Original Contribution
Oxidative stress, chronic inflammation, and telomere length in patients with periodontitis

https://doi.org/10.1016/j.freeradbiomed.2010.12.031Get rights and content

Abstract

The aim of this study was to determine leukocyte telomere length (LTL) in individuals with periodontitis and controls, exploring its relationship with systemic inflammation and oxidative stress. Five hundred sixty-three participants were recruited for this case–control study: 356 subjects with and 207 subjects without periodontitis. LTL was measured by a qPCR technique from leukocytes' DNA. Global measures of oxidative stress (reactive oxygen metabolites) and biological antioxidant potential in plasma were performed together with high-sensitivity assays for C-reactive protein (CRP). Leukocyte counts and lipid profiles were performed using standard biochemistry. Cases had higher levels of CRP (2.1 ± 3.7 mg/L vs 1.3 ± 5.4 mg/L, P < 0.001) and reactive oxygen metabolites (378.1 ± 121.1 U Carr vs 277.4 ± 108.6 U Carr, P < 0.001) compared to controls. Overall, cases had shorter LTL with respect to controls (1.23 ± 0.42 vs 1.12 ± 0.31 T/S ratio, P = 0.006), independent of age, gender, ethnicity, and smoking habit. When divided by subgroup of periodontal diagnosis (chronic, n = 285; aggressive, n = 71), only chronic cases displayed shorter LTL (P = 0.01). LTL was negatively correlated with age (P = 0.001; R =  0.2), oxidative stress (P = 0.008; R =  0.2), and severity of periodontitis (P = 0.003; R =  0.2) in both the whole population and the subgroups (cases and controls). We conclude that shorter telomere lengths are associated with a diagnosis of periodontitis and their measures correlate with the oxidative stress and severity of disease.

Section snippets

Study groups

In a case–control design, a total of 563 participants were recruited among subjects referred to the UCL Eastman Dental Institute in London between 2002 and 2006. For all participants a complete medical history was obtained via interview (including smoking history and current or previous use of medications). Subjects with any medical disorder, including cancer, type 2 diabetes, hypertension, and major cardiovascular/endocrine diseases, were excluded from the study. All subjects currently taking

Results

The characteristics of the study population are summarized in Table 1. Periodontal patients had higher serum levels of CRP (P < 0.001) and leukocyte counts (P < 0.001) compared to controls. Further, greater total cholesterol (P = 0.003) and LDL cholesterol (P < 0.001) levels, as well as lower HDL cholesterol (P < 0.001), were observed. Cases exhibited higher levels of reactive oxygen metabolites (P < 0.001) and lower antioxidant potential (P < 0.001) as assessed by D-ROM and BAP tests, respectively (Table 1

Discussion

This is the first report to describe an association between shorter LTL and periodontitis. Patients with periodontitis presented shorter LTL, higher systemic inflammation, and higher oxidative stress compared to controls. Furthermore, LTL was negatively correlated with total levels of reactive oxidative metabolites detected by D-ROM test and severity of periodontitis. These associations were independent of age, gender, ethnicity, and smoking differences. In subgroup analyses of periodontal

Conclusions

In conclusion our data suggest that chronic inflammation could be the main driver of shorter LTL in patients with periodontitis and that the local and systemic effects of oxidative stress could be considered the main predictor of the LTL attrition. Moreover, the evidence of shorter LTL detected in individuals with chronic periodontitis could provide a possible biological explanation for the reported higher mortality rate in these patients compared to the general population. Further research and

Acknowledgments

This work was undertaken at UCLH/UCL, which received a proportion of funding from the Department of Health's NIHR Biomedical Research Centres funding scheme. S.E.H. and K.D.S. are funded by the British Heart Foundation (RG2008/08 and FS/06/053). F.D. holds a Clinical Senior Lectureship Award supported by the UK Clinical Research Collaboration. We thank Prof. Eugenio Iorio for his assistance with the laboratory oxidative stress analyses.

References (37)

  • A. Aviv

    Leukocyte telomere length, hypertension, and atherosclerosis: are there potential mechanistic explanations?

    Hypertension

    (2009)
  • R.T. Demmer et al.

    Epidemiologic patterns of chronic and aggressive periodontitis

    Periodontology

    (2010)
  • R.C. Williams

    Periodontal disease

    N. Engl. J. Med.

    (1990)
  • H. Birkedal-Hansen

    Role of cytokines and inflammatory mediators in tissue destruction

    J. Periodontal Res.

    (1993)
  • S.S. Socransky

    Microbiology of plaque

    Compend. Contin. Educ. Dent. Suppl.

    (1984)
  • S.S. Socransky et al.

    Microbial complexes in subgingival plaque

    J. Clin. Periodontol.

    (1998)
  • S. Offenbacher

    Periodontal diseases: pathogenesis

    Ann. Periodontol.

    (1996)
  • B.G. Loos et al.

    Elevation of systemic markers related to cardiovascular diseases in the peripheral blood of periodontitis patients

    J. Periodontol.

    (2000)
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      Some mechanisms, including oxidative stress and systemic inflammation, have been postulated to underlie the relationship of exposure to PAHs and molecular changes (DNA and proteins). Both increased inflammation and oxidative stress have been suggested to play a main role in the shorting of the TL (Houben et al., 2008; Masi et al., 2011). PAHs metabolites are detoxified through P450 enzymes such as glutathione S-transferase M1 (GSTM1) (Seidegård and Ekström, 1997), but their high and continuous exposure has the potential to generate oxygen radicals, which, in turn, could result in the formation of 8-hydro-20-deoxyguanosine (8-OHdG) and DNA damage (Asami et al., 1997).

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    These authors equally contributed to this work.

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