 2017, vol. 153, no. 9, pp. 72–74 (in Russian).
  23. Mayansky A.N., Abadzhidi M.A., Mayanskaya I.V., Zaslavskaya M.I., Makhrova T.V. Reaktivnost' bukkal'nykh epiteliotsitov: indikatsiya mestnykh i obshchikh narushenii gomeostaza (obzor literatury) [Reactivity of buccal epithelial cells: indication of local and general disorders of homeostasis (literature review)]. Klinicheskaya laboratornaya diagnostika, 2004, no. 8, pp. 31–34 (in Russian).
  24. Agafonova E.V., Reshetnikova I.D., Bayazitova L.T., Khaldeyeva E.V., Tyurin Yu.A., Isayeva G.Sh. Violation of an-timicrobial strategies of neutrophils at the level of mucosal immunity in COVID-19 convalescents. Prakticheskaya meditsina, 2022, vol. 20, no. 7, pp. 122–130. DOI: 10.32000/2072-1757-2022-7-122-130 (in Russian).
  25. Nesterova I.V., Kolesnikova N.V., Chudilova G.A., Lomtatidze L.V., Kovaleva S.V., Evglevsky A.A., Nguyen T.D.L. The new look at neutrophilic granulocytes: rethinking old dogmas. Part 1. Infektsiya i immunitet, 2017, vol. 7, no. 3, pp. 219–230. DOI: 10.15789/2220-7619-2017-3-219-230 (in Russian).
  26. Masnavieva L.B., Efimova N.B. Indicators of Local and Systemic Immunity of Adolescents under Combined Exposure to Air Pollution and Cigarette Smoke. ZNiSO, 2022, no. 8, pp. 57–63. DOI: 10.35627/2219-5238/2022-30-8-57-63 (in Russian).
  27. Eguiluz-Gracia I., Mathioudakis A.G., Bartel S., Vijverberg S.J.H., Fuertes E., Comberiati P., Cai Y.S., Tomazic P.V. [et al.]. The need for clean air: The way air pollution and climate change affect allergic rhinitis and asthma. Allergy, 2020, vol. 75, no. 9, pp. 2170–2184. DOI: 10.1111/all.14177
  28. Rosário Filho N.A., Urrutia-Pereira M., D'Amato G., Cecchi L., Ansotegui I.J., Galán C., Pomés A., Murrieta-Aguttes M. [et al.]. Air pollution and indoor settings. World Allergy Organ. J., 2021, vol. 14, no. 1, pp. 100499. DOI: 10.1016/j.waojou.2020.100499
  29. Hellings P.W., Steelant B. Epithelial barriers in allergy and asthma. J. Allergy Clin. Immunol., 2020, vol. 145, no. 6, pp. 1499–1509. DOI: 10.1016/j.jaci.2020.04.010
  30. Takahashi T., Iwasaki A. Sex differences in immune responses. Science, 2021, vol. 371, no. 6527, pp. 347–348. DOI: 10.1126/science.abe7199
  31. Shepherd R., Cheung A.S., Pang K., Saffery R., Novakovic B. Sexual dimorphism in innate immunity: The role of sex hormones and epigenetics. Front. Immunol., 2021, vol. 11, pp. 604000. DOI: 10.3389/fimmu.2020.604000
  32. Tulgar Y.K., Cakar S., Tulgar S., Dalkilic O., Cakiroglu B., Uyanik B.S. The effect of smoking on neutro-phil/lymphocyte and platelet/lymphocyte ratio and platelet ındices: a retrospective study. Eur. Rev. Med. Pharmacol. Sci., 2016, vol. 20, no. 14, pp. 3112–3118.
  33. Adeluyi A., Guerin L., Fisher M.L., Galloway A., Cole R.D., Chan S.S.L., Wyatt M.D., Davis S.W. [et al.]. Microglia morphology and proinflammatory signaling in the nucleus accumbens during nicotine withdrawal. Sci. Adv., 2019, vol. 5, no. 10, pp. eaax7031. DOI: 10.1126/sciadv.aax7031
  34. Soares A.R., Picciotto M.R. Nicotinic regulation of microglia: potential contributions to addiction. J. Neural Transm. (Vienna), 2024, vol. 131, no. 5, pp. 425–435. DOI: 10.1007/s00702-023-02703-9
  35. Aryal S.P., Fu X., Sandin J.N., Neupane K.R., Lakes J.E., Grady M.E., Richards C.I. Nicotine induces morphological and functional changes in astrocytes via nicotinic receptor activity. Glia, 2021, vol. 69, no. 8, pp. 2037–2053. DOI: 10.1002/glia.24011
  36. Brooks A.C., Henderson B.J. Systematic review of nicotine exposure’s efects on neural stem and progenitor cells. Brain Sci., 2021, vol. 11, no. 2, pp. 172. DOI: 10.3390/brainsci11020172
  37. Bye L.J., Finol-Urdaneta R.K., Tae H.-S., Adams D.J. Nicotinic acetylcholine receptors: key targets for attenuating neurodegenerative diseases. Int. J. Biochem. Cell. Biol., 2023, vol. 157, pp. 106387. DOI: 10.1016/j.biocel.2023.106387
  38. Chen D., Li J., Huang Y., Wei P., Miao W., Yang Y., Gao Y. Interleukin 13 promotes longterm recovery after ischemic stroke by inhibiting the activation of STAT3. J. Neuroinfammation, 2022, vol. 19, no. 1, pp. 112. DOI: 10.1186/s12974-022-02471-5
  39. Gould T.J. Epigenetic and long-term effects of nicotine on biology, behavior, and health. Pharmacol. Res., 2023, vol. 192, pp. 106741. DOI: 10.1016/j.phrs.2023.106741
Received: 
05.06.2024
Approved: 
19.09.2024
Accepted for publication: 
23.09.2024

You are here

Home