Evaluation of Local and Systemic Levels of Interleukin-17, Interleukin-23, and Myeloperoxidase in Response to Periodontal Therapy in Patients with Generalized Aggressive Periodontitis

Inflammation

Volumn 38, Issue 5, 2015, Pages 1959-1968

  Cifcibasi, E ^a   Koyuncuoglu, C ^b   Ciblak, M ^c   Badur, S ^c   Kasali, K ^c   Firatli, E ^a   Cintan, S ^a  

^a ISTANBUL UNIVERSITY   (Turkey)

^b ISTANBUL AYDIN UNIVERSITY   (Turkey)

^c ISTANBUL UNIVERSITY   (Turkey)

Author keywords

aggressive periodontitis; gingival crevicular fluid; IL 17; IL 23; myeloperoxidase; periodontal therapy; serum

Indexed keywords

INTERLEUKIN 17; INTERLEUKIN 23; MYELOPEROXIDASE; BIOLOGICAL MARKER; PEROXIDASE;

ADULT; AGGRESSIVE PERIODONTITIS; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GINGIVITIS; HUMAN; MALE; PROTEIN BLOOD LEVEL; SERODIAGNOSIS; BLOOD; EVALUATION STUDY; METABOLISM; PERIODONTAL POCKET; YOUNG ADULT;

ADULT; AGGRESSIVE PERIODONTITIS; BIOMARKERS; FEMALE; GINGIVAL CREVICULAR FLUID; HUMANS; INTERLEUKIN-17; INTERLEUKIN-23; MALE; PERIODONTAL POCKET; PEROXIDASE; YOUNG ADULT;

EID: 84941181704     PISSN: 03603997     EISSN: 15732576     Source Type: Journal    
DOI: 10.1007/s10753-015-0176-3     Document Type: Article

References (65)

1. Lindhe, J., N.P. Lang, and K. Karring. 2003. Periodontology and implant dentistry, 4th ed, 217. Oxford: Blackwell Munksgaard.
2. Page, R.C., and K.S. Kornman. 1997. The pathogenesis of human periodontitis: an introduction. Periodontology 2000(14): 9–11.
3. Sahingur, S.E., and R.E. Cohen. 2004. Analysis of host responses and risk for disease progression. Periodontology 2000(34): 57–583. Review.
4. Page, R.C., S. Offenbacher, H.E. Schroeder, G.J. Seymour, and K.S. Kornman. 1997. Advances in the pathogenesis of periodontitis: summary of developments, clinical implications and future directions. Periodontology 2000(14): 216–248.
5. Mosmann, T., H. Cherwinski, M. Bond, M. Giedlin, and R. Coffman. 1986. Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins. Journal of Immunology 136: 2348–2357.
6. Houri-Haddad, Y., A. Wilensky, and L. Shapira. 2007. T-cell phenotype as a risk factor for periodontal disease. Periodontology 2000(45): 67–75.
7. Harrington, L.E., P.R. Mangan, and C.T. Weaver. 2006. Expanding the effector CD4 T-cell repertoire: the Th17 lineage. Current Opinion in Immunology 18: 349–356.
8. Steinman, L. 2007. A brief history of T(H)17, the first major revision in the T(H)1/T(H)2 hypothesis of T cell-mediated tissue damage. Nature Medicine 13: 139–145. Review.
9. Tesmer, L.A., S.K. Lundy, S. Sarkar, and D.A. Fox. 2008. Th17 cells in human disease. Immunological Reviews 223: 87–113. doi:10.1111/j.1600-065X.2008.00628.x.
10. Ferretti, S., O. Bonneau, G.R. Dubois, C.E. Jones, and A. Trifilieff. 2003. IL-17, produced by lymphocytes and neutrophils, is necessary for lipopolysaccharide-induced airway neutrophilia: IL-15 as a possible trigger. The Journal of Immunology 170: 2106–2112.
11. Kramer, J.M., and S.L. Gaffen. 2007. Interleukin-17: a new paradigm in inflammation, autoimmunity, and therapy. Journal of Periodontology 78: 1083–1093.
12. Johnson, R.B., N. Wood, and F.G. Serio. 2004. Interleukin-11 and IL-17 and the pathogenesis of periodontal disease. Journal of Periodontology 75: 37–43.
13. Eskan, M.A., R. Jotwani, T. Abe, J. Chmelar, J.H. Lim, S. Liang, P.A. Ciero, J.L. Krauss, F. Li, M. Rauner, L.C. Hofbauer, E.Y. Choi, K.J. Chung, A. Hashim, M.A. Curtis, T. Chavakis, and G. Hajishengallis. 2012. The leukocyte integrin antagonist Del-1 inhibits IL-17-mediated inflammatory bone loss. Nature Immunology 13: 465–473. doi:10.1038/ni.2260.
14. Ito, H., T. Honda, H. Domon, T. Oda, T. Okui, R. Amanuma, T. Nakajima, and K. Yamazaki. 2005. Gene expression analysis of the CD4+ T-cell clones derived from gingival tissues of periodontitis patients. Oral Microbiology and Immunology 20: 382–386.
15. Vernal, R., N. Dutzan, A. Chaparro, J. Puente, M. Antonieta Valenzuela, and J. Gamonal. 2005. Levels of interleukin-17 in gingival crevicular fluid and in supernatants of cellular cultures of gingival tissue from persons with chronic periodontitis. Journal of Clinical Periodontology 32: 383–389.
16. Schenkein, H.A., T.E. Koertge, C.N. Brooks, R. Sabatini, D.E. Purkall, and J.G. Tew. 2010. IL-17 in sera from patients with aggressive periodontitis. Journal of Dental Research 89: 943. doi:10.1177/0022034510369297.
17. Ozcaka, O., A. Nalbantsoy, and N. Buduneli. 2011. Interleukin-17 and interleukin-18 levels in saliva and plasma of patients with chronic periodontitis. Journal of Periodontal Research 46: 592–598.
18. Lester, S.R., J.L. Bain, R.B. Johnson, and F.G. Serio. 2007. Gingival concentrations of interleukin-23 and -17 at healthy sites and at sites of clinical attachment loss. Journal of Periodontology 78: 1545–1550.
19. Zhao, L., Y. Zhou, Y. Xu, Y. Sun, L. Li, and W. Chen. 2011. Effect of non-surgical periodontal therapy on the levels of Th17/Th1/Th2 cytokines and their transcription factors in Chinese chronic periodontitis patients. Journal of Clinical Periodontology 38: 509–516.
20. Duarte, P.M., M. da Rocha, E. Sampaio, M.J. Mestnik, M. Feres, L.C. Figueiredo, M.F. Bastos, and M. Faveri. 2010. Serum levels of cytokines in subjects with generalized chronic and aggressive periodontitis before and after non-surgical periodontal therapy: a pilot study. Journal of Periodontology 81: 1056–1063.
21. Borch, T.S., M. Lobner, K. Bendtzen, P. Holmstrup, and C.H. Nielsen. 2009. Decreased interleukin-2 responses to Fusobacterium nucleatum and Porphyromonas gingivalis in generalized aggressive periodontitis. Journal of Periodontology 80: 800–887.
22. Takahashi, K., T. Azuma, H. Motohira, D.F. Kinane, and S. Kitetsu. 2005. The potential role of interleukin-17 in the immunopathology of periodontal disease. Journal of Clinical Periodontology 32: 369–374.
23. Beklen, A., T. Sorsa, and Y. Konttinen. 2009. Toll-like receptors 2 and 5 in human gingival epithelial cells co-operate with T cell cytokine interleukin-17. Oral Microbiology and Immunology 24: 38–42.
24. Sato, K., A. Suematsu, K. Okamoto, A. Yamaguchi, Y. Morishita, Y. Kadono, S. Tanaka, T. Kodama, S. Akira, Y. Iwakura, D.J. Cua, and H. Takayanagi. 2006. Th17 functions as an osteoclastogenic helper T cell subset that links T cell activation and bone destruction. The Journal of Experimental Medicine 203: 2673–2682.
25. Ohyama, H., N. Kato-Kogoe, A. Kuhara, F. Nishimura, K. Nakasho, K. Yamanegi, N. Yamada, M. Hata, J. Yamane, and N. Terada. 2009. The involvement of IL-23 and the Th17 pathway in periodontitis. Journal of Dental Research 88: 633–638.
26. Beklen, A., M. Ainola, M. Hukkanen, C. Gurgan, T. Sorsa, and Y.T. Konttinen. 2007. MMPs, IL-1, and TNF are regulated by IL-17 in periodontitis. Journal of Dental Research 86: 347–351.
27. Buduneli, N., E. Buduneli, and N. Kutukculer. 2009. Interleukin-17, RANKL, and osteoprotegerin levels in gingival crevicular fluid from smoking and nonsmoking patients with chronic periodontitis during initial periodontal treatment. Journal of Periodontology 80: 1274–1280.
28. Zelante, T., A. De Luca, P. Bonifazi, C. Montagnoli, S. Bozza, S. Moretti, M.L. Belladonna, C. Vacca, C. Conte, P. Mosci, F. Bistoni, P. Puccetti, R.A. Kastelein, M. Kopf, and L. Romani. 2007. IL-23 and the Th17 pathway promote inflammation and impair antifungal immune resistance. European Journal of Immunology 37: 2695–2706.
29. Watford, W.T., B.D. Hissong, J.H. Bream, Y. Kanno, L. Muul, and J.J. O’Shea. 2004. Signaling by IL-12 and IL-23 and the immunoregulatory roles of STAT4. Immunological Reviews 202: 139–156.
30. Kastelein, R.A., C.A. Hunter, and D.J. Cua. 2007. Discovery and biology of IL-23 and IL-27: related but functionally distinct regulators of inflammation. Annual Review of Immunology 25: 221–42. Review.
31. Tan, Z.Y., K.W. Bealgey, Y. Fang, Y.M. Gong, and S. Bao. 2009. Interleukin-23: immunological roles and clinical implications. The International Journal of Biochemistry & Cell Biology 41: 733–735. Review.
32. Iwakura, Y., and H. Ishigame. 2006. The IL-23/IL-17 axis in inflammation. Journal of Clinical Investigation 116: 1218–1222.
33. Yu, J.J., M.J. Ruddy, G.C. Wong, C. Sfintescu, P.J. Baker, J.B. Smith, R.T. Evans, and S.L. Gaffen. 2007. An essential role for IL-17 in preventing pathogen-initiated bone destruction: recruitment of neutrophils to inflamed bone requires IL-17 receptor-dependent signals. Blood 109: 3794–3802.
34. Sorsa, T., L. Tjäderhane, Y.T. Konttinen, A. Lauhio, T. Salo, H.M. Lee, L.M. Golub, D.L. Brown, and P. Mäntylä. 2006. Matrix metalloproteinases: contribution to pathogenesis, diagnosis and treatment of periodontal inflammation. Annals of Medicine 38: 306–321.
35. Bradley, P.P., D.A. Priebat, R.D. Christensen, and G. Rothstein. 1982. Measurement of cutaneous inflammation: estimation of neutrophil content with an enzyme marker. Journal of Investigative Dermatology 78: 206–209.
36. Travis, J., R. Pike, T. Imamura, and J. Potempa. 1994. The role of proteolytic enzymes in the development of pulmonary emphysema and periodontal disease. American Journal of Respiratory and Critical Care Medicine 150: 143–146. Review.
37. Yamalik, N., F. Caglayan, K. Kilinc, A. Kilinc, and C. Tumer. 2000. The importance of data presentation regarding gingival crevicular fluid myeloperoxidase and elastase-like activity in periodontal disease and health status. Journal of Periodontology 71: 460–467.
38. Hernandez, M., J. Gamonal, T. Tervahartiala, P. Mäntylä, O. Rivera, A. Dezerega, N. Dutzan, and T. Sorsa. 2010. Associations between matrix metalloproteinase-8 and -14 and myeloperoxidase in gingival crevicular fluid from subjects with progressive chronic periodontitis: a longitudinal study. Journal of Periodontology 81: 1644–1652.
39. Marcaccini, A.M., C.A. Meschiari, L.R. Zuardi, T.S. de Sousa, M. Taba Jr., J.M. Teofilo, A.L. Jacob-Ferreira, J.E. Tanus-Santos, A.B. Novaes Jr., and R.F. Gerlach. 2010. Gingival crevicular fluid levels of MMP-8, MMP-9, TIMP-2, and MPO decrease after periodontal therapy. Journal of Clinical Periodontology 37: 180–190.
40. Ozcaka, O., N. Bicakci, P. Pussinen, T. Sorsa, T. Köse, and N. Buduneli. 2011. Smoking and matrix metalloproteinases, neutrophil elastase and myeloperoxidase in chronic periodontitis. Oral Diseases 17: 68–76.
41. Meschiari, C.A., A.M. Marcaccini, B.C. Santos Moura, L.R. Zuardi, J.E. Tanus-Santos, and R.F. Gerlach. 2013. Salivary MMPs, TIMPs, and MPO levels in periodontal disease patients and controls. Clinical Chimica Acta 421: 140–146.
42. Holzhausen, M., L.C. Spolidorio, and N. Vergnolle. 2005. Proteinase-activated receptor-2 (PAR2) agonist causes periodontitis in rats. Journal of Dental Research 84: 154–159.
43. Gomes, D.A., J.R. Pires, E.P. Zuza, M.N. Muscara, B.S. Herrera, L.C. Spolidorio, B.E. Toledo, and D.M. Spolidorio. 2009. Myeloperoxidase as inflammatory marker of periodontal disease: experimental study in rats. Immunological Investigations 38: 117–122. doi:10.1080/08820130802457503.
44. Akman, S., V. Canakci, A. Kara, U. Tozoglu, T. Arabaci, and I.M. Dagsuyu. 2013. Therapeutic effects of alpha lipoic acid and vitamin C on alveolar bone resorption after experimental periodontitis in rats: a biochemical, histochemical, and stereologic study. Journal of Periodontology 84: 666–674.
45. Sorsa, T., L. Tjäderhane, and T. Salo. 2004. Matrix metalloproteinases (MMPs) in oral diseases. Oral Diseases 10: 311–318.
46. Queiroz-Junior, C.M., C.M. Pacheco, A.H. Fonsec, A. Klein, M.V. Caliari, and J.N. de Francischi. 2009. Myeloperoxidase content is a marker of systemic inflammation in a chronic condition: the example given by the periodontal disease in rats. Mediators of Inflammation 2009: 760837. doi:10.1155/2009/760837.
47. Kaner, D., J.P. Bernimoulin, B.M. Kleber, W.R. Heizmann, and A. Friedmann. 2006. Gingival crevicular fluid levels of calprotectin and myeloperoxidase during therapy for generalized aggressive periodontitis. Journal of Periodontal Research 41: 132–139.
48. Ay, Z.Y., G. Yılmaz, M. Ozdem, H. Koçak, R. Sütçü, E. Uskun, M.Ö. Tonguç, and F.Y. Kırzıoğlu. 2012. The gingival crevicular fluid levels of interleukin-11 and interleukin-17 in patients with aggressive periodontitis. Journal of Periodontology 83: 1425–1431.
49. Himani, G.S., M.L. Prabhuji, and B.V. Karthikeyan. 2014. Gingival crevicular fluid and interleukin-23 concentration in systemically healthy subjects: their relationship in periodontal health and disease. Journal of Periodontal Research 49: 237–245.
50. Armitage, G.C. 1999. Development of a classification system for periodontal diseases and conditions. Annals of Periodontology 4: 1–6.
51. BMI classification. Global database on body mass index. World Health Organization. 2006. Retrieved July 27, 2012. http://apps.who.int/bmi/index.jsp?introPage=intro_3.html
52. Silness, J., and H. Löe. 1964. Periodontal disease in pregnancy. II. Correlation between oral hygiene and periodontal condition. Acta Odontologica Scandinavica 22: 121–135.
53. Mendonca, A.C., V.R. Santos, F.V. Ribeiro, J.A. Lima, T.S. Miranda, M. Feres, and P.M. Duarte. 2012. Surgical and non-surgical therapy with systemic antimicrobials for residual pockets in type 2 diabetics with chronic periodontitis: a pilot study. Journal of Clinical Periodontology 39: 368–376. doi:10.1111/j.1600-051X.2012.01860.x.
54. Graves, D. 2008. Cytokines that promote periodontal tissue destruction. Journal of Periodontology 79: 1585–1591. doi:10.1902/jop.2008.080183. Review.
55. Chabaud, M., F. Fossiez, J. Taupin, and P. Miossec. 1998. Enhancing effect of IL-17 on IL-1-induced IL-6 and leukemia inhibitory factor production by rheumatoid arthritis synoviocytes and its regulation by Th2 cytokines. The Journal of Immunology 161: 409–414.
56. Matusevicius, D., P. Kivisakk, B. He, N. Kostulas, V. Ozenci, S. Fredrikson, and H. Link. 1999. Interleukin-17 mRNA expression in blood and CSF mononuclear cells is augmented in multiple sclerosis. Multiple Sclerosis Journal 5: 101–104.
57. Mendonca, A.C., V.R. Santos, F.V. Ribeiro, J.A. Lima, T.S. Miranda, M. Feres, and P.M. Duarte. 2012. Surgical and non-surgical therapy with systemic antimicrobials for residual pockets in type 2 diabetics with chronic periodontitis: a pilot study. Journal of Clinical Periodontology 39: 368–376.
58. Santos, V.R., F.V. Ribeiro, J.A. Lima, T.S. Miranda, M. Feres, M.F. Bastos, and P.M. Duarte. 2012. Partial- and full-mouth scaling and root planing in type 2 diabetic subjects: a 12-mo follow-up of clinical parameters and levels of cytokines and osteoclastogenesis-related factors. Journal of Periodontal Research 47: 45–54.
59. de Ribeiro, F.V., A.C. Mendonca, V.R. Santos, M.F. Bastos, L.C. Figueiredo, and P.M. Duarte. 2011. Cytokines and bone-related factors in systemically healthy patients with chronic periodontitis and patients with type 2 diabetes and chronic periodontitis. Journal of Periodontology 82: 1187–1196. doi:10.1902/jop.2011.100643.
60. Kulkarni, C., and D.F. Kinane. 2014. Host response in aggressive periodontitis. Periodontology 2000 65(1): 79–91.
61. Smith, Q.T., J.E. Hinrichs, and R.S. Melnyk. 1986. Gingival crevicular fluid myeloperoxidase at periodontitis sites. Journal of Periodontal Research 21: 45–55.
62. Cao, C.F., and Q.T. Smith. 1989. Crevicular fluid myeloperoxidase at healthy, gingivitis and periodontitis sites. Journal of Clinical Periodontology 16: 17–20.
63. Wei, P.F., K.Y. Ho, Y.P. Ho, Y.M. Wu, Y.H. Yang, and C.C. Tsai. 2004. The investigation of glutathione peroxidase, lactoferrin, myeloperoxidase and interleukin-1 beta in gingival crevicular fluid: implications for oxidative stress in human periodontal diseases. Journal of Periodontal Research 39: 287–293.
64. Nizam, N., P. Gumus, J. Pitkänen, T. Tervahartiala, T. Sorsa, and N. Buduneli. 2014. Serum and salivary matrix metalloproteinases, neutrophil elastase, myeloperoxidase in patients with chronic or aggressive periodontitis. Inflammation 37: 1771–1778. doi:10.1007/s10753-014-9907-0.
65. Shaddox, L.M., P.F. Gonçalves, A. Vovk, N. Allin, H. Huang, W. Hou, et al. 2013. LPS-induced inflammatory response after therapy of aggressive periodontitis. Journal of Dental Research 92(8): 702–708.