Skip to main content

Advertisement

SpringerLink
Log in

Expressions of Interleukin-1β and Interleukin-6 Within Aortas and Uteri of Rats with Various Severities of Ligature-Induced Periodontitis

  • Published:
Inflammation Aims and scope Submit manuscript

Abstract

To investigate the associations of periodontitis with histological lesions in some other organs, various severities of periodontitis were induced in rats by 3/0 silk ligatures tied around different numbers of their molar necks. Six weeks after the initial placement of ligatures, all rats were sacrificed by an anaesthetic overdose. The distances from the cemento-enamel junction to the alveolar bone crest within the placement zone of the ligature and their contralateral zone in groups L2 and L3 were measured. The levels of interleukin (IL)-1β and IL-6 in serum were assayed by enzyme-linked immunosorbent assay techniques, and those within aortas and uteri were measured by real-time polymerase chain reaction and by immunohistochemistry. We divided the ligature-induced periodontitis models into mild, moderate and severe rat periodontitis and observed that although no association between periodontitis and the serum concentrations of IL-1β was detected, the differences in the severity of rat periodontitis led to varying degrees of elevated expressions of IL-1β and IL-6 within aortas and uteri.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Ross, R. 1999. Atherosclerosis—an inflammatory disease. The New England Journal of Medicine 340(2): 115–126.

    Article  PubMed  CAS  Google Scholar 

  2. Epstein, S.E., Y.F. Zhou, and J. Zhu. 1999. Infection and atherosclerosis: Emerging mechanistic paradigms. Circulation 100(4): e20–e28.

    PubMed  CAS  Google Scholar 

  3. Ford, P.J., K. Yamazaki, and G.J. Seymour. 2007. Cardiovascular and oral disease interactions: What is the evidence? Primary Dental Care 14(2): 59–66.

    Article  PubMed  Google Scholar 

  4. Li, X., K.M. Kolltveit, L. Tronstad, and I. Olsen. 2000. Systemic diseases caused by oral infection. Clinical Microbiology Reviews 13(4): 547–558.

    Article  PubMed  CAS  Google Scholar 

  5. Cullinan, M.P., P.J. Ford, and G.J. Seymour. 2009. Periodontal disease and systemic health: Current status. Australian Dental Journal 54(Suppl 1): S62–S69.

    Article  PubMed  Google Scholar 

  6. Manau, C., A. Echeverria, A. Agueda, A. Guerrero, and J.J. Echeverria. 2008. Periodontal disease definition may determine the association between periodontitis and pregnancy outcomes. Journal of Clinical Periodontology 35(5): 385–397.

    Article  PubMed  Google Scholar 

  7. Romero, R., and M. Mazor. 1988. Infection and preterm labor. Clinical Obstetrics and Gynecology 31(3): 553–584.

    Article  PubMed  CAS  Google Scholar 

  8. Clothier, B., M. Stringer, and M.K. Jeffcoat. 2007. Periodontal disease and pregnancy outcomes: Exposure, risk and intervention. Best Practice & Research. Clinical Obstetrics & Gynaecology 21(3): 451–466.

    Article  CAS  Google Scholar 

  9. Goepfert, A.R., M.K. Jeffcoat, W.W. Andrews, O. Faye-Petersen, S.P. Cliver, R.L. Goldenberg, and J.C. Hauth. 2004. Periodontal disease and upper genital tract inflammation in early spontaneous preterm birth. Obstetrics and Gynecology 104(4): 777–783.

    Article  PubMed  Google Scholar 

  10. Srinivas, S.K., M.D. Sammel, D.M. Stamilio, B. Clothier, M.K. Jeffcoat, S. Parry, G.A. Macones, M.A. Elovitz, and J. Metlay. 2009. Periodontal disease and adverse pregnancy outcomes: Is there an association? American Journal of Obstetrics & Gynecology 200(5): 497.e1–497.e8.

    Article  Google Scholar 

  11. Parahitiyawa, N.B., L.J. Jin, W.K. Leung, W.C. Yam, and L.P. Samaranayake. 2009. Microbiology of odontogenic bacteremia: Beyond endocarditis. Clinical Microbiology Reviews 22(1): 46–64. Table of Contents.

    Article  PubMed  CAS  Google Scholar 

  12. Preshaw, P.M. 2009. Definitions of periodontal disease in research. Journal of Clinical Periodontology 36(1): 1–2.

    Article  PubMed  Google Scholar 

  13. Klausen, B. 1991. Microbiological and immunological aspects of experimental periodontal disease in rats: A review article. The Journal of Periodontology 62(1): 59–73.

    CAS  Google Scholar 

  14. Tonetti, M.S., and N. Claffey. 2005. Advances in the progression of periodontitis and proposal of definitions of a periodontitis case and disease progression for use in risk factor research. Group C consensus report of the 5th European Workshop in Periodontology. Journal of Clinical Periodontology 32(Suppl 6): 210–213.

    Article  PubMed  Google Scholar 

  15. Page, R.C., and P.I. Eke. 2007. Case definitions for use in population-based surveillance of periodontitis. The Journal of Periodontology 78(7 Suppl): 1387–1399.

    Article  Google Scholar 

  16. Li, Z.Y., G.B. Xu, and T.A. Xia. 2006. Prevalence rate of metabolic syndrome and dyslipidemia in a large professional population in Beijing. Atherosclerosis 184(1): 188–192.

    Article  PubMed  CAS  Google Scholar 

  17. Beck, J., R. Garcia, G. Heiss, P.S. Vokonas, and S. Offenbacher. 1996. Periodontal disease and cardiovascular disease. The Journal of Periodontology 67(10 Suppl): 1123–1137.

    CAS  Google Scholar 

  18. Anderson, J.L., J.F. Carlquist, J.B. Muhlestein, B.D. Horne, and S.P. Elmer. 1998. Evaluation of C-reactive protein, an inflammatory marker, and infectious serology as risk factors for coronary artery disease and myocardial infarction. Journal of the American College of Cardiology 32(1): 35–41.

    Article  PubMed  CAS  Google Scholar 

  19. Beck, J.D., and S. Offenbacher. 2002. Relationships among clinical measures of periodontal disease and their associations with systemic markers. Annals of Periodontology 7(1): 79–89.

    Article  PubMed  Google Scholar 

  20. Golub, L.M., J.B. Payne, R.A. Reinhardt, and G. Nieman. 2006. Can systemic diseases co-induce (not just exacerbate) periodontitis? A hypothetical “two-hit” model. Journal of Dental Research 85(2): 102–105.

    Article  PubMed  CAS  Google Scholar 

  21. Buhlin, K., A. Gustafsson, A.G. Pockley, J. Frostegard, and B. Klinge. 2003. Risk factors for cardiovascular disease in patients with periodontitis. European Heart Journal 24(23): 2099–2107.

    Article  PubMed  Google Scholar 

  22. Goldenberg, R.L., and J.F. Culhane. 2006. Preterm birth and periodontal disease. The New England Journal of Medicine 355(18): 1925–1927.

    Article  PubMed  CAS  Google Scholar 

  23. Vidal, F., C.M. Figueredo, I. Cordovil, and R.G. Fischer. 2009. Periodontal therapy reduces plasma levels of interleukin-6, C-reactive protein, and fibrinogen in patients with severe periodontitis and refractory arterial hypertension. The Journal of Periodontology 80(5): 786–791.

    Article  CAS  Google Scholar 

  24. Loos, B.G., J. Craandijk, F.J. Hoek, P.M. Wertheim-van Dillen, and U. van der Velden. 2000. Elevation of systemic markers related to cardiovascular diseases in the peripheral blood of periodontitis patients. The Journal of Periodontology 71(10): 1528–1534.

    Article  CAS  Google Scholar 

  25. Page, R.C. 1991. The role of inflammatory mediators in the pathogenesis of periodontal disease. Journal of Periodontal Research 26(3 Pt 2): 230–242.

    Article  PubMed  CAS  Google Scholar 

  26. Kweider, M., G.D. Lowe, G.D. Murray, D.F. Kinane, and D.A. McGowan. 1993. Dental disease, fibrinogen and white cell count; links with myocardial infarction? Scottish Medical Journal 38(3): 73–74.

    PubMed  CAS  Google Scholar 

  27. Ebersole, J.L., R.L. Machen, M.J. Steffen, and D.E. Willmann. 1997. Systemic acute-phase reactants, C-reactive protein and haptoglobin, in adult periodontitis. Clinical and Experimental Immunology 107(2): 347–352.

    Article  PubMed  CAS  Google Scholar 

  28. Pussinen, P.J., and K. Mattila. 2004. Periodontal infections and atherosclerosis: Mere associations? Current Opinion in Lipidology 15(5): 583–588.

    Article  PubMed  CAS  Google Scholar 

  29. Mengel, R., M. Bacher, and L. Flores-De-Jacoby. 2002. Interactions between stress, interleukin-1beta, interleukin-6 and cortisol in periodontally diseased patients. Journal of Clinical Periodontology 29(11): 1012–1022.

    Article  PubMed  CAS  Google Scholar 

  30. Marcaccini, A.M., C.A. Meschiari, C.A. Sorgi, M.C. Saraiva, A.M. de Souza, L.H. Faccioli, J.E. Tanus-Santos, A.B. Novaes, and R.F. Gerlach. 2009. Circulating interleukin-6 and high-sensitivity C-reactive protein decrease after periodontal therapy in otherwise healthy subjects. The Journal of Periodontology 80(4): 594–602.

    Article  CAS  Google Scholar 

  31. Heimonen, A., S.J. Janket, R. Kaaja, L.K. Ackerson, P. Muthukrishnan, and J.H. Meurman. 2009. Oral inflammatory burden and preterm birth. The Journal of Periodontology 80(6): 884–891.

    Article  Google Scholar 

  32. Fitzsimmons, T.R., A.E. Sanders, P.M. Bartold, and G.D. Slade. 2010. Local and systemic biomarkers in gingival crevicular fluid increase odds of periodontitis. Journal of Clinical Periodontology 37(1): 30–36.

    Article  PubMed  CAS  Google Scholar 

  33. Romero, R., J. Espinoza, L.F. Goncalves, J.P. Kusanovic, L.A. Friel, and J.K. Nien. 2006. Inflammation in preterm and term labour and delivery. Seminars in Fetal & Neonatal Medicine 11(5): 317–326.

    Article  Google Scholar 

  34. Shimizu, K., R.N. Mitchell, and P. Libby. 2006. Inflammation and cellular immune responses in abdominal aortic aneurysms. Arteriosclerosis, Thrombosis, and Vascular Biology 26(5): 987–994.

    Article  PubMed  CAS  Google Scholar 

  35. Sprague, A.H., and R.A. Khalil. 2009. Inflammatory cytokines in vascular dysfunction and vascular disease. Biochemical Pharmacology 78(6): 539–552.

    Article  PubMed  CAS  Google Scholar 

  36. Saito, S. 2000. Cytokine network at the feto-maternal interface. Journal of Reproductive Immunology 47(2): 87–103.

    Article  PubMed  CAS  Google Scholar 

  37. Dudley, D.J. 1999. Immunoendocrinology of preterm labor: The link between corticotropin-releasing hormone and inflammation. American Journal of Obstetrics and Gynecology 180(1 Pt 3): S251–S256.

    Article  PubMed  CAS  Google Scholar 

  38. Wassmann, S., M. Stumpf, K. Strehlow, A. Schmid, B. Schieffer, M. Bohm, and G. Nickenig. 2004. Interleukin-6 induces oxidative stress and endothelial dysfunction by overexpression of the angiotensin II type 1 receptor. Circulation Research 94(4): 534–541.

    Article  PubMed  CAS  Google Scholar 

  39. Libby, P., P.M. Ridker, and A. Maseri. 2002. Inflammation and atherosclerosis. Circulation 105(9): 1135–1143.

    Article  PubMed  CAS  Google Scholar 

  40. Abeywardena, M.Y., W.R. Leifert, K.E. Warnes, J.N. Varghese, and R.J. Head. 2009. Cardiovascular biology of interleukin-6. Current Pharmaceutical Design 15(15): 1809–1821.

    Article  PubMed  CAS  Google Scholar 

  41. Sanavi, F., M.A. Listgarten, F. Boyd, K. Sallay, and A. Nowotny. 1985. The colonization and establishment of invading bacteria in periodontium of ligature-treated immunosuppressed rats. The Journal of Periodontology 56(5): 273–280.

    CAS  Google Scholar 

  42. Livak, K.J., and T.D. Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25(4): 402–408.

    Article  PubMed  CAS  Google Scholar 

  43. Murtha, A.P., P.C. Greig, C.E. Jimmerson, and W.N. Herbert. 1998. Maternal serum interleukin-6 concentration as a marker for impending preterm delivery. Obstetrics and Gynecology 91(2): 161–164.

    Article  PubMed  CAS  Google Scholar 

  44. Turhan, N.O., A. Karabulut, and B. Adam. 2000. Maternal serum interleukin 6 levels in preterm labor: Prediction of admission-to-delivery interval. Journal of Perinatal Medicine 28(2): 133–139.

    Article  PubMed  CAS  Google Scholar 

  45. Lencki, S.G., M.B. Maciulla, and G.S. Eglinton. 1994. Maternal and umbilical cord serum interleukin levels in preterm labor with clinical chorioamnionitis. American Journal of Obstetrics and Gynecology 170(5 Pt 1): 1345–1351.

    PubMed  CAS  Google Scholar 

  46. Feldman, J.D., E.N. Kontaxis, and M.P. Sherman. 1985. Congenital bacteremia due to Capnocytophaga. Pediatric Infectious Disease 4(4): 415–416.

    Article  PubMed  CAS  Google Scholar 

  47. Katz, J., N. Chegini, K.T. Shiverick, and R.J. Lamont. 2009. Localization of P. gingivalis in preterm delivery placenta. Journal of Dental Research 88(6): 575–578.

    Article  PubMed  CAS  Google Scholar 

  48. Sehringer, B., W.R. Schafer, B. Wetzka, W.R. Deppert, R. Brunner-Spahr, E. Benedek, and H.P. Zahradnik. 2000. Formation of proinflammatory cytokines in human term myometrium is stimulated by lipopolysaccharide but not by corticotropin-releasing hormone. The Journal of Clinical Endocrinology and Metabolism 85(12): 4859–4865.

    Article  PubMed  CAS  Google Scholar 

  49. Steinborn, A., A. Niederhut, C. Solbach, R. Hildenbrand, C. Sohn, and M. Kaufmann. 1999. Cytokine release from placental endothelial cells, a process associated with preterm labour in the absence of intrauterine infection. Cytokine 11(1): 66–73.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We are grateful to Mr. Qinghai Yang and Mrs. Lijie Wang for their excellent technical assistance. This work was supported by National Natural Science Foundation of China (Grant No. 30973326), the Professor Academic Development Grants of Fujian Medical University (No. JS06104) and the Key Disciplines Research Foundation (No. 2008-39) from School of Stomatology, Fujian Medical University.

Author information

Authors and Affiliations

  1. School and Hospital of Stomatology, Fujian Medical University, 246 Yangqiao Zhong Road, Fuzhou, Fujian, 350002, People’s Republic of China

    Shouzhi Ma, Jianbin Guo, Xiaoqing You, Wen Xia & Fuhua Yan

Authors
  1. Shouzhi Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jianbin Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xiaoqing You
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Wen Xia
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Fuhua Yan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Fuhua Yan.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ma, S., Guo, J., You, X. et al. Expressions of Interleukin-1β and Interleukin-6 Within Aortas and Uteri of Rats with Various Severities of Ligature-Induced Periodontitis. Inflammation 34, 260–268 (2011). https://doi.org/10.1007/s10753-010-9232-1

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10753-010-9232-1

KEY WORDS

Search

Navigation