Content of pro- and anti-infl ammatory cytokines in the dynamics of experimental periodontitis in rats with chronic pain syndrome

• Anna E. Brusentsova
• Andrei Yu. Liashev
• Nikolay V. Tsygan
• Nicolas E. Tzenios
• Yuri D. Lyashev

Abstract

Introduction. The influence of chronic pain on the development of periodontitis is still unclear in spite of the wide spreading of periodontitis and chronic pain syndrome, especially in adult and elderly patients.

The aim of study – analysis of the influence of preliminary simulated chronic pain syndrome on the dynamics of pro- and anti-inflammatory cytokines in rats with experimental periodontitis development.

Material and methods. Chronic pain syndrome in Wistar rats was modeled by two-sided ligaturing sciatic nerves. Experimental periodontitis was modeled using the method supposed by A.I. Volozhin and S.I. Vinogradova. The following groups were formed in the study: naïve rats, animals with chronic pain syndrome, sham-operated rats, animals with experimental periodontitis, sham-operated rats with experimental periodontitis, animals with chronic pain syndrome and experimental periodontitis. The animals were deduced from the experiment on the 7^th, 14^th and 21^st days after thread removing. The content of cytokines: IL-1β, IL-4, IL-6, IL-10, as well as TNFα and interferon-γ were detected in the blood plasm.

Results. The simulation of the chronic pain symdrome or sham operation didn’t cause the changes in the cytokines content in blood plasm. The increase of the concentration of pro- and anti-inflammatory cytokines in blood plasm of the rats with experimental periodontitis and sham-operated animals with experimental periodontitis was found throughout the experiment. The higher content of proinflammatory cytokines (IL-1β, IL-6, TNFα) in the blood plasma was revealed in the animals with experimental periodontitis and chronic pain syndrome throughout the experiment compared to the group, which experimental periodontitis was modeled. The concentration of anti-inflammatory interleukins in this group was less than one in rats with experimental periodontitis: IL-10 on the 7^th–21^st days and IL-4 on the 21^st day. Indicated changes are conditioned by the influence of chronic pain syndrome on the development of experimental periodontitis in the animals.

Conclusion. The peculiarities of experimental periodontitis development in the rats with chronic pain syndrome were found in the study: the increase of the concentration of proinflammatory and decrease of the content of anti-inflammatory cytokines in blood plasm, compared to the group, which experimental periodontitis was modeled

Keywords:chronic pain syndrome; periodontitis; cytokines

References

1. Leont’ev V.K., Faustov L.A., Galenko-Yaroshevsky P.A., Popkov V.L. Chronic generalized periodontitis: clinical and experimental pharmacotherapy by metabolic correctors. Krasnodar: Prosveshcheniye-Yug, 2012: 403 p. (in Russian)

2. Loktionov A.L., Konoplya A.I., Lunev M.A., Karaulov A.V. Immune and oxidant disorders in the pathogenesis of inflammatory periodontium diseases. Immunologiya. 2015; 36 (5): 319–28. (in Russian)

3. Kotieva I.M., Frantsiyants E.M., Kaplieva I.V., Bandovkina V.A., Kozlova L.C., Trepitaki L.K., Pogorelova Yu.A., Cheryarina N.D. The influence of chronic pain on some metabolic processes in the skin of female mice. Rossiyskiy zhurnal boli. 2018; 4: 46–54. DOI: https://doi.org/10.25731/RASP.2018.04.027 (in Russian)

4. Sturgill J., McGee E., Menzies V. Unique cytokine signature in the plasma of patients with fibromyalgia. J. Immunol. Res. 2014; 1: 1–5. DOI: https://doi.org/10.1155/2014/938576

5. Khan J., Puchimada P., Kadouri D., Zusman T., Javed F., Eliav E. The anti-nociceptive effects of Porphyromonas gingivalis lipopolysaccharide. Arch. Oral Biol. 2019; 102: 193–8. DOI: https://doi.org/10.1016/j.archoralbio.2019.04.012

6. Volozhin A.I., Vinogradova S.I. Modeling and treatment of the inflammation in periodontitis. Pathologicheskaya fiziologiya i experimental’naya terapiya. 1990; 6: 49–51. (in Russian)

7. Sesti-Costa R., Ignacchiti M.D., Chedraoui-Silva S., Marchi L.F., Mantovani B. Chronic cold stress in mice induces a regulatory phenotype in macrophages: correlation with increased 11beta-hydroxysteroid dehydrogenase expression. Brain Behav. Immun. 2012; 26: 50–60. DOI: https://doi.org/10.1016/j.bbi.2011.07.234

8. Ahmad S.F., Zoheir K.M., Ansari M.A., Korashy H.M., Bakheet S.A., Ashour A.E., Attia S.M. Stimulation of the histamine 4 receptor with 4-methylhistamine modulates the effects of chronic stress on the Th1/Th2 cytokine balance. Immunobiology. 2015; 220: 341–9. DOI: https://doi.org/10.1016/j.imbio.2014.10.014

9. Woda A., Picard P., Dutheil F. Dysfunctional stress responses in chronic pain. Psychoneuroendocrinology. 2016; 71: 127–35. DOI: https://doi.org/10.1016/j.psyneuen.2016.05.017

10. Pekny M., Pekna M. Astrocyte reactivity and reactive astrogliosis: costs and benefits. Physiol. Rev. 2014; 94: 1077–98. DOI: https://doi.org/10.1152/physrev.00041.2013

11. Marklund N., Peltonen M., Nilsson T.K., Olsson T. Low and high circulating cortisol levels predict mortality and cognitive dysfunction early after stroke. J. Intern. Med. 2004; 256: 15–21.

12. Grigorovich E.Sh., Pomogaylo E.G., Khomutova E.Yu., Stepanov S.S. Clinical variants of chronic generalized periodontitis, genetic polymorphism and system production of inflammatory cytokines. Stomatologiya. 2015: 94 (5): 11–6. DOI: https://doi.org/10.17116/stomat2018594511-16 (in Russian)

13. Petrukhina N.B., Zorina O.A., Shikh E.V., Kartysheva E.V., Kudryavtsev A.V., Berkutova I.S. The change of proinflammatory cytokines in the patients with chronic periodontitis on the background of metabolic syndrome in dependence on sex and age. Stomatologiya. 2018; 97 (6): 38–44. DOI: https://doi.org/10.17116/stomat20189706138 (in Russian)

14. Luchting B., Rachinger-Adam B., Heyn J., Hinske L., Kreth S., Azad S. Antiinflammatory T-cell shift in neuropathic pain. J. Neuroinflamm. 2015; 12 (1): 12. DOI: https://doi.org/10.1186/s12974-014-0225-0

15. Kolesnikova N.V., Samoylenko E.S. The role of cytokines in the pathogenesis of infectious endocardidtis. Immunologiya. 2020; 41 (3): 262–8. DOI: https://doi.org/10.33029/0205-4952-2020-41-3-262-268 (in Russian)

16. Ketlinsky S.A., Simbirtsev A.S. Cytokines. Saint Petersburg: Foliant, 2008. (in Russian)

17. Malkiel S., Barlev A.N., Atisha-Fregoso Y., Suurmond Y., Diamond B. Plasma cell differentiation pathways in systemic lupus erythematosus. Front. Immunol. 2018; 9: 427. DOI: https://doi.org/10.3389/fimmu.2018.00427

18. Yoshimoto T. The hunt for the source of primary interleukin-4: how we discovered that natural killer T cells and basophils determine T helper type 2 cell differentiation in vivo. Front. Immunol. 2018; 9: 716. DOI: https://doi.org/10.3389/fimmu.2018.00716

19. Sasaki H., Okamatsu Y., Kawai T., Kent R., Taubman M., Stashenko P. The interleukin-10 knockout mouse is highly susceptible to Porphyromonas gingivalis induced alveolar bone loss. J. Periodontal Res. 2004; 39 (6): 432–41.

20. Balmasova I.P., Tsarev V.N., Yushchuk E.N., Dorovskikh A.S., Malova E.S., Karakov K.G., El’bekyan K.S., Arutyunov S.D. The diseases of periodontitis and atherosclerosis: microecological, metabolic and immunological mechanisms of interrelation. Immunologiya. 2020; 41 (4): 370–80. DOI: https://doi.org/10.33029/0206-4952-2020-41-4-370-380 (in Russian)

21. Li L., Michel R., Cohen J., Decarlo A., Kozarov E. Intracellular survival and vascular cell-to-cell transmission of Porphyromonas gingivalis. BMC Microbiol. 2008; 8: 26–36. DOI: https://doi.org/10.1186/1471-2180-8-26

22. Gur’yanova S.V., Kolesnikova N.V., Gudima G.O., Lezhava N.L., Karaulov A.V. Dynamics of immunological and microbiological indices of throat fluid in the therapy of cavity. Immunologiya. 2021; 42 (4): 386–94. DOI: https://doi.org/10.33029/0206-4952-2021-42-4-386-394 (in Russian)

23. Lonn J., Ljunggren S., Klarstrom-Engstrom K., Demirel I., Bengtsson T., Karlsson H. Lipoprotein modifications by gingipains of Porphyromonas gingivalis. J. Periodontal Res. 2018; 53 (3): 403–13. DOI: https://doi.org/10.1111/jre.12527

24. Abramova A.Yu., Pertsov S.S. Correlation dependence between the indices of nociceptive sensitivity and cytokines level in the biological mediums in the rats after lipopolysaccharide injection. Byulleten’ eksperimental’noi biologii i meditsiny. 2014; 157 (5): 548–53. (in Russian)

25. Kushlinsky N.E., Solovykh E.A., Karaoglanova T.B., Bayar W., Gersteyn E.S., Troshin A.A., Maksimovskaya L.N., Yanushevich O.O. Matrix metalloproteases and inflammatory cytokines in the throat fluid of the patients by chronic periodontitis with the different constructive materials. Byulleten’ eksperimental’noi biologii i meditsiny. 2012; 153 (1): 82–7. (in Russian)

All articles in our journal are distributed under the Creative Commons Attribution 4.0 International License (CC BY 4.0 license)