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Local and Systemic Biomarkers in Gingival Crevicular Fluid Increase

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Local and Systemic Biomarkers in Gingival Crevicular Fluid Increase J Clin Periodontol 2010; 37: 30–36 doi: 10.1111/j.1600-051X.2009.01506.x Tracy R. Fitzsimmons1, Anne E. Local and systemic biomarkers in Sanders2, P. Mark Bartold1 and Gary D. Slade2 1Centre for Orofacial Research and Learning, gingival crevicular fluid increase Colgate Australia Clinical Dental Research Centre, School of Dentistry, University of Adelaide, Adelaide, SA, Australia; odds of periodontitis 2Australian Research Centre for Population Oral Health, School of Dentistry, University of Adelaide, Adelaide, SA, Australia Fitzsimmons TR, Sanders AE, Bartold PM, Slade GD. Local and systemic biomarkers in gingival crevicular fluid increase odds of periodontitis. J Clin Periodontol 2010; 37: 30–36. doi: 10.1111/j.1600-051X.2009.01506.x. Abstract Aim: To determine the independent and combined associations of interleukin-1b (IL-1b) and C-reactive protein (CRP) in gingival crevicular fluid (GCF) on periodontitis case status in the Australian population. Materials and Methods: GCF was collected from 939 subjects selected from the 2004–2006 Australian National Survey of Adult Oral Health: 430 cases had examiner- diagnosed periodontitis, and 509 controls did not. IL-1b and CRP in GCF were detected by enzyme-linked immunosorbent assays. Odds ratios (OR) and 95% confidence intervals (CIs) were calculated in bivariate and stratified analysis and fully adjusted ORs were estimated using multivariate logistic regression. Results: Greater odds of having periodontitis was associated with higher amounts of IL-1b (OR 5 2.4, 95% CI 5 1.7–3.4 for highest tertile of IL-1b relative to lowest tertile) and CRP (OR 5 1.9, 95% CI 5 1.5–2.5 for detectable CRP relative to undetectable CRP). In stratified analysis, there was no significant interaction between biomarkers (p 5 0.68). In the multivariate analyses that controlled for conventional periodontal risk factors, these relationships remained (IL-1b OR 5 1.8, 95% CI 5 1.1–2.6; CRP OR 5 1.7, 95% CI 5 1.3–2.3). Conclusions: Elevated odds of clinical periodontitis was associated independently Key words: C-reactive protein; gingival with each biomarker. This suggests that people with elevated biomarkers indicative of crevicular fluid; interleukin-1b; periodontitis either local (IL-1b) or systemic (CRP) inflammation are more likely to suffer from periodontal disease. Accepted for publication 14 October 2009 Numerous studies have shown that bio- retson et al. 2002, Bostanci et al. 2007, from the periodontium become elevated markers of inflammatory response are Zhong et al. 2007). These biomarkers in response to periodontitis only as a elevated in people with periodontitis include cytokines known to be produced consequence of locally produced bio- compared with healthy controls (Mogi locally in periodontal tissues [e.g. inter- markers in the periodontium. If that et al. 1999, Gamonal et al. 2000, Engeb- leukin-1b (IL-1b)] as well as acute phase were so, then the association between reactants that predominantly are pro- CRP and periodontitis would be depen- duced in tissues remote from the infection dent upon IL-1b levels in the period- Conflict of interest and source of [e.g. C-reactive protein (CRP), predomi- ontium. However, if both CRP and funding statement nantly produced in liver]. Our own case– IL-1b are independently associated The authors declare that there are no control study confirmed these findings in with periodontitis, it would suggest the conflicts of interest in this study. samples of gingival crevicular fluid relationship is more complex, and This study was supported by grants from (GCF) collected from a representative potentially could offer insight into sepa- the National Health and Medical Res- population-based sample of Australian rate mechanisms by which local and earch Council (Project Grants #349514 adults in which we measured IL-1b and systemic inflammatory responses are and #299060). Dr. Sanders is supported CRP (Fitzsimmons et al. 2009). related to the disease. by a NHMRC Sidney Sax Public Health It is possible that inflammatory bio- The relationship between inflamma- Fellowship (#399222). markers produced in tissues remote tory biomarkers and periodontitis is 30 r 2009 University of Adelaide GCF IL-1b, CRP and periodontitis 31 most likely bidirectional. On the one Consequently, in the current analyses, probing depths were recorded. Where hand, bacterial infection in the perio- we focus on periodontitis as the depen- all probing depth measurements were dontal tissues stimulates a local immune dent variable with the primary aim to o4 mm, a simple random sampling response involving the production and determine the combined effects of each method was used to select all four sites. release of several inflammatory media- biomarker on occurrence of clinical Otherwise, a stratified random sampling tors into the surrounding tissue. The role periodontitis. Our hypothesis was that method was used to collect GCF from of one such mediator, IL-1b, is well each biomarker would contribute inde- up to two sites with probing depth 4 mm, known in periodontal disease progres- pendently to the odds of periodontitis, and the remaining samples from sites sion (Lo et al. 1999, Graves & Cochran and that their effects would be observa- with probing depth o4 mm. 2003) and as an indicator of active ble even after adjusting for conventional inflammation. Produced locally at the risk factors for periodontitis. Such a Case definition site of infection by a number of cells finding is consistent with the notion involved in host defence against perio- that both local and systemic inflamma- For this study, 939 examined survey dontal pathogens including macro- tory processes contribute to the risk of participants were selected using a phages, neutrophils and gingival having periodontitis. case–control study design. Cases were fibroblasts (Takahashi et al. 1995, Lo If this hypothesis is supported, find- people with two or more interproximal et al. 1999, Steffen et al. 2000), IL-1b is ings will build on existing evidence to sites with X4 mm clinical attachment initially released to combat infection. provide ‘‘proof-of-principle’’ support loss and two or more interproximal sites However, persistent infection leads to for a potential etiological association with PD of X5 mm or more were the dysregulation of the immune system between both sources of inflammation defined as moderate or severe perio- and a cascade of events, initiated by IL- and periodontitis case status. dontitis cases, while non-cases had less 1b, results in chronic inflammation of extensive disease (Page & Eke 2007). the periodontal supporting tissues, cul- All examined NSAOH subjects who met minating in destruction of alveolar Materials and Methods criteria as periodontal cases were bone mediated via IL-1b regulation of included in this study, while NSAOH Study design and sampling osteoclasts (Graves & Cochran 2003). subjects who were non-cases were These inflammatory processes in perio- The current case–control study as pre- sampled at random for this study to dontal tissues can trigger a more gen- viously described (Fitzsimmons et al. select an approximately equivalent eralized systemic response in tissues 2009) was nested within the National number of non-cases for this study. remote from the periodontium, such as Survey of Adult Oral Health (2004– Non-cases from the NSAOH subjects the liver. 2006) (NSAOH) (Slade et al. 2007). were selected at random using a random Meanwhile, inflammatory processes The University of Adelaide’s Human number generator in SAS (SAS v.9.2, elsewhere in the body can contribute to Research Ethics Committee granted SAS Institute, Cary, NC, USA), with periodontitis. Some systemic diseases approval for the National Survey. Dur- frequency matching within states/terri- (such as diabetes) that increase risk of ing the survey, 5505 people underwent tories to achieve similar numbers of periodontitis also contribute to inflam- standardized oral epidemiological cases and non-cases within each juris- matory responses in numerous tissues, examinations. All examined subjects diction. increasing systemic levels of each bio- provided written informed consent marker. Finally, there is speculation that before the examination. Examinations GCF collection and analysis a common underlying hyper-inflamma- included measurements of periodontal tory phenotype might predispose peo- pocket depth (PD) and gingival reces- GCF was collected on two PerioPapert ple, both to periodontitis and systemic sion on all teeth except third molars. strips (Oraflow Inc., Plainview, NY, inflammation (Offenbacher & Beck Three sites were assessed per tooth: USA) per site as previously described 2005). These bidirectional effects mean mesiobuccal, mid-buccal and distobuc- (Fitzsimmons et al. 2009). Briefly, the that elevated levels of inflammatory cal. Clinical periodontal attachment area was isolated from saliva with cot- biomarkers may signify both the causes level was calculated as the sum of PD ton rolls and air dried before placing the and consequences of periodontitis. and recession at each site during subse- strip into the gingival crevice for 10 s. Given the likely bidirectional causal quent data management. Following Paper strips were wrapped in foil before pathways linking periodontitis and probing measurements, up to four perio- shipping to the laboratory by mail where inflammatory biomarkers, it is informa- dontal sites were selected at random they were frozen at À 201C until pro- tive to examine these relationships using from among all measured periodontal cessed. GCF samples contaminated
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