J Clin Periodontol 2015; 42: 733–739 doi: 10.1111/jcpe.12421
Association between overweight/ obesity and increased risk of periodontitis Suvan JE, Petrie A, Nibali L, Darbar U, Rakmanee T, Donos N, D’Aiuto F. Association between overweight/obesity and increased risk of periodontitis. J Clin Periodontol 2015; 42: 733–739. doi:10.1111/jcpe.12421.
Abstract Objective: To investigate periodontitis as a co-morbidity of overweight/obesity in an age-matched sample of periodontitis cases or periodontally healthy controls. Methods: Participants were periodontally assessed using whole mouth clinical periodontal measures. Multivariable conditional logistic regression was used to calculate the odds ratio for diagnosis of periodontitis when body mass index (kg/m2), overweight (BMI 25–29.99 kg/m2, or obese BMI ≥ 30 kg/m2) were the explanatory variables. A receiver operating characteristic (ROC) curve was generated of all possible BMI (kg/m2) cut-off points discriminating individuals for diagnosis of periodontitis. Results: The study comprised 286 participants. BMI showed a dose–response association with increased odds (1.12 per increase of 1 kg/m2, 95% CI 1.05–1.20, p = 0.001) of being a case compared to a control independent of gender, ethnicity, smoking status and dental plaque level. Similarly overweight/obese were independently associated with increased odds of diagnosis of periodontitis for overweight (OR = 2.56, 95% CI 1.210–5.400, p = 0.014) and for obese (OR = 3.11, 95% CI 1.052–6.481, p = 0.015) compared to normal weight individuals. The ROC curve analysis confirmed diagnosis of periodontitis was 1.6 times more likely in an individual with the BMI ≥ 24.32 kg/m2. Conclusions: Overweight/obese individuals are more likely to suffer from periodontitis compared to normal weight individuals in this case–control sample.
Obesity is a highly prevalent condition worldwide especially in developed countries (WHO 2006). It is a Conflict of interest and sources of funding: The authors declare no conflicts of interest. This work was undertaken at UCLH/UCL who received a proportion of funding from the Department of Health’s NIHR Biomedical Research Centres funding scheme. Francesco D’Aiuto holds a Clinical Senior Lectureship Award supported by the UK Clinical Research Collaboration.
metabolic condition occurring due to an energy imbalance (intake > consumption), which subsequently leads to an increase in adipose tissue deposits (Bray 2007). As adipocytes exert a number of endocrine functions, increased adiposity is associated with a state of low-grade inflammation and insulin resistance (Bray 2004, Gimeno & Klaman 2005). Periodontitis is a chronic inflammatory disease driven by bacterial pathogens and is one of the most common oral infections worldwide (WHO 2004). The host response to
© 2015 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Jean E. Suvan1, Aviva Petrie2, Luigi Nibali1, Ulpee Darbar3, Thanasak Rakmanee4, Nikos Donos1 and Francesco D’Aiuto1 1
Unit of Periodontology, University College London (UCL), Eastman Dental Institute, London, UK; 2Biostatistics Unit, UCL Eastman Dental institute, London, UK; 3 University College London Hospitals NHS Trust (UCLH), Eastman Dental Hospital, London, UK; 4Faculty of Dentistry, Thammasat University, Patumthani, Thailand
Key words: body mass index; obesity; overweight; periodontitis Accepted for publication 2 June 2015
periodontal pathogens represents a crucial determinant of the individual’s susceptibility to periodontitis. Several pro-inflammatory molecules and processes implicated in the pathogenesis of periodontitis, including cytokines (e.g. Interleukin-IL-6), chemokines and T-cell function, could be altered by obesity (Falagas & Kompoti 2006). An altered (delayed and sustained) inflammatory state, such as that found both in animal experimental conditions (Amar et al. 2007) and in obese individuals, could predispose individuals to increased periodontal tissue
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destruction (Boesing et al. 2009). These findings are also corroborated by several lines of clinical evidence suggesting that obesity could be a novel risk factor for periodontitis (Suvan et al. 2011). Indeed, obese individuals present with an increased prevalence of periodontitis, with raised gingival inflammatory responses and possibly altered periodontal microbial compositions (Boesing et al. 2009). Previously published evidence of the association between overweight/ obesity and periodontitis has largely been based upon cross-sectional epidemiological data collection and/or re-analysis of existing health survey databases (Chaffee & Weston 2010, Suvan et al. 2011). These studies have been valuable in generating the hypothesis of association, however fall short of using robust and consistent methods to diagnose periodontitis (pragmatic screening and heterogeneous case definitions) which may lead to biased results. The aim of this study was to ascertain the odds of having periodontitis if an individual is overweight or obese. The null hypothesis was of no association between overweight/obesity and diagnosis of periodontitis (case definition proposed for studies of risk factors for periodontitis (Tonetti & Claffey 2005) in an agematched sample of adults).
Study participants
The overall clinical study sample consisted of 471 individuals recruited from the UCLH NHS Trust (UCLH Eastman Dental Hospital) new patient clinics between June 2006 and December 2010. Periodontitis cases were recruited from referrals to the Unit of Periodontology whilst periodontally healthy controls from other units within UCLH Eastman Dental Hospital. All participants (cases and controls) were ≥18 years old, had a minimum of 20 natural teeth and were otherwise systemically healthy (no active infectious diseases such as hepatitis, HIV or TB, or uncontrolled metabolic diseases including diabetes, kidney, liver or cardiovascular diseases assessed by the examining clinician and medical history). Exclusion criteria comprised pregnancy, chronic use of non-steroidal anti-inflammatory drugs; antibiotics use within 3 months of study visit and past periodontal therapy. Cases were included if they presented with the presence of one or more sites with PPD ≥5 mm or radiographic evidence of bone loss ≥20% of the root length. Controls were included if they had no evidence of periodontitis (absence of sites with PPD ≥5 mm). Case definition and age matching
Materials and Methods Study design
This study was designed as a case– control analysis of age-matched participants enrolled in a larger clinical study recruiting cases and controls based on the presence or absence of periodontitis as confirmed by fullmouth periodontal examination. The exposure of body mass index (BMI) was calculated during data analysis based upon height and weight (kg/m2) measured by the clinician during the study visit. The protocol was reviewed and approved by the Joint UCL/UCLH Committees on the Ethics of Human Research (Ref 05/ Q0502/84). All participants gave written informed consent prior to participation. This report conforms to the STROBE guidelines for the strengthening of reporting of observational studies (von Elm et al. 2008).
This subset study sample was selected from the overall based upon the European Federation of Periodontology (EFP) case definition of periodontitis for epidemiological studies of risk factors. A “periodontitis case” was defined when “proximal attachment loss of ≥3 mm in ≥2 non-adjacent teeth” was identified (Tonetti & Claffey 2005). Based on presence/absence of this criterion a case or a control population were identified. Furthermore, as ageing represents an important risk factor for periodontal tissue loss (Grossi et al. 1994), 143 age-matched pairs (one to one based on year of birth) were identified for analysis. Sample size calculation
Sample Size Tables for Clinical Studies software were used to calculate the sample size for this study (Machin et al. 2008). A sample of
274 individuals (137 participants per group) would have 90% power to detect a clinically relevant odds ratio of 2.0 for presence of periodontitis in obese compared to normal weight individuals, assuming a prevalence of obesity in the general population of 23.8% and using a 0.05 two-sided significance level (DOH UK 2006). Data collection
Data collection methods were the same for all study participants. All visits were carried out in the same setting and measurements were performed by one of the three calibrated study examiners. Prior to the initiation of the study, an examiner repeatability exercise was undertaken to confirm adequate intra-examiner repeatability using 10 non-study patients suffering from moderate to severe periodontitis (duplicate measurements with another patient or waiting a time period of 30 min between). Following this, a calibration exercise was carried out on 10 patients per examiner to confirm inter-examiner agreement (measured by one examiner then alternate examiner on the same day). The data were analysed to confirm intra-examiner repeatability and inter-examiner calibration at a pre-determined success criteria level of agreement within 2 mm for CAL in a minimum 98% of sites measured. All examiners reached levels above the 98% agreement threshold for repeatability and calibration. At the study visit, following informed consent, the study examiner obtained the participant’s medical history update, oral examination, a lifestyle questionnaire (exercise, diet, oral hygiene practice, etc.), demographic data (age, gender, smoking history and ethnicity) and body weight and height for calculation of BMI. Height and weight were measured by a trained dental nurse using a wall-mounted height measure and mechanical scales (BMI was calculated as kg/m2 during data processing). Periodontal health or disease status was based upon recording of whole mouth probing pocket depths and clinical recession. Dental plaque levels and gingival bleeding on probing scores were assessed dichotomously as plaque or bleeding being present or absent (O’Leary et al.
© 2015 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Overweight/Obesity and Risk of Periodontitis 1972, Ainamo & Bay 1975). All clinical parameters were assessed at six sites per tooth for all teeth present in the mouth. Statistical analysis
SPSS 20.0 (IBM Corp 2011) statistical software package and Stata 10.0 (StataCorp) were used for data analyses. Data for all participants were combined in SPSS 20.0 and the database was checked for accuracy and consistency. The data were then imported into Stata 10.0. Following completion of descriptive statistics, statistical significance was set at a p-value of
Association between overweight/ obesity and increased risk of periodontitis Suvan JE, Petrie A, Nibali L, Darbar U, Rakmanee T, Donos N, D’Aiuto F. Association between overweight/obesity and increased risk of periodontitis. J Clin Periodontol 2015; 42: 733–739. doi:10.1111/jcpe.12421.
Abstract Objective: To investigate periodontitis as a co-morbidity of overweight/obesity in an age-matched sample of periodontitis cases or periodontally healthy controls. Methods: Participants were periodontally assessed using whole mouth clinical periodontal measures. Multivariable conditional logistic regression was used to calculate the odds ratio for diagnosis of periodontitis when body mass index (kg/m2), overweight (BMI 25–29.99 kg/m2, or obese BMI ≥ 30 kg/m2) were the explanatory variables. A receiver operating characteristic (ROC) curve was generated of all possible BMI (kg/m2) cut-off points discriminating individuals for diagnosis of periodontitis. Results: The study comprised 286 participants. BMI showed a dose–response association with increased odds (1.12 per increase of 1 kg/m2, 95% CI 1.05–1.20, p = 0.001) of being a case compared to a control independent of gender, ethnicity, smoking status and dental plaque level. Similarly overweight/obese were independently associated with increased odds of diagnosis of periodontitis for overweight (OR = 2.56, 95% CI 1.210–5.400, p = 0.014) and for obese (OR = 3.11, 95% CI 1.052–6.481, p = 0.015) compared to normal weight individuals. The ROC curve analysis confirmed diagnosis of periodontitis was 1.6 times more likely in an individual with the BMI ≥ 24.32 kg/m2. Conclusions: Overweight/obese individuals are more likely to suffer from periodontitis compared to normal weight individuals in this case–control sample.
Obesity is a highly prevalent condition worldwide especially in developed countries (WHO 2006). It is a Conflict of interest and sources of funding: The authors declare no conflicts of interest. This work was undertaken at UCLH/UCL who received a proportion of funding from the Department of Health’s NIHR Biomedical Research Centres funding scheme. Francesco D’Aiuto holds a Clinical Senior Lectureship Award supported by the UK Clinical Research Collaboration.
metabolic condition occurring due to an energy imbalance (intake > consumption), which subsequently leads to an increase in adipose tissue deposits (Bray 2007). As adipocytes exert a number of endocrine functions, increased adiposity is associated with a state of low-grade inflammation and insulin resistance (Bray 2004, Gimeno & Klaman 2005). Periodontitis is a chronic inflammatory disease driven by bacterial pathogens and is one of the most common oral infections worldwide (WHO 2004). The host response to
© 2015 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Jean E. Suvan1, Aviva Petrie2, Luigi Nibali1, Ulpee Darbar3, Thanasak Rakmanee4, Nikos Donos1 and Francesco D’Aiuto1 1
Unit of Periodontology, University College London (UCL), Eastman Dental Institute, London, UK; 2Biostatistics Unit, UCL Eastman Dental institute, London, UK; 3 University College London Hospitals NHS Trust (UCLH), Eastman Dental Hospital, London, UK; 4Faculty of Dentistry, Thammasat University, Patumthani, Thailand
Key words: body mass index; obesity; overweight; periodontitis Accepted for publication 2 June 2015
periodontal pathogens represents a crucial determinant of the individual’s susceptibility to periodontitis. Several pro-inflammatory molecules and processes implicated in the pathogenesis of periodontitis, including cytokines (e.g. Interleukin-IL-6), chemokines and T-cell function, could be altered by obesity (Falagas & Kompoti 2006). An altered (delayed and sustained) inflammatory state, such as that found both in animal experimental conditions (Amar et al. 2007) and in obese individuals, could predispose individuals to increased periodontal tissue
733
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destruction (Boesing et al. 2009). These findings are also corroborated by several lines of clinical evidence suggesting that obesity could be a novel risk factor for periodontitis (Suvan et al. 2011). Indeed, obese individuals present with an increased prevalence of periodontitis, with raised gingival inflammatory responses and possibly altered periodontal microbial compositions (Boesing et al. 2009). Previously published evidence of the association between overweight/ obesity and periodontitis has largely been based upon cross-sectional epidemiological data collection and/or re-analysis of existing health survey databases (Chaffee & Weston 2010, Suvan et al. 2011). These studies have been valuable in generating the hypothesis of association, however fall short of using robust and consistent methods to diagnose periodontitis (pragmatic screening and heterogeneous case definitions) which may lead to biased results. The aim of this study was to ascertain the odds of having periodontitis if an individual is overweight or obese. The null hypothesis was of no association between overweight/obesity and diagnosis of periodontitis (case definition proposed for studies of risk factors for periodontitis (Tonetti & Claffey 2005) in an agematched sample of adults).
Study participants
The overall clinical study sample consisted of 471 individuals recruited from the UCLH NHS Trust (UCLH Eastman Dental Hospital) new patient clinics between June 2006 and December 2010. Periodontitis cases were recruited from referrals to the Unit of Periodontology whilst periodontally healthy controls from other units within UCLH Eastman Dental Hospital. All participants (cases and controls) were ≥18 years old, had a minimum of 20 natural teeth and were otherwise systemically healthy (no active infectious diseases such as hepatitis, HIV or TB, or uncontrolled metabolic diseases including diabetes, kidney, liver or cardiovascular diseases assessed by the examining clinician and medical history). Exclusion criteria comprised pregnancy, chronic use of non-steroidal anti-inflammatory drugs; antibiotics use within 3 months of study visit and past periodontal therapy. Cases were included if they presented with the presence of one or more sites with PPD ≥5 mm or radiographic evidence of bone loss ≥20% of the root length. Controls were included if they had no evidence of periodontitis (absence of sites with PPD ≥5 mm). Case definition and age matching
Materials and Methods Study design
This study was designed as a case– control analysis of age-matched participants enrolled in a larger clinical study recruiting cases and controls based on the presence or absence of periodontitis as confirmed by fullmouth periodontal examination. The exposure of body mass index (BMI) was calculated during data analysis based upon height and weight (kg/m2) measured by the clinician during the study visit. The protocol was reviewed and approved by the Joint UCL/UCLH Committees on the Ethics of Human Research (Ref 05/ Q0502/84). All participants gave written informed consent prior to participation. This report conforms to the STROBE guidelines for the strengthening of reporting of observational studies (von Elm et al. 2008).
This subset study sample was selected from the overall based upon the European Federation of Periodontology (EFP) case definition of periodontitis for epidemiological studies of risk factors. A “periodontitis case” was defined when “proximal attachment loss of ≥3 mm in ≥2 non-adjacent teeth” was identified (Tonetti & Claffey 2005). Based on presence/absence of this criterion a case or a control population were identified. Furthermore, as ageing represents an important risk factor for periodontal tissue loss (Grossi et al. 1994), 143 age-matched pairs (one to one based on year of birth) were identified for analysis. Sample size calculation
Sample Size Tables for Clinical Studies software were used to calculate the sample size for this study (Machin et al. 2008). A sample of
274 individuals (137 participants per group) would have 90% power to detect a clinically relevant odds ratio of 2.0 for presence of periodontitis in obese compared to normal weight individuals, assuming a prevalence of obesity in the general population of 23.8% and using a 0.05 two-sided significance level (DOH UK 2006). Data collection
Data collection methods were the same for all study participants. All visits were carried out in the same setting and measurements were performed by one of the three calibrated study examiners. Prior to the initiation of the study, an examiner repeatability exercise was undertaken to confirm adequate intra-examiner repeatability using 10 non-study patients suffering from moderate to severe periodontitis (duplicate measurements with another patient or waiting a time period of 30 min between). Following this, a calibration exercise was carried out on 10 patients per examiner to confirm inter-examiner agreement (measured by one examiner then alternate examiner on the same day). The data were analysed to confirm intra-examiner repeatability and inter-examiner calibration at a pre-determined success criteria level of agreement within 2 mm for CAL in a minimum 98% of sites measured. All examiners reached levels above the 98% agreement threshold for repeatability and calibration. At the study visit, following informed consent, the study examiner obtained the participant’s medical history update, oral examination, a lifestyle questionnaire (exercise, diet, oral hygiene practice, etc.), demographic data (age, gender, smoking history and ethnicity) and body weight and height for calculation of BMI. Height and weight were measured by a trained dental nurse using a wall-mounted height measure and mechanical scales (BMI was calculated as kg/m2 during data processing). Periodontal health or disease status was based upon recording of whole mouth probing pocket depths and clinical recession. Dental plaque levels and gingival bleeding on probing scores were assessed dichotomously as plaque or bleeding being present or absent (O’Leary et al.
© 2015 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Overweight/Obesity and Risk of Periodontitis 1972, Ainamo & Bay 1975). All clinical parameters were assessed at six sites per tooth for all teeth present in the mouth. Statistical analysis
SPSS 20.0 (IBM Corp 2011) statistical software package and Stata 10.0 (StataCorp) were used for data analyses. Data for all participants were combined in SPSS 20.0 and the database was checked for accuracy and consistency. The data were then imported into Stata 10.0. Following completion of descriptive statistics, statistical significance was set at a p-value of
