Periodontal Health and Salivary Thiol-Disulphide Homeostasis in Multiple Sclerosis Patients
Year 2024,
Volume: 31 Issue: 2, 125 - 133, 29.06.2024
Fatma Yeşim Kırzıoğlu
,
Serpil Demirci
,
Çağla Varol
,
Melike Doğan Ünlü
,
Mustafa Calapoğlu
,
Hikmet Orhan
Abstract
Objective: Multiple sclerosis (MS) is a chronic autoimmune disease in which neuroinflammation and oxidative stress play important roles in its pathology. Thiol-disulphide homeostasis is considered a marker of oxidative stress and shown to be affected in several disorders including MS. The aim of this study was to compare salivary disulfide and thiol levels in MS patients with systemically healthy controls and to evaluate whether periodontal status had an effect on thiol-disulfide homeostasis in saliva.
Material and Method: This descriptive study included a total of 184 volunteers, 92 with MS and 92 systemically healthy volunteers. Each person underwent medical, neurological and oral examinations. In saliva samples, native thiol (NT), total thiol (TT), disulphide levels were measured. The ratios of NT/TT, disulphide/NT, D/TT were calculated and compared between the patient and control groups.
Results: There was not any difference in the periodontal parameters between the MS and healthy volunteers (p>0.05), however, the biomarkers of thiol-disulphide homeostasis in saliva were significantly different between the groups (p<0.002), except for TT. When grouped according to periodontal status, although salivary parameters did not differ in both the MS and control groups (p>0.05), MS patients showed decreased NT/TT and increased disulphide/NT ratios compared to the healthy volunteers (p<0.05).
Conclusion: Our results have shown that salivary thiol-disulphide balance was shifted to the oxidative side in MS patients.
Supporting Institution
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References
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- 4. Minohara M, Matsuoka T, Li W, Osoegawa M, Ishizu T, Ohyagi Y, Kira J. Upregulation of Myeloperoxidase in Patients with Opticospinal Multiple Sclerosis: Positive Correlation with Disease Severity. J Neuroimmunol 2006;178(1-2):156‐160. doi: 10.1016/j.jneuroim.2006.05.026
- 5. Acar A, Cevik MU, Evliyaoglu O, Uzar E, Tamam Y, Arıkanoglu A, Yavuz Y, Varol S, Onder H, Taşdemir N. Evaluation of Serum Oxidant/Antioxidant Balance in Multiple Sclerosis. Acta Neurol Belg 2012;112(3):275‐80. doi: 10.1007/s13760-012-0059-4
- 6. Zhang S-Y, Gui L-N, Liu Y-Y, Shi S, Cheng Y. Oxidative Stress Marker Aberrations in Multiple Sclerosis: A Meta-Analysis Study. Front. Neurosci 2020;14:823. doi: 10.3389/fnins.2020.00823
- 7. Albandar JM, Susin C, Hughes FJ. Manifestations of Systemic Diseases and Conditions that Affect the Periodontal Attachment Apparatus: Case Definitions and Diagnostic Considerations. J Clin Periodontol 2018;45(20):171-189. doi: 10.1111/jcpe.12947
- 8. Manchery N, Henry JD, Nangle MR. A Systematic Review of Oral Health in people with Multiple Sclerosis. Community Dent Oral Epidemiol 2020;48(2):89-100. doi: 10.1111/cdoe.12512
- 9. D'Aiuto F, Nibali L, Parkar M, Patel K, Suvan J, Donos N. Oxidative Stress, Systemic Inflammation, and Severe Periodontitis. J Dent Res 2010;89(11):1241–1246. doi: 10.1177/0022034510375830
- 10. Wang J, Schipper HM, Velly AM, Mohit S, Gornitsky M. Salivary Biomarkers of Oxidative Stress: A Critical Review. Free Radic Biol Med 2015;85:95-104. doi: 10.1016/j.freeradbiomed.2015.04.005
- 11. Al-Ansari A. Is There an Association Between Multiple Sclerosis and Oral Health? Evid Based Dent 2021;22(1):44-45. doi: 10.1038/s41432-021-0159-1
- 12. He L, He T, Farrar S, Ji L, Liu T, Ma X. Antioxidants Maintain Cellular Redox Homeostasis by Elimination of Reactive Oxygen Species. Cell Physiol Biochem 2017;44(2):532-553. doi: 10.1159/000485089
- 13. Erel Ö, Erdoğan S. Thiol-disulfide Homeostasis: An Integrated Approach with Biochemical and Clinical Aspects. Turk J Med Sci 2020;50(SI-2):1728-1738. doi: 10.3906/sag-2003-64
- 14. Biswas S, Chida AS, Rahman I. Redox Modifications of Protein-Thiols: Emerging Roles in Cell Signaling. Biochem Pharmacol 2006;71:551–564. doi: 10.1016/j.bcp.2005.10.044
- 15. Vural G, Gümüşyayla Ş, Deniz O, Neşelioğlu S, Erel Ö. Relationship Between Thiol-Disulphide Homeostasis and Visual Evoked Potentials in Patients with Multiple Sclerosis. Neurol Sci 2019;40(22):385–391. doi:10.1007/s10072-018-3660-3
- 16. Ozben S, Kucuksayan E, Koseoglu M, Erel O, Neselioglu S, Ozben T. Plasma Thiol/disulphide Homeostasis Changes in Patients with Relapsing-Remitting Multiple Sclerosis. Int J Clin Pract 2021;75(7):14241. doi: 10.1111/ijcp.14241
- 17. Tayman MA, Bal C, Nural C, Günhan M. Evaluation of Dynamic Thiol/Disulfide Homeostasis in Patients with Periodontitis. Meandros Med Dent J 2021;22:41-49. doi: 10.4274/meandros.galenos.2020.14622
- 18. Thompson AJ, Banwell BL, Barkhof F, Carroll WM, Coetzee T, Comi G, Correale J et al. Diagnosis of Multiple Sclerosis: 2017 Revisions of the McDonald Criteria. Lancet Neurol 2017;17(2):162–173. doi: 10.1016/S1474-4422(17)30470-2
- 19. Kurtzke JF. Rating neurologic impairment in multiple sclerosis: An Expanded Disability Status Scale (EDSS). Neurology 1983;33(11):1444‐1452. doi: 10.1212/wnl.33.11.1444
- 20. Silness J, Loe H. Periodontal Disease in Pregnancy. II. Correlation Between Oral Hygiene and Periodontal Condition. Acta Odontol Scand 1964;22:121‐135. doi: 10.3109/00016356408993968
- 21. Loe H, Silness J. Periodontal Disease in Pregnancy. I. PrevalenceaAnd Severity. Acta Odontol Scand 1963;21:533‐51. doi: 10.3109/00016356309011240
- 22. Ainamo J, Bay I. Problems and Proposals for Recording Gingivitis and Plaque. Int Dent J 1975;25(4):229‐35. PMID: 1058834
- 23. Papapanou PN, Sanz M, Buduneli N, Dietrich T, Feres M, Fine DH, et al. Periodontitis: Consensus Report of Workgroup 2 of the 2017 World Workshop on the Classification of Periodontal and Peri-Implant Diseases and Conditions. J Clin Periodontol 2018;45(20):162-170. doi: 10.1111/jcpe.12946
- 24. Gümüş P, Nizam N, Lappin DF, Buduneli N. Saliva and Serum Levels of B‐cell Activating Factors and Tumor Necrosis Factor‐α in Patients with Periodontitis. J Periodontol 2014;85(2):270–280. doi: 10.1902/jop.2013.130117
- 25. Erel O, Neselioglu S. A Novel and Automated Assay for Thiol/Disulphide Homeostasis. Clin Biochem 2014;47(18):326-332. doi: 10.1016/j.clinbiochem.2014.09.026
- 26. Sheu JJ, Lin HC. Association Between Multiple Sclerosis and Chronic Periodontitis: A Population-Based Pilot Study. Eur J Neurol 2013;20:1053-1059. doi: 10.1111/ene.12103
- 27. Gustavsen MW, Celius EG, Moen SM, Bjølgerud A, Berg-Hansen P, et al. No Association Between Multiple Sclerosis and Periodontitis After Adjusting for Smoking Habits. Eur J Neurol 2015;22:588-590. doi: 10.1111/ene.12520
- 28. Hatipoglu H, Canbaz SK, Gungor MH, Ozden H. Expanded Disability Status Scale-Based Disability and Dental-Periodontal Conditions in Patients with Multiple Sclerosis. Med Princ and Pract 2016;25(1):49-55. doi: 10.1159/000440980
- 29. Dulamea AO, Boscaiu V, Sava MM. Disability Status and Dental Pathology in Multiple Sclerosis Patients. Mult Scler Relat Disord 2015;4(6):567-571. doi: 10.1016/j.msard.2015.09.001
- 30. Karim S, Pratibha PK, Kamath S, Bhat GS, Kamath U, et al. Superoxide Dismutase Enzyme and Thiol Antioxidants in Gingival Crevicular Fluid and Saliva. Dent Res J (Isfahan) 2012;9(3):266-272. PMID: 23087730
- 31. Demirdöğen BC, Kılıç OO, Yılmaz AA, Mungan S, Neşelioğlu S, Erel Ö. Neurocognitive Impairment in Multiple Sclerosis and its Association with Thiol-Disulfide Homeostasis and Ischemia-Modified Albumin. J Neurosci Res 2023;101(4):508-523. doi: 10.1002/jnr.25163
- 32. Arslan B, Arslan GA, Tuncer A, Karabudak R, Dinçel AS. Evaluation of Thiol Homeostasis in Multiple Sclerosis and Neuromyelitis Optica Spectrum Disorders. Front. Neurol 2021;12:716195. doi: 10.3389/fneur.2021.716195
- 33. Hauser SL, Cree BAC. Treatment of Multiple Sclerosis: A Review. Am J Med 2020;133(12):1380-1390. doi: 10.1016/j.amjmed.2020.05.049
Multipl Skleroz Hastalarında Tükürük Tiyol-Disülfit Homeostazisinin Değerlendirilmesi
Year 2024,
Volume: 31 Issue: 2, 125 - 133, 29.06.2024
Fatma Yeşim Kırzıoğlu
,
Serpil Demirci
,
Çağla Varol
,
Melike Doğan Ünlü
,
Mustafa Calapoğlu
,
Hikmet Orhan
Abstract
Amaç: Multipl skleroz (MS), patolojisinde nöroinflamasyon ve oksidatif stresin önemli rol oynadığı kronik otoimmün bir hastalıktır. Tiyol-disülfit homeostazı, oksidatif stresin bir belirteci olarak kabul edilir ve MS de dahil olmak üzere birçok hastalıktan etkilendiği gösterilmiştir. Bu çalışmanın amacı, MS hastalarında tükürük disülfit ve tiyol düzeylerini belirlemek ve sistemik olarak sağlıklı kontrollerle karşılaştırmak ve periodontal durumun tükürükte tiyol-disülfit homeostazı üzerine etkisinin olup olmadığını değerlendirmektir.
Gereç ve Yöntemler: Tanımlayıcı tipteki bu çalışmaya 92 MS hastası ve 92 sistemik olarak sağlıklı gönüllü olmak üzere toplam 184 gönüllü dahil edildi. Her bireye tıbbi, nörolojik ve sözlü muayene yapıldı. Tükürük örneklerinde nativ tiyol (NT), total tiyol (TT), disülfit düzeyleri ölçüldü. NT/TT, disülfit/NT, D/TT oranları hesaplandı ve hasta ve kontrol grupları arasında karşılaştırıldı.
Bulgular: MS ve sağlıklı gönüllüler arasında periodontal parametreler açısından herhangi bir fark yoktu (P>0.05), ancak tükürükteki tiyol-disülfit homeostazının biyobelirteçleri, TT hariç, gruplar arasında anlamlı derecede farklıydı (P<0.002). Periodontal duruma göre gruplandırıldığında tükürük parametreleri hem MS hem de kontrol gruplarında farklılık göstermemesine rağmen (P>0.05), MS hastalarında sağlıklı gönüllülere göre NT/TT'de azalma ve disülfit/NT oranlarında artış (P<0.05) gösterdi.
Sonuç: Sonuçlarımız, MS hastalarında tükürük tiyol-disülfit dengesinin oksidatif tarafa kaydığını göstermiştir.
References
- 1. Thompson AJ, Baranzini SE, Geurts J, Hemmer B, Ciccarelli O. Multiple Sclerosis. Lancet 2018;391(10130): 1622-1636. doi:10.1016/ S0140-6736(18)30481-1
- 2. van Horssen J, Witte ME, Schreibelt G, de Vries HE. Radical Changes in Multiple Sclerosis Pathogenesis. Biochim Biophys Acta 2011;1812(2):141-150. doi: 10.1016/j.bbadis.2010.06.011
- 3. Karlík M, Valkovič P, Hančinová V, Krížová L, Tóthová Ľ, Celec P. Markers of Oxidative Stress in Plasma and Saliva in Patients with Multiple Sclerosis. Clin Biochem 2015;48(1-2):24‐28. doi: 10.1016/j.clinbiochem.2014.09.023
- 4. Minohara M, Matsuoka T, Li W, Osoegawa M, Ishizu T, Ohyagi Y, Kira J. Upregulation of Myeloperoxidase in Patients with Opticospinal Multiple Sclerosis: Positive Correlation with Disease Severity. J Neuroimmunol 2006;178(1-2):156‐160. doi: 10.1016/j.jneuroim.2006.05.026
- 5. Acar A, Cevik MU, Evliyaoglu O, Uzar E, Tamam Y, Arıkanoglu A, Yavuz Y, Varol S, Onder H, Taşdemir N. Evaluation of Serum Oxidant/Antioxidant Balance in Multiple Sclerosis. Acta Neurol Belg 2012;112(3):275‐80. doi: 10.1007/s13760-012-0059-4
- 6. Zhang S-Y, Gui L-N, Liu Y-Y, Shi S, Cheng Y. Oxidative Stress Marker Aberrations in Multiple Sclerosis: A Meta-Analysis Study. Front. Neurosci 2020;14:823. doi: 10.3389/fnins.2020.00823
- 7. Albandar JM, Susin C, Hughes FJ. Manifestations of Systemic Diseases and Conditions that Affect the Periodontal Attachment Apparatus: Case Definitions and Diagnostic Considerations. J Clin Periodontol 2018;45(20):171-189. doi: 10.1111/jcpe.12947
- 8. Manchery N, Henry JD, Nangle MR. A Systematic Review of Oral Health in people with Multiple Sclerosis. Community Dent Oral Epidemiol 2020;48(2):89-100. doi: 10.1111/cdoe.12512
- 9. D'Aiuto F, Nibali L, Parkar M, Patel K, Suvan J, Donos N. Oxidative Stress, Systemic Inflammation, and Severe Periodontitis. J Dent Res 2010;89(11):1241–1246. doi: 10.1177/0022034510375830
- 10. Wang J, Schipper HM, Velly AM, Mohit S, Gornitsky M. Salivary Biomarkers of Oxidative Stress: A Critical Review. Free Radic Biol Med 2015;85:95-104. doi: 10.1016/j.freeradbiomed.2015.04.005
- 11. Al-Ansari A. Is There an Association Between Multiple Sclerosis and Oral Health? Evid Based Dent 2021;22(1):44-45. doi: 10.1038/s41432-021-0159-1
- 12. He L, He T, Farrar S, Ji L, Liu T, Ma X. Antioxidants Maintain Cellular Redox Homeostasis by Elimination of Reactive Oxygen Species. Cell Physiol Biochem 2017;44(2):532-553. doi: 10.1159/000485089
- 13. Erel Ö, Erdoğan S. Thiol-disulfide Homeostasis: An Integrated Approach with Biochemical and Clinical Aspects. Turk J Med Sci 2020;50(SI-2):1728-1738. doi: 10.3906/sag-2003-64
- 14. Biswas S, Chida AS, Rahman I. Redox Modifications of Protein-Thiols: Emerging Roles in Cell Signaling. Biochem Pharmacol 2006;71:551–564. doi: 10.1016/j.bcp.2005.10.044
- 15. Vural G, Gümüşyayla Ş, Deniz O, Neşelioğlu S, Erel Ö. Relationship Between Thiol-Disulphide Homeostasis and Visual Evoked Potentials in Patients with Multiple Sclerosis. Neurol Sci 2019;40(22):385–391. doi:10.1007/s10072-018-3660-3
- 16. Ozben S, Kucuksayan E, Koseoglu M, Erel O, Neselioglu S, Ozben T. Plasma Thiol/disulphide Homeostasis Changes in Patients with Relapsing-Remitting Multiple Sclerosis. Int J Clin Pract 2021;75(7):14241. doi: 10.1111/ijcp.14241
- 17. Tayman MA, Bal C, Nural C, Günhan M. Evaluation of Dynamic Thiol/Disulfide Homeostasis in Patients with Periodontitis. Meandros Med Dent J 2021;22:41-49. doi: 10.4274/meandros.galenos.2020.14622
- 18. Thompson AJ, Banwell BL, Barkhof F, Carroll WM, Coetzee T, Comi G, Correale J et al. Diagnosis of Multiple Sclerosis: 2017 Revisions of the McDonald Criteria. Lancet Neurol 2017;17(2):162–173. doi: 10.1016/S1474-4422(17)30470-2
- 19. Kurtzke JF. Rating neurologic impairment in multiple sclerosis: An Expanded Disability Status Scale (EDSS). Neurology 1983;33(11):1444‐1452. doi: 10.1212/wnl.33.11.1444
- 20. Silness J, Loe H. Periodontal Disease in Pregnancy. II. Correlation Between Oral Hygiene and Periodontal Condition. Acta Odontol Scand 1964;22:121‐135. doi: 10.3109/00016356408993968
- 21. Loe H, Silness J. Periodontal Disease in Pregnancy. I. PrevalenceaAnd Severity. Acta Odontol Scand 1963;21:533‐51. doi: 10.3109/00016356309011240
- 22. Ainamo J, Bay I. Problems and Proposals for Recording Gingivitis and Plaque. Int Dent J 1975;25(4):229‐35. PMID: 1058834
- 23. Papapanou PN, Sanz M, Buduneli N, Dietrich T, Feres M, Fine DH, et al. Periodontitis: Consensus Report of Workgroup 2 of the 2017 World Workshop on the Classification of Periodontal and Peri-Implant Diseases and Conditions. J Clin Periodontol 2018;45(20):162-170. doi: 10.1111/jcpe.12946
- 24. Gümüş P, Nizam N, Lappin DF, Buduneli N. Saliva and Serum Levels of B‐cell Activating Factors and Tumor Necrosis Factor‐α in Patients with Periodontitis. J Periodontol 2014;85(2):270–280. doi: 10.1902/jop.2013.130117
- 25. Erel O, Neselioglu S. A Novel and Automated Assay for Thiol/Disulphide Homeostasis. Clin Biochem 2014;47(18):326-332. doi: 10.1016/j.clinbiochem.2014.09.026
- 26. Sheu JJ, Lin HC. Association Between Multiple Sclerosis and Chronic Periodontitis: A Population-Based Pilot Study. Eur J Neurol 2013;20:1053-1059. doi: 10.1111/ene.12103
- 27. Gustavsen MW, Celius EG, Moen SM, Bjølgerud A, Berg-Hansen P, et al. No Association Between Multiple Sclerosis and Periodontitis After Adjusting for Smoking Habits. Eur J Neurol 2015;22:588-590. doi: 10.1111/ene.12520
- 28. Hatipoglu H, Canbaz SK, Gungor MH, Ozden H. Expanded Disability Status Scale-Based Disability and Dental-Periodontal Conditions in Patients with Multiple Sclerosis. Med Princ and Pract 2016;25(1):49-55. doi: 10.1159/000440980
- 29. Dulamea AO, Boscaiu V, Sava MM. Disability Status and Dental Pathology in Multiple Sclerosis Patients. Mult Scler Relat Disord 2015;4(6):567-571. doi: 10.1016/j.msard.2015.09.001
- 30. Karim S, Pratibha PK, Kamath S, Bhat GS, Kamath U, et al. Superoxide Dismutase Enzyme and Thiol Antioxidants in Gingival Crevicular Fluid and Saliva. Dent Res J (Isfahan) 2012;9(3):266-272. PMID: 23087730
- 31. Demirdöğen BC, Kılıç OO, Yılmaz AA, Mungan S, Neşelioğlu S, Erel Ö. Neurocognitive Impairment in Multiple Sclerosis and its Association with Thiol-Disulfide Homeostasis and Ischemia-Modified Albumin. J Neurosci Res 2023;101(4):508-523. doi: 10.1002/jnr.25163
- 32. Arslan B, Arslan GA, Tuncer A, Karabudak R, Dinçel AS. Evaluation of Thiol Homeostasis in Multiple Sclerosis and Neuromyelitis Optica Spectrum Disorders. Front. Neurol 2021;12:716195. doi: 10.3389/fneur.2021.716195
- 33. Hauser SL, Cree BAC. Treatment of Multiple Sclerosis: A Review. Am J Med 2020;133(12):1380-1390. doi: 10.1016/j.amjmed.2020.05.049