Changes in heavy metal levels in the oral fluid of young patients with and without plaque-induced gingivitis undergoing treatment with braces

Relevance. Research into the effects of nickel-titanium alloys and heavy metal ions on the development of inflammatory oral diseases is becoming increasingly significant in orthodontics. The relationship between toxic elements and inflammatory responses remains under-researched and controversial. Data on the connection between heavy metals and inflammatory reactions could influence the choice of orthodontic appliance materials and guide the subsequent management and monitoring of patients with braces. The question of the safe use of nickel-titanium alloy braces continues to be a relevant concern.

Purpose. To assess the levels of heavy metals in the oral fluid of young patients with braces, both in those who developed plaque-induced gingivitis and those who did not.

Materials and Methods. The study involved 50 clinically healthy patients (Groups I and II health categories) with intact teeth, including patients with compensated dental caries (isolated carious lesions – Grade I) and no periodontal diseases (PMA index <20), presenting with dental crowding and malocclusion (K07.2, K07.3). The average age of the patients was 22.1 ± 2.7 years, all of whom were undergoing treatment with metal braces. Oral fluid samples were analyzed for 12 heavy metal elements using inductively coupled plasma mass spectrometry (ICP-MS) in a laboratory setting. Additionally, lysozyme activity and oral fluid pH were measured before appliance placement and six months into orthodontic treatment.

Results. Adaptation to braces in young patients is frequently complicated by the development of gingivitis and periodontitis due to impaired oral hygiene and the mechanical pressure exerted on teeth and gums, leading to elemental imbalances. Patients with gingivitis during orthodontic treatment are particularly at risk of developing such imbalances and therefore require timely correction of their mineral metabolism.

1. Tihonov VE, Grishin MI, Mitin NE. Comparing of prevalence of anomalies of dental facial system among students living in conditions of large industrial cities and rural areas. Actual problems in dentistry. 2017;13(4):70-73 (In Russ.). doi: 10.18481/2077-7566-2017-13-4-70-73

2. Rakitskii VN, Stepkin YuI, Klepikov OV, Kurolap SA. Assessment of carcinogenic risk caused by the impact of the environmental factors on urban population health. Hygiene and Sanitation. 2021;100(3):188-195 (In Russ.). doi: 10.47470/0016-9900-2021-100-3-188-195

3. Musabekova SA. Elemental structure of hair as an indicator of natural and technological situation of the territory for the judicial-medical identification of the human. Medicine and ecology. 2018;(4):105-110 (In Russ.). Available from: https://medecol.elpub.ru/jour/article/view/85/84

4. Astarkhanova TS, Kosyreva TF, Astarkhanova FI, Astarkhanov IR, Alibalaeva LI, Osmanov IN. The impact of adverse environmental factors on the occurrence and prevalence of diseases in the Republic of Dagestan. E3S Web of Conferences, International Conference on Advances in Energy Systems and Environmental Engineering (ASEE19). 2019;116:00036. doi: 10.1051/e3sconf/201911600036.

5. Osmanova FI, Osmanov IN, Kosyreva TF. Assessment of environmental factors on the incidence of the health population of the northern regions Republic of Dagestan. The Dental Institute. 2021;(1):48-93 (In Russ). Available from: https://instom.spb.ru/catalog/magazine/15898/?view=pdf

6. Kosyreva TF, Pronyaeva AI. Effects of drinking water for hair trace element composition of children with systemic hypoplasia. Pediatric dentistry and dental prophylaxis. 2011;10(3):46–52. Available from: https://elibrary.ru/item.asp?id=16753226

7. Skalnaya MG, Demidov VA, Skalny AV. On the limits of physiological (normal) content of Ca, Mg, P, Fe, Zn and C in human hair. Microelements in Medicine. 2003;4(2):5–10 (In Russ). Available from: https://www.elibrary.ru/item.asp?id=16223666

8. Ramadan A.A. Effect of nickel and chromium on gingival tissues during orthodontic treatment: a longitudinal study. World J Orthod. 2004;5(3):230-234. Available from: https://pubmed.ncbi.nlm.nih.gov/15612342/

9. Matos de Souza R, Macedo de Menezes L. Nickel, chromium and iron levels in the saliva of patients with simulated fixed orthodontic appliances. Angle Orthod. 2008;78(2):345-50. doi: 10.2319/111806-466.1.

10. Khaneh Masjedi M, Haghighat Jahromi N, Niknam O, Hormozi E, Rakhshan V. Effects of fixed orthodontic treatment using conventional (two-piece) versus metal injection moulding brackets on hair nickel and chromium levels: a double-blind randomized clinical trial. Eur J Orthod. 2017;39(1):17-24. doi: 10.1093/ejo/cjw017

11. Mikulewicz M, Chojnacka K. Cytocompatibility of medical biomaterials containing nickel by osteoblasts: a systematic literature review. Biol Trace Elem Res. 2011;142(3):865-89. doi: 10.1007/s12011-010-8798-7

12. Khaneh Masjedi M, Niknam O, Haghighat Jahromi N, Javidi P, Rakhshan V. Effects of Fixed Orthodontic Treatment Using Conventional, Copper-Included, and Epoxy-Coated Nickel-Titanium Archwires on Salivary Nickel Levels: A Double-Blind Randomized Clinical Trial. Biol Trace Elem Res. 2016;174(1):27-31. doi: 10.1007/s12011-016-0690-7

13. Petoumenou E, Arndt M, Keilig L, Reimann S, Hoederath H, Eliades T, et al. Nickel concentration in the saliva of patients with nickel-titanium orthodontic appliances. Am J Orthod Dentofacial Orthop. 2009;135(1):59-65. doi: 10.1016/j.ajodo.2006.12.018

14. Ganidis C, Nikolaidis AK, Gogos C, Koulaouzidou EA. Determination of metal ions release from orthodontic archwires in artificial saliva using inductively coupled plasma-optical emission spectrometer (ICP-OES). Main Group Chemistry. 2023;22:201-212. doi: 10.3233/MGC-220013

15. Galeotti A, Uomo R, Spagnuolo G, Paduano S, Cimino R, Valletta R, et al. Effect of pH on in vitro biocompatibility of orthodontic miniscrew implants. Prog Orthod. 2013;14:15. doi: 10.1186/2196-1042-14-15

16. Perinetti G, Contardo L, Ceschi M, Antoniolli F, Franchi L, Baccetti T, et al. Surface corrosion and fracture resistance of two nickel-titanium-based archwires induced by fluoride, pH, and thermocycling. An in vitro comparative study. Eur J Orthod. 2012;34(1):1-9. doi: 10.1093/ejo/cjq093

17. Varma DP, Chidambaram S, Reddy KB, Vijay M, Ravindranath D, Prasad MR. Comparison of galvanic corrosion potential of metal injection molded brackets to that of conventional metal brackets with nickel-titanium and copper nickel-titanium archwire combinations. J Contemp Dent Pract. 2013;14(3):488–495. doi: 10.5005/jp-journals-10024-1350

18. Strużyńska L, Skalska J. Mechanisms Underlying Neurotoxicity of Silver Nanoparticles. Adv Exp Med Biol. 2018;1048:227-250. doi: 10.1007/978-3-319-72041-8_14.

19. Gonzalez-Carter DA, Leo BF, Ruenraroengsak P, Chen S, Goode AE, Theodorou IG et al. Silver nanoparticles reduce brain inflammation and related neurotoxicity through induction of H2S-synthesizing enzymes. Scientific Reports. 2017;7:42871. doi: 10.1038/srep42871

20. Zheng X, Huo X, Zhang Y, Wang Q, Zhang Y, Xu X. Cardiovascular endothelial inflammation by chronic coexposure to lead (Pb) and polycyclic aromatic hydrocarbons from preschool children in an e-waste recycling area. Environ Pollut. 2019;246:587-596. doi: 10.1016/j.envpol.2018.12.055

21. Chowdhury R, Ramond A, O'Keeffe LM, Shahzad S, Kunutsor SK, Muka T, et al. Environmental toxic metal contaminants and risk of cardiovascular disease: systematic review and meta-analysis. BMJ. 2018;362:k3310. doi: 10.1136/bmj.k3310

22. Yan X, Liu Y, Xie T, Liu F. α-Tocopherol protected against cobalt nanoparticles and cocl2 induced cytotoxicity and inflammation in Balb/3T3 cells. Immunopharmacol Immunotoxicol. 2018;40(2):179-185. doi: 10.1080/08923973.2018.1424901

23. Guo H, Liu H, Jian Z, Cui H, Fang J, Zuo Z, et al. Immunotoxicity of nickel: Pathological and toxicological effects. Ecotoxicol Environ Saf. 2020;15;203:111006. doi: 10.1016/j.ecoenv.2020.111006

24. You DJ, Lee HY, Taylor-Just AJ, Linder KE, Bonner JC. Sex differences in the acute and subchronic lung inflammatory responses of mice to nickel nanoparticles. Nanotoxicology. 2020;14(8):1058-1081. doi: 10.1080/17435390.2020.1808105

25. Maale G, Mohammadi D, Kennard, Srinivasaraghavan A. Early Failures of Total Knee Patients with Nickel Allergies Secondary to Carbon Fiber Debris. The Open Orthopaedics Journal. 2020;14(1):161-175. doi: 10.2174/1874325002014010161

26. Dorofeichuk VG, Potekhin PP. Possibilities of a lysozyme use in oncology. Modern technologies in medicine. 2010; (3): 80-83. (In Russ.). Available from: https://elibrary.ru/item.asp?id=15176935

27. Yanushevich OO, Dukhovskaya NE, Vavilova TP, Ostrovskaya IG, Evarnitskaya NR. Saliva indices in patients with somatic pathology. Dental Forum. 2019;(1):2-5. (In Russ.). Available from: https://elibrary.ru/item.asp?id=37307576

28. Podoplelova DV, Admakin OI, Startseva IV, Agakishieva MI, Ozden KA, Ivanenko AA. Comparative analysis of individual oral hygiene during treatment with bracket systems and aligners. Pediatric dentistry and dental prophylaxis. 2022;22(3):170-176 (In Russ.). doi: 10.33925/1683-3031-2022-22-3-170-176.

29. Vali SW, Lindahl PA. Might nontransferrin-bound iron in blood plasma and sera be a nonproteinaceous high-molecular-mass FeIII aggregate? J Biol Chem. 2022;298(12):102667. doi: 10.1016/j.jbc.2022.102667

30. Domenyuk DA, Dmitrienko SV, Vedeshina EG, Chizhikova TS, Ogonyan EA, Chizhikova TV. Assessment of the severity of dentoalveolar anomalies in terms of bioelement composition of saliva. International journal of applied and fundamental research. 2016;(1-2):153-157. (In Russ.). Available from: https://applied-research.ru/ru/article/view?id=8339

31. Yurasov VV, Morozova GD, Sadykov AR, Namiot ED, Almasry R, Lobanova YuN. Study of the relationship of tin and antimony concentrations with the crp in blood serum. Trace elements in medicine. 2022;23(1):41-46 (In Russ.). doi: 10.19112/2413-6174-2022-23-1-41-46

32. Yurasov VV, Sadykov AR, Morozova GD, Namiot ED, Lobanova YuN, Rejnyuk VL. Study of the relationship of nickel, silver, strontium, zirconium concentrations with the c-reactive protein in blood serum. Trace elements in medicine. 2022;23(3):28-36 (In Russ.). doi: 10.19112/2413-6174-2022-23-3-28-36

33. Ajsuvakova OP, Skalnaya MG, Michalke B, Tinkov AA, Serebryansky EP, Karganov MY, et al. Alteration of iron (Fe), copper (Cu), zinc (Zn), and manganese (Mn) tissue levels and speciation in rats with desferioxamine-induced iron deficiency. BioMetals. 2021;34(4):923-936. doi: 10.1007/s10534-021-00318-9

34. Morozova GD, Logvinenko AA, Grabeklis AR, Nikolaev SE, Sadykov AR, Yurasov VV, et al. Trace elements and the inflammatory process development: predictive possibilities. Molekulyarnaya Meditsina (Molecular medicine. 2024;22(1):29-34 (In Russ.). doi: 10.29296/24999490-2024-01-04

35. Arsenina OI, Popova NV, Grudyanov AI, Nadtochiy AG, Karpanova AS. Improving the diagnostic evaluation of the gingival biotype in the planning of orthodontic treatment. Clinical Dentistry (Russia). 2019;2(90):34-38 (In Russ.). doi: 10.37988/1811-153X_2019_2_34