CC BY 4.0 · Eur J Dent 2024; 18(01): 253-264
DOI: 10.1055/s-0043-1768154
Original Article

Salivary IL-17 and IL-10 as Potential Diagnostic Biomarkers of Different Stages of Periodontitis in Smoker and Nonsmoker Patients

Maha Abdulsalam Mohammed
1   Department of Periodontology, College of Dentistry, University of Baghdad, Baghdad, Iraq
,
Raghad Fadhil Abbas
1   Department of Periodontology, College of Dentistry, University of Baghdad, Baghdad, Iraq
,
1   Department of Periodontology, College of Dentistry, University of Baghdad, Baghdad, Iraq
› Author Affiliations
Funding None.

Abstract

Objectives The gold standard in the field of periodontal research currently is to find a valid biomarker that can reliably be used for diagnosing periodontal diseases. Given the limitations of the current diagnostic tools that stall to predict susceptible individuals and determine whether active tissue destruction is occurring, there is an increased urge to develop alternative diagnostic techniques that would compensate for the problems inherited in these available methods, such as measuring levels of biomarkers present in oral fluids such as saliva; so the aim of this study was to determine the diagnostic potential of interleukin-17 (IL-17) and IL-10 to differentiate periodontal health from smoker and nonsmoker periodontitis, and to differentiate among different stages (severities) of periodontitis.

Materials and Methods An observational case–control study was performed on 175 systemically healthy participants grouped into healthy as controls and periodontitis as cases. Periodontitis cases were divided according to the severity into stages I, II, and III, and each of the stages was further subdivided into smokers and nonsmokers patients. Unstimulated saliva samples were collected, clinical parameters were recorded, and salivary levels were assayed using enzyme-linked immunosorbent assay.

Results Elevated levels of IL-17 and IL-10 were associated with stage I and II compared with the healthy controls. However, a significant decrease in stage III was observed compared with the control group for both biomarkers.

Conclusion Salivary IL-17 and IL-10 might be useful for distinguishing periodontal health from periodontitis; however, further research is needed to substantiate their use as potential biomarkers for the diagnosis of periodontitis

Strengths and Limitations of the Study

The strength aspect of the study lies in the relatively high number of study participants and their division into seven subcategories, taking into account cigarette smoking that is a common habit in society and a confirmed risk factor for periodontitis, thus, enabling the sample to become more representative of the population and giving more solidity to the results. Another important aspect is the use of ROC test for not only determining the sensitivity and specificity of the selected biomarkers but also comparing levels in health versus disease.


Limitations and future suggestions include using a multitude of biomarkers as this will improve the sensitivity and specificity, including gingivitis group in future studies is highly recommended, as well as including stage IV along with the incorporation of periodontitis grade.


Institutional Review Board Statement

The protocol was approved by the Ethics Committee in College of Dentistry, the University of Baghdad in 19–1-2022, Ref. number: 451.


Informed Consent Statement

Informed consent was obtained from all subjects involved in the study.


Data Availability Statement

The data illustrated in the study is available on request.




Publication History

Article published online:
12 May 2023

© 2023. The Author(s). This is an open access article published by Thieme under the terms of the Creative Commons Attribution License, permitting unrestricted use, distribution, and reproduction so long as the original work is properly cited. (https://creativecommons.org/licenses/by/4.0/)

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  • References

  • 1 Chapple ILC, Mealey BL, Van Dyke TE. et al. Periodontal health and gingival diseases and conditions on an intact and a reduced periodontium: consensus report of workgroup 1 of the 2017 World Workshop on the Classification of Periodontal and Peri-Implant Diseases and Conditions. J Periodontol 2018; 89 (Suppl. 01) S74-S84
  • 2 Kornman KS. Mapping the pathogenesis of periodontitis: a new look. J Periodontol 2008; 79 (8, Suppl): 1560-1568
  • 3 Cekici A, Kantarci A, Hasturk H, Van Dyke TE. Inflammatory and immune pathways in the pathogenesis of periodontal disease. Periodontol 2000 2014; 64 (01) 57-80
  • 4 Ramadan DE, Hariyani N, Indrawati R, Ridwan RD, Diyatri I. Cytokines and chemokines in periodontitis. Eur J Dent 2020; 14 (03) 483-495
  • 5 Graves DT, Cochran D. The contribution of interleukin-1 and tumor necrosis factor to periodontal tissue destruction. J Periodontol 2003; 74 (03) 391-401
  • 6 Khader SA, Gaffen SL, Kolls JK. Th17 cells at the crossroads of innate and adaptive immunity against infectious diseases at the mucosa. Mucosal Immunol 2009; 2 (05) 403-411
  • 7 Mocellin S, Panelli MC, Wang E, Nagorsen D, Marincola FM. The dual role of IL-10. Trends Immunol 2003; 24 (01) 36-43
  • 8 Madiba TK, Bhayat A. Periodontal disease – risk factors and treatment options. S Afr Dent J 2018; 73 (09) 571-575
  • 9 He W, You M, Wan W, Xu F, Li F, Li A. Point-of-care periodontitis testing: biomarkers, current technologies, and perspectives. Trends Biotechnol 2018; 36 (11) 1127-1144
  • 10 Srivastava N, Nayak PA, Rana S. Point of care- a novel approach to periodontal diagnosis-a review. J Clin Diagn Res 2017; 11 (08) ZE01-ZE06
  • 11 Inönü E, Kayis SA, Eskan MA, Hakki SS. Salivary Del-1, IL-17, and LFA-1 levels in periodontal health and disease. J Periodontal Res 2020; 55 (04) 511-518
  • 12 Tonetti MS, Greenwell H, Kornman KS. Staging and grading of periodontitis: Framework and proposal of a new classification and case definition. J Periodontol 2018; 89 (Suppl. 01) S159-S172
  • 13 Preventing chronic disease: Current volume. Centers for Disease Control and Prevention. Accessed March 10, 2023 at: https://www.cdc.gov/pcd/issues/2015/2015_toc.htm
  • 14 O'Leary TJ, Drake RB, Naylor JE. The plaque control record. J Periodontol 1972; 43 (01) 38
  • 15 Asif S, Ahmad B, Hamza SA, Taib H, Kassim NK, Zainuddin SLA. Investigation of salivary RANKL and OPG levels in periodontitis patients at hospital Universiti Sains Malaysia. Eur J Dent 2022; 16 (01) 173-178
  • 16 Lertpimonchai A, Rattanasiri S, Arj-Ong Vallibhakara S, Attia J, Thakkinstian A. The association between oral hygiene and periodontitis: a systematic review and meta-analysis. Int Dent J 2017; 67 (06) 332-343
  • 17 Albandar JM, Streckfus CF, Adesanya MR, Winn DM. Cigar, pipe, and cigarette smoking as risk factors for periodontal disease and tooth loss. J Periodontol 2000; 71 (12) 1874-1881
  • 18 Hormdee D, Prajaneh S, Kampichai A, Tak R, Chaiyarit P. Prolonged suppressive effects of periodontitis on salivary TFF3 production. Eur J Dent 2019; 13 (02) 193-198
  • 19 Ali BG, Ali OH. Detection of salivary flow rate and minerals in smokers and nonsmokers with chronic periodontitis (Clinical and Biochemical study). J Bagh College Dentistry 2012; 24 (01) 68-71
  • 20 Ameer LR, Ali BG. Effects of light smoking on salivary levels of alkaline phosphatase and osteocalcin in chronic periodontitis patients. J Bagh College of Dentistry 2015; 27 (02) 110-114
  • 21 Velidandla S, Bodduru R, Birra V, Jain Y, Valluri R, Ealla KKR. Distribution of periodontal pockets among smokers and nonsmokers in patients with chronic periodontitis: a cross-sectional study. Cureus 2019; 11 (09) e5586 DOI: 10.7759/cureus.5586.
  • 22 Zhou J, Olson BL, Windsor LJ. Nicotine increases the collagen-degrading ability of human gingival fibroblasts. J Periodontal Res 2007; 42 (03) 228-235
  • 23 Mavi S, Arora S, Chinna S. et al. Influence of sociodemographic factors and behavioral habits on periodontal disease status. Dent J Adv Stud 2021; 9 (02) 77-82
  • 24 Zenobia C, Hajishengallis G. Basic biology and role of interleukin-17 in immunity and inflammation. Periodontol 2000 2015; 69 (01) 142-159
  • 25 Severino VO, Napimoga MH, de Lima Pereira SA. Expression of IL-6, IL-10, IL-17 and IL-8 in the peri-implant crevicular fluid of patients with peri-implantitis. Arch Oral Biol 2011; 56 (08) 823-828
  • 26 Techatanawat S, Surarit R, Chairatvit K. et al. Salivary and serum interleukin-17A and interleukin-18 levels in patients with type 2 diabetes mellitus with and without periodontitis. PLoS One 2020; 15 (02) e0228921 DOI: 10.1371/journal.pone.0228921.
  • 27 Nair V, Grover V, Arora S. et al. Comparative evaluation of Gingival crevicular fluid interleukin-17, 18 and 21 in different stages of periodontal health and disease. Medicina (Kaunas) 2022; 58 (08) 1042 DOI: 10.3390/medicina58081042.
  • 28 Arief EM, Mubin MB, Zainuddin SL, Abdullah NA, Ahmad B. Serum interleukin-17 (IL-17) in chronic periodontitis patients. Padjadjaran Journal of Dentistry 2017; 29 (03) 138-142
  • 29 Liukkonen J, Gürsoy UK, Pussinen PJ, Suominen AL, Könönen E. Salivary concentrations of interleukin (il)-1β, IL-17A, and IL-23 vary in relation to periodontal status. J Periodontol 2016; 87 (12) 1484-1491
  • 30 Sadeghi R, Sattari M, Dehghan F, Akbari S. Interleukin-17 and interleukin-23 levels in gingival crevicular fluid of patients with chronic and aggressive periodontitis. Cent Eur J Immunol 2018; 43 (01) 76-80
  • 31 Rodríguez-Montaño R. Ruiz-Gutiérrez Adel, Martínez-Rodríguez VM, et al Levels of IL-23/il-17 axis in plasma and gingival tissue of periodontitis patients according to the new classification. Appl Sci (Basel) 2022; 12 (16) 8051 DOI: 10.3390/app12168051.
  • 32 Sulistio E, Masulili SL, Lessang R, Auerkari EI. The influence of smoking on IL-17 cytokine in chronic periodontitis patients. J Int Dent Medical Res 2019; 12 (01) 199-202
  • 33 Javed F, Al-Zawawi AS, Allemailem KS. et al. Periodontal conditions and whole salivary IL-17A and -23 levels among young adult cannabis sativa (marijuana)-smokers, heavy cigarette-smokers and non-smokers. Int J Environ Res Public Health 2020; 17 (20) 7435 DOI: 10.3390/ijerph17207435.
  • 34 Ge S, Ye P, Li G-Y. et al. Effects of active and passive smoking on salivary cytokines levels in rats: a pilot study. Toxicol Ind Health 2019; 35 (02) 109-118
  • 35 Mokeem SA, Alasqah MN, Michelogiannakis D, Al-Kheraif AA, Romanos GE, Javed F. Clinical and radiographic periodontal status and whole salivary cotinine, IL-1β and IL-6 levels in cigarette- and waterpipe-smokers and E-cig users. Environ Toxicol Pharmacol 2018; 61: 38-43
  • 36 Ozçaka O, Nalbantsoy A, Buduneli N. Interleukin-17 and interleukin-18 levels in saliva and plasma of patients with chronic periodontitis. J Periodontal Res 2011; 46 (05) 592-598
  • 37 Fenol A, Sasidharan RK, Krishnan S. Levels of interleukin -10 in gingival crevicular fluid and its role in the initiation and progression of gingivitis to periodontitis. J Oral Hyg Health 2014; 02 (03) 135
  • 38 Varma SR, Thomas B, Ramesh A. et al. Estimation of sialic acid and IL10 levels in stage 1 and 2 periodontitis patients. Int J Dent 2019; 2019: 2917124 DOI: 10.1155/2019/2917124.
  • 39 Tâlvan ET, Mohor C, Chisnoiu D, Cristea V, Câmpian RS. Expression of interleukin (il)-1β, IL-8, IL-10 and IL-13 in chronic adult periodontitis progression. Arch Med (Oviedo) 2017; 09 (03) 4 DOI: 10.21767/1989-5216.1000219.
  • 40 He C-Y, Gao X-Q, Jiang L-P. The impact of smoking on levels of chronic periodontitis-associated biomarkers. Exp Mol Pathol 2016; 101 (01) 110-115
  • 41 Ojima M, Hanioka T. Destructive effects of smoking on molecular and genetic factors of periodontal disease. Tob Induc Dis 2010; 8 (01) 4 DOI: 10.1186/1617-9625-8-4.
  • 42 de Heens GL, Kikkert R, Aarden LA, van der Velden U, Loos BG. Effects of smoking on the ex vivo cytokine production in periodontitis. J Periodontal Res 2009; 44 (01) 28-34
  • 43 Medara N, Lenzo JC, Walsh KA, Darby IB, O'Brien-Simpson NM, Reynolds EC. T helper 17 cell-related cytokines in serum and saliva during management of periodontitis. Cytokine 2020; 134: 155186 DOI: 10.1016/j.cyto.2020.155186.
  • 44 Moretti S, Bartolommei L, Galosi C. et al. Fine-tuning of th17 cytokines in periodontal disease by IL-10. J Dent Res 2015; 94 (09) 1267-1275
  • 45 Sun L, Girnary M, Wang L. et al. Il-10 dampens an IL-17–mediated periodontitis-associated inflammatory network. J Immunol 2020; 204 (08) 2177-2191
  • 46 Armijo-Olivo S. The importance of determining the clinical significance of research results in physical therapy clinical research. Braz J Phys Ther 2018; 22 (03) 175-176