Evaluation of Pentraxin-3 and Interleukin-6 Levels in Serum and Gingival Crevicular Fluid in Patients with Generalized Periodontitis and Periodontal Health Controls before and after Scaling and Root Planing
-
Siamak Yaghobee
,
Sadegh Hasannia
,
Fatemeh Hamidzadeh
,
Saman Valadan Tahbaz
,
Rojin Shahmohammadi
,
Farzaneh Poursafar
Abstract
Objectives: Pentraxin-3 (PTX3) and interleukin-6 (IL-6) are two of the most important inflammatory cytokines produced by cells in periodontal tissues. The present study aims to evaluate the levels of PTX3 and IL-6 in serum and gingival crevicular fluid (GCF) in patients with generalized periodontitis stages II and III, grades A and B, and periodontal health individuals before and after scaling and root planing (SRP).
Materials and Methods: In this study, 22 patients with periodontitis (12 males and 10 females) and 22 periodontal health controls (11 males and 11 females) were selected. All patients underwent full-mouth SRP. Serum and GCF samples were collected before and one month after SRP. PTX3 and IL-6 levels in serum and GCF samples were evaluated by enzyme-linked immunosorbent assay. Data analysis was performed using Mann-Whitney U and Wilcoxon tests (P<0.05).
Results: Serum levels of PTX3 were significantly higher in the periodontitis group than the controls (P<0.05). GCF PTX3 levels and serum and GCF IL-6 levels were not significantly different between the groups. Furthermore, this study did not show any significant changes in the levels of these cytokines before and after SRP.
Conclusion: Among the studied cytokines and media, only serum PTX3 levels showed a significant difference between periodontitis patients and healthy controls and could serve as a diagnostic marker of periodontal inflammation. SRP did not affect the levels of these cytokines, suggesting that other inflammatory factors may be involved in disease process. However, additional longitudinal prospective studies are needed to confirm these results.
1. Gemmell E, Marshall RI, Seymour GJ. Cytokines and prostaglandins in immune homeostasis and tissue destruction in periodontal disease. Periodontol 2000. 1997 Jun;14:112-43.
2. Bottazzi B, Vouret-Craviari V, Bastone A, De Gioia L, Matteucci C, Peri G, et al. Multimer formation and ligand recognition by the long pentraxin PTX3. Similarities and differences with the short pentraxins C-reactive protein and serum amyloid P component. J Biol Chem. 1997 Dec 26;272(52):32817-23.
3. Cieślik P, Hrycek A. Long pentraxin 3 (PTX3) in the light of its structure, mechanism of action and clinical implications. Autoimmunity. 2012 Mar;45(2):119-28.
4. Lee GW, Lee TH, Vilcek J. TSG-14, a tumor necrosis factor- and IL-1-inducible protein, is a novel member of the pentaxin family of acute phase proteins. J Immunol. 1993 Mar 1;150(5):1804-12.
5. Dagna L, Salvo F, Tiraboschi M, Bozzolo EP, Franchini S, Doglioni C, et al. Pentraxin-3 as a marker of disease activity in Takayasu arteritis. Ann Intern Med. 2011 Oct 4;155(7):425-33.
6. Bevelacqua V, Libra M, Mazzarino MC, Gangemi P, Nicotra G, Curatolo S, et al. Long pentraxin 3: a marker of inflammation in untreated psoriatic patients. Int J Mol Med. 2006 Sep;18(3):415-23.
7. Steel DM, Whitehead AS. The major acute phase reactants: C-reactive protein, serum amyloid P component and serum amyloid A protein. Immunol Today. 1994 Feb;15(2):81-8.
8. Elgendy EA, Ali SA, Zineldeen DH. Effect of local application of tea tree (Melaleuca alternifolia) oil gel on long pentraxin level used as an adjunctive treatment of chronic periodontitis: A randomized controlled clinical study. J Indian Soc Periodontol. 2013 Jul;17(4):444-8.
9. Becerik S, Öztürk VÖ, Atmaca H, Atilla G, Emingil G. Gingival crevicular fluid and plasma acute-phase cytokine levels in different periodontal diseases. J Periodontol. 2012 Oct;83(10):1304-13.
10. Nibali L, Fedele S, D'Aiuto F, Donos N. Interleukin-6 in oral diseases: a review. Oral Dis. 2012 Apr;18(3):236-43.
11. al-Humidan A, Ralston SH, Hughes DE, Chapman K, Aarden L, Russell RG, et al. Interleukin-6 does not stimulate bone resorption in neonatal mouse calvariae. J Bone Miner Res. 1991 Jan;6(1):3-8.
12. Bartold PM, Haynes DR. Interleukin-6 production by human gingival fibroblasts. J Periodontal Res. 1991 Jul;26(4):339-45.
13. Norioka K, Hara M, Harigai M, Kitani A, Hirose T, Suzuki K, et al. Production of B cell stimulatory factor-2/interleukin-6 activity by human endothelial cells. Biochem Biophys Res Commun. 1988 Jun 30;153(3):1045-50.
14. Fujihashi K, Kono Y, Beagley KW, Yamamoto M, McGhee JR, Mestecky J, et al. Cytokines and periodontal disease: immunopathological role of interleukins for B cell responses in chronic inflamed gingival tissues. J Periodontol. 1993 May;64(5 Suppl):400-6.
15. Revel M. Host defense against infections and inflammations: role of the multifunctional IL-6/IFN-beta 2 cytokine. Experientia. 1989 Jun 15;45(6):549-57.
16. D'Aiuto F, Parkar M, Andreou G, Suvan J, Brett PM, Ready D, et al. Periodontitis and systemic inflammation: control of the local infection is associated with a reduction in serum inflammatory markers. J Dent Res. 2004 Feb;83(2):156-60.
17. Shingu M, Nagai Y, Isayama T, Naono T, Nobunaga M, Nagai Y. The effects of cytokines on metalloproteinase inhibitors (TIMP) and collagenase production by human chondrocytes and TIMP production by synovial cells and endothelial cells. Clin Exp Immunol. 1993 Oct;94(1):145-9.
18. Lotz M, Guerne PA. Interleukin-6 induces the synthesis of tissue inhibitor of metalloproteinases-1/erythroid potentiating activity (TIMP-1/EPA). J Biol Chem. 1991 Feb 5;266(4):2017-20.
19. Schindler R, Mancilla J, Endres S, Ghorbani R, Clark SC, Dinarello CA. Correlations and interactions in the production of interleukin-6 (IL-6), IL-1, and tumor necrosis factor (TNF) in human blood mononuclear cells: IL-6 suppresses IL-1 and TNF. Blood. 1990 Jan 1;75(1):40-7.
20. Tilg H, Trehu E, Atkins MB, Dinarello CA, Mier JW. Interleukin-6 (IL-6) as an anti-inflammatory cytokine: induction of circulating IL-1 receptor antagonist and soluble tumor necrosis factor receptor p55. Blood. 1994 Jan 1;83(1):113-8.
21. Teles FR, Teles RP, Martin L, Socransky SS, Haffajee AD. Relationships among interleukin-6, tumor necrosis factor-α, adipokines, vitamin D, and chronic periodontitis. J Periodontol. 2012 Sep;83(9):1183-91.
22. Gani DK, Lakshmi D, Krishnan R, Emmadi P. Evaluation of C-reactive protein and interleukin-6 in the peripheral blood of patients with chronic periodontitis. J Indian Soc Periodontol. 2009 May;13(2):69-74.
23. Reinhardt RA, Masada MP, Kaldahl WB, DuBois LM, Kornman KS, Choi JI, et al. Gingival fluid IL-1 and IL-6 levels in refractory periodontitis. J Clin Periodontol. 1993 Mar;20(3):225-31.
24. Sanz M, Herrera D, Kebschull M, Chapple I, Jepsen S, Beglundh T, et al. Treatment of stage I-III periodontitis-The EFP S3 level clinical practice guideline. J Clin Periodontol. 2020 Jul;47 Suppl 22(Suppl 22):4-60.
25. Fujita Y, Ito H, Sekino S, Numabe Y. Correlations between pentraxin 3 or cytokine levels in gingival crevicular fluid and clinical parameters of chronic periodontitis. Odontology. 2012 Jul;100(2):215-21.
26. Mathew V, Varghese S, Malaiappan S, Jayakumar D. Evaluation of Pentraxins 3 in Chronic Periodontitis Patients Before and After the Treatment. Int J Med Exercise Sci. 2015;1(1):9-15.
27. Lamster IB, Grbic JT. Diagnosis of periodontal disease based on analysis of the host response. Periodontol 2000. 1995 Feb;7:83-99.
28. Temelli B, Yetkin Ay Z, Savaş HB, Aksoy F, Kumbul Doğuç D, Uskun E, et al. Circulation levels of acute phase proteins pentraxin 3 and serum amyloid A in atherosclerosis have correlations with periodontal inflamed surface area. J Appl Oral Sci. 2018;26:e20170322.
29. Pradeep AR, Kathariya R, Raghavendra NM, Sharma A. Levels of pentraxin-3 in gingival crevicular fluid and plasma in periodontal health and disease. J Periodontol. 2011 May;82(5):734-41.
30. Brüünsgaard H, Pedersen BK. Age-related inflammatory cytokines and disease. Immunol Allergy Clin North Am. 2003 Feb;23(1):15-39.
31. Keles GC, Balli U, Cetinkaya BO, Ayas B, Findik A, Keles ZP, et al. Biochemical analysis of pentraxin 3 and fibrinogen levels in experimental periodontitis model. Mediators Inflamm. 2012;2012:809801.
32. Folwaczny M, Karnesi E, Berger T, Paschos E. Clinical association between chronic periodontitis and the leukocyte extravasation inhibitors developmental endothelial locus-1 and pentraxin-3. Eur J Oral Sci. 2017 Aug;125(4):258-264.
33. Gümüş P, Nizam N, Nalbantsoy A, Özçaka Ö, Buduneli N. Saliva and serum levels of pentraxin-3 and interleukin-1β in generalized aggressive or chronic periodontitis. J Periodontol. 2014 Mar;85(3):e40-6.
34. Gheorghe DN, Popescu DM, Salan A, Boldeanu MV, Ionele CM, Pitru A, et al. Non-Surgical Periodontal Therapy Could Improve the Periodontal Inflammatory Status in Patients with Periodontitis and Chronic Hepatitis C. J Clin Med. 2021 Nov 13;10(22):5275.
35. Tasdemir Z, Oskaybas MN, Alkan AB, Cakmak O. The effects of ozone therapy on periodontal therapy: A randomized placebo-controlled clinical trial. Oral Dis. 2019 May;25(4):1195-1202.
36. Page RC. The role of inflammatory mediators in the pathogenesis of periodontal disease. J Periodontal Res. 1991 May;26(3 Pt 2):230-42.
37. Keles ZP, Keles GC, Avci B, Cetinkaya BO, Emingil G. Analysis of YKL-40 acute-phase protein and interleukin-6 levels in periodontal disease. J Periodontol. 2014 Sep;85(9):1240-6.
38. Yaghobee S, Khorsand A, Rasouli Ghohroudi AA, Sanjari K, Kadkhodazadeh M. Assessment of interleukin-1beta and interleukin-6 in the crevicular fluid around healthy implants, implants with peri-implantitis, and healthy teeth: a cross-sectional study. J Korean Assoc Oral Maxillofac Surg. 2014 Oct;40(5):220-4.
39. Goutoudi P, Diza E, Arvanitidou M. Effect of periodontal therapy on crevicular fluid interleukin-6 and interleukin-8 levels in chronic periodontitis. Int J Dent. 2012;2012:362905.
40. Marcaccini AM, Meschiari CA, Sorgi CA, Saraiva MC, de Souza AM, Faccioli LH, et al. Circulating interleukin-6 and high-sensitivity C-reactive protein decrease after periodontal therapy in otherwise healthy subjects. J Periodontol. 2009 Apr;80(4):594-602.
2. Bottazzi B, Vouret-Craviari V, Bastone A, De Gioia L, Matteucci C, Peri G, et al. Multimer formation and ligand recognition by the long pentraxin PTX3. Similarities and differences with the short pentraxins C-reactive protein and serum amyloid P component. J Biol Chem. 1997 Dec 26;272(52):32817-23.
3. Cieślik P, Hrycek A. Long pentraxin 3 (PTX3) in the light of its structure, mechanism of action and clinical implications. Autoimmunity. 2012 Mar;45(2):119-28.
4. Lee GW, Lee TH, Vilcek J. TSG-14, a tumor necrosis factor- and IL-1-inducible protein, is a novel member of the pentaxin family of acute phase proteins. J Immunol. 1993 Mar 1;150(5):1804-12.
5. Dagna L, Salvo F, Tiraboschi M, Bozzolo EP, Franchini S, Doglioni C, et al. Pentraxin-3 as a marker of disease activity in Takayasu arteritis. Ann Intern Med. 2011 Oct 4;155(7):425-33.
6. Bevelacqua V, Libra M, Mazzarino MC, Gangemi P, Nicotra G, Curatolo S, et al. Long pentraxin 3: a marker of inflammation in untreated psoriatic patients. Int J Mol Med. 2006 Sep;18(3):415-23.
7. Steel DM, Whitehead AS. The major acute phase reactants: C-reactive protein, serum amyloid P component and serum amyloid A protein. Immunol Today. 1994 Feb;15(2):81-8.
8. Elgendy EA, Ali SA, Zineldeen DH. Effect of local application of tea tree (Melaleuca alternifolia) oil gel on long pentraxin level used as an adjunctive treatment of chronic periodontitis: A randomized controlled clinical study. J Indian Soc Periodontol. 2013 Jul;17(4):444-8.
9. Becerik S, Öztürk VÖ, Atmaca H, Atilla G, Emingil G. Gingival crevicular fluid and plasma acute-phase cytokine levels in different periodontal diseases. J Periodontol. 2012 Oct;83(10):1304-13.
10. Nibali L, Fedele S, D'Aiuto F, Donos N. Interleukin-6 in oral diseases: a review. Oral Dis. 2012 Apr;18(3):236-43.
11. al-Humidan A, Ralston SH, Hughes DE, Chapman K, Aarden L, Russell RG, et al. Interleukin-6 does not stimulate bone resorption in neonatal mouse calvariae. J Bone Miner Res. 1991 Jan;6(1):3-8.
12. Bartold PM, Haynes DR. Interleukin-6 production by human gingival fibroblasts. J Periodontal Res. 1991 Jul;26(4):339-45.
13. Norioka K, Hara M, Harigai M, Kitani A, Hirose T, Suzuki K, et al. Production of B cell stimulatory factor-2/interleukin-6 activity by human endothelial cells. Biochem Biophys Res Commun. 1988 Jun 30;153(3):1045-50.
14. Fujihashi K, Kono Y, Beagley KW, Yamamoto M, McGhee JR, Mestecky J, et al. Cytokines and periodontal disease: immunopathological role of interleukins for B cell responses in chronic inflamed gingival tissues. J Periodontol. 1993 May;64(5 Suppl):400-6.
15. Revel M. Host defense against infections and inflammations: role of the multifunctional IL-6/IFN-beta 2 cytokine. Experientia. 1989 Jun 15;45(6):549-57.
16. D'Aiuto F, Parkar M, Andreou G, Suvan J, Brett PM, Ready D, et al. Periodontitis and systemic inflammation: control of the local infection is associated with a reduction in serum inflammatory markers. J Dent Res. 2004 Feb;83(2):156-60.
17. Shingu M, Nagai Y, Isayama T, Naono T, Nobunaga M, Nagai Y. The effects of cytokines on metalloproteinase inhibitors (TIMP) and collagenase production by human chondrocytes and TIMP production by synovial cells and endothelial cells. Clin Exp Immunol. 1993 Oct;94(1):145-9.
18. Lotz M, Guerne PA. Interleukin-6 induces the synthesis of tissue inhibitor of metalloproteinases-1/erythroid potentiating activity (TIMP-1/EPA). J Biol Chem. 1991 Feb 5;266(4):2017-20.
19. Schindler R, Mancilla J, Endres S, Ghorbani R, Clark SC, Dinarello CA. Correlations and interactions in the production of interleukin-6 (IL-6), IL-1, and tumor necrosis factor (TNF) in human blood mononuclear cells: IL-6 suppresses IL-1 and TNF. Blood. 1990 Jan 1;75(1):40-7.
20. Tilg H, Trehu E, Atkins MB, Dinarello CA, Mier JW. Interleukin-6 (IL-6) as an anti-inflammatory cytokine: induction of circulating IL-1 receptor antagonist and soluble tumor necrosis factor receptor p55. Blood. 1994 Jan 1;83(1):113-8.
21. Teles FR, Teles RP, Martin L, Socransky SS, Haffajee AD. Relationships among interleukin-6, tumor necrosis factor-α, adipokines, vitamin D, and chronic periodontitis. J Periodontol. 2012 Sep;83(9):1183-91.
22. Gani DK, Lakshmi D, Krishnan R, Emmadi P. Evaluation of C-reactive protein and interleukin-6 in the peripheral blood of patients with chronic periodontitis. J Indian Soc Periodontol. 2009 May;13(2):69-74.
23. Reinhardt RA, Masada MP, Kaldahl WB, DuBois LM, Kornman KS, Choi JI, et al. Gingival fluid IL-1 and IL-6 levels in refractory periodontitis. J Clin Periodontol. 1993 Mar;20(3):225-31.
24. Sanz M, Herrera D, Kebschull M, Chapple I, Jepsen S, Beglundh T, et al. Treatment of stage I-III periodontitis-The EFP S3 level clinical practice guideline. J Clin Periodontol. 2020 Jul;47 Suppl 22(Suppl 22):4-60.
25. Fujita Y, Ito H, Sekino S, Numabe Y. Correlations between pentraxin 3 or cytokine levels in gingival crevicular fluid and clinical parameters of chronic periodontitis. Odontology. 2012 Jul;100(2):215-21.
26. Mathew V, Varghese S, Malaiappan S, Jayakumar D. Evaluation of Pentraxins 3 in Chronic Periodontitis Patients Before and After the Treatment. Int J Med Exercise Sci. 2015;1(1):9-15.
27. Lamster IB, Grbic JT. Diagnosis of periodontal disease based on analysis of the host response. Periodontol 2000. 1995 Feb;7:83-99.
28. Temelli B, Yetkin Ay Z, Savaş HB, Aksoy F, Kumbul Doğuç D, Uskun E, et al. Circulation levels of acute phase proteins pentraxin 3 and serum amyloid A in atherosclerosis have correlations with periodontal inflamed surface area. J Appl Oral Sci. 2018;26:e20170322.
29. Pradeep AR, Kathariya R, Raghavendra NM, Sharma A. Levels of pentraxin-3 in gingival crevicular fluid and plasma in periodontal health and disease. J Periodontol. 2011 May;82(5):734-41.
30. Brüünsgaard H, Pedersen BK. Age-related inflammatory cytokines and disease. Immunol Allergy Clin North Am. 2003 Feb;23(1):15-39.
31. Keles GC, Balli U, Cetinkaya BO, Ayas B, Findik A, Keles ZP, et al. Biochemical analysis of pentraxin 3 and fibrinogen levels in experimental periodontitis model. Mediators Inflamm. 2012;2012:809801.
32. Folwaczny M, Karnesi E, Berger T, Paschos E. Clinical association between chronic periodontitis and the leukocyte extravasation inhibitors developmental endothelial locus-1 and pentraxin-3. Eur J Oral Sci. 2017 Aug;125(4):258-264.
33. Gümüş P, Nizam N, Nalbantsoy A, Özçaka Ö, Buduneli N. Saliva and serum levels of pentraxin-3 and interleukin-1β in generalized aggressive or chronic periodontitis. J Periodontol. 2014 Mar;85(3):e40-6.
34. Gheorghe DN, Popescu DM, Salan A, Boldeanu MV, Ionele CM, Pitru A, et al. Non-Surgical Periodontal Therapy Could Improve the Periodontal Inflammatory Status in Patients with Periodontitis and Chronic Hepatitis C. J Clin Med. 2021 Nov 13;10(22):5275.
35. Tasdemir Z, Oskaybas MN, Alkan AB, Cakmak O. The effects of ozone therapy on periodontal therapy: A randomized placebo-controlled clinical trial. Oral Dis. 2019 May;25(4):1195-1202.
36. Page RC. The role of inflammatory mediators in the pathogenesis of periodontal disease. J Periodontal Res. 1991 May;26(3 Pt 2):230-42.
37. Keles ZP, Keles GC, Avci B, Cetinkaya BO, Emingil G. Analysis of YKL-40 acute-phase protein and interleukin-6 levels in periodontal disease. J Periodontol. 2014 Sep;85(9):1240-6.
38. Yaghobee S, Khorsand A, Rasouli Ghohroudi AA, Sanjari K, Kadkhodazadeh M. Assessment of interleukin-1beta and interleukin-6 in the crevicular fluid around healthy implants, implants with peri-implantitis, and healthy teeth: a cross-sectional study. J Korean Assoc Oral Maxillofac Surg. 2014 Oct;40(5):220-4.
39. Goutoudi P, Diza E, Arvanitidou M. Effect of periodontal therapy on crevicular fluid interleukin-6 and interleukin-8 levels in chronic periodontitis. Int J Dent. 2012;2012:362905.
40. Marcaccini AM, Meschiari CA, Sorgi CA, Saraiva MC, de Souza AM, Faccioli LH, et al. Circulating interleukin-6 and high-sensitivity C-reactive protein decrease after periodontal therapy in otherwise healthy subjects. J Periodontol. 2009 Apr;80(4):594-602.
| Issue | Vol 22 (Continuously Published Article-Based) | |
| Section | Original Article | |
| DOI | https://doi.org/10.18502/fid.v22i1.17393 | |
| Keywords | ||
| Periodontitis Interleukin-6 Pentraxin 3 Gingival Crevicular Fluid Serum | ||
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Yaghobee S, Hasannia S, Hamidzadeh F, Valadan Tahbaz S, Shahmohammadi R, Poursafar F. Evaluation of Pentraxin-3 and Interleukin-6 Levels in Serum and Gingival Crevicular Fluid in Patients with Generalized Periodontitis and Periodontal Health Controls before and after Scaling and Root Planing. Front Dent. 2024;22.
