COPD, 11:424–430, 2014 ISSN: 1541-2555 print / 1541-2563 online Copyright © Informa Healthcare USA, Inc. DOI: 10.3109/15412555.2013.858316
ORIGINAL RESEARCH
The Association between Periodontal Disease and Chronic Obstructive Pulmonary Disease: A Case Control Study
COPD Downloaded from informahealthcare.com by University of Newcastle on 09/28/14 For personal use only.
Görkem Öztekin,1 Ulku Baser,1 Meric Kucukcoskun,1 Sevda Tanrikulu-Kucuk,2 Evin Ademoglu,3 Gulden Isik,1 Gulcihan Ozkan,4 Funda Yalcin,1 and Esen Kiyan5 1
Department of Periodontology, Faculty of Dentistry, Istanbul University, Istanbul, Turkey
2
Department of Biochemistry, Faculty of Medicine, Istanbul Bilim University, Istanbul, Turkey
3
Department of Biochemistry, Istanbul Faculty of Medicine, Istanbul University, Istanbul, Turkey
4
Yedikule Chest Diseases and Thoracic Surgery Training and Research Hospital, Istanbul, Turkey
5
Department of Pulmonary Diseases, Istanbul Faculty of Medicine, Istanbul University, Istanbul, Turkey
Abstract Introduction: Although there are studies evaluating the effects of periodontal health on chronic obstructive pulmonary disease (COPD), the effects of COPD – a systemic disease, on periodontal tissue is unknown. The aim of this study is to evaluate the effects of COPD on periodontal tissues by comparing COPD patients and controls. Methods: Fifty-two COPD patients and 38 non-COPD controls were included in this case-control study. Number of teeth, plaque index (PI), gingival index (GI), bleeding on probing, clinical attachment level and probing depth were included in the periodontal examination. In addition to clinical evaluations, gingival crevicular fluid (GCF) levels of high-sensitive C-reactive protein (hs-CRP), interleukin-1 beta (IL-l) and prostaglandin-E2 (PGE2), and serum hs-CRP levels were measured in COPD patients and the controls. Results: The number of teeth was significantly lower while PI and GI were significantly higher in COPD patients when compared to the controls. As well as serum hs-CRP levels, the GCF levels of hs-CRP, IL-1 and PGE2 were significantly higher in COPD patients than the controls. Conclusion: Our results demonstrated that COPD may be associated with periodontal disease as manifested by lower number of teeth and higher levels of inflammatory mediators especially CRP in GCF. This finding may be a reflection of systemic effects of COPD on periodontal tissues. Poor oral health behavior of COPD patients have to be considered in larger size group studies in the future.
Introduction
Keywords: pulmonary disease, chronic obstructive, periodontal disease, periodontitis, C-reactive protein, interleukin-1beta Correspondence to: Dr. Ulku Baser, Istanbul University, Faculty of Dentistry, Department of Periodontology, 34390 Capa, Istanbul, Turkey, Phone: +902124142020/ 30253, Fax: +902125340807, email: baserulku@ hotmail.com
424
Chronic obstructive pulmonary disease (COPD) is a chronic progressive disease characterized by airflow limitation that is not fully reversible, and is associated with an abnormal inflammatory response of the lungs to inhaled noxious particles or gases. It is a major cause of morbidity and mortality in the World (1). COPD is associated with inflammation, both in the stable phase of the disease and during exacerbations. Inflammation in the lung is also associated with a certain degree of systemic inflammation (2). For this reason, COPD has been considered as a systemic disease in recent years and some inflammatory mediators are responsible for COPD-related systemic manifestations (3, 4). A meta-analysis done by Gan et al. has shown that even patients with stable COPD have increased white blood cell count and elevated C-reactive protein (CRP), fibrinogen and cytokines (e.g. interleukin-1 beta, interleukin-6,tumor necrosis factor-alpha) levels (5). High levels of Prostaglandin E2 (PGE2), which is a pro-inflammatory mediator, correlates with the severity of airflow limitation in stable COPD (6). Therefore, PGE2 may be one of the major contributors to the pathogenesis of inflammation in COPD.
COPD Downloaded from informahealthcare.com by University of Newcastle on 09/28/14 For personal use only.
Effect of COPD on periodontal tissues
Periodontitis is a chronic inflammatory disease which serves as a reservoir of Gram-negative anaerobic organisms, lipopolysaccharides and some proinflammatory mediators (7). Among the pro-inflammatory mediators, PGE2 and interleukin-1 beta (IL-lβ) play critical roles in inflammatory processes leading to alveolar bone and connective tissue loss in periodontal disease (8–10). In periodontitis, the local destruction of the periodontal tissues causes a large surface area of ulcerated pocket epithelium which allows exchange between bacterial and host products (11). It has been suggested that while periodontitis may have systemic effects, some systemic diseases such as cardiovascular diseases, diabetes, respiratory diseases, adverse pregnancy outcomes and osteoporosis have negative effects on periodontal tissue (12–14). The relation between periodontal and systemic diseases is believed to be mediated through systemic inflammatory reactants such as acute-phase proteins and immune effectors, but the underlying biological mechanisms are yet unclear, and speculative (2, 13). The association between periodontal diseases and respiratory diseases has been discussed for years. Large-scale studies have been performed in patients with different respiratory diseases including COPD. These studies were designed to observe the effects of periodontal health on COPD (15–18). There is little information known about the effect of COPD and systemic inflammation in COPD in particular, on periodontal health. Our hypothesis was that COPD patients might have higher inflammatory response and worse periodontal health due to the subsequent pro-inflammatory events that occur in COPD when compared to non-COPD patients. The aim of this case-control study was to evaluate the effects of COPD on periodontal tissues by measuring clinical parameters and gingival crevicular fluid (GCF) IL-1β, PGE2 in addition to serum and GCF high-sensitive C-reactive protein (hs-CRP) levels.
Material and Methods Subjects and study design We screened the medical records of COPD patients (560 cases) who were followed on an outpatient basis by three chest clinics in Istanbul (Istanbul Medical Faculty Department of Respiratory Diseases, Yedikule Chest Diseases and Thoracic Surgery Training and Research Hospital and Sureyyapasa Chest Diseases and Thoracic Surgery Training and Research Hospital) between August 2008 and October 2011. Of 560 COPD patients, 440 who fulfilled the GOLD diagnostic criteria (1) were evaluated with regard to exclusion criteria. Patients with less than 8 teeth (n = 55) or who were edentulous (n = 288), as well as those who had significant respiratory diseases in addition to COPD (n = 6), a history of significant cardiovascular disorders or diabetes (n = 37), www.copdjournal.com
or a history of smoking in the last 2 years (n = 2) were excluded. As a result, 52 stable COPD patients fulfilling the inclusion criteria participated in the study. All patients were stable when included in the study (no infective exacerbation within one month prior to being included in the study). The COPD group (n = 52) was divided into two subgroups with regard to the disease severity; patients with mild and moderate COPD were included in group I and the patients with severe and very severe COPD were included in group II. Thirty-eight non-COPD controls who attended to Istanbul University, Faculty of Dentistry Department of Periodontology with matching age and gender constituted the control group. The controls with less than 8 teeth or who were edentulous or who had any respiratory diseases, significant cardiovascular disorders or diabetes were excluded. All controls were former smokers at least 2 years post-cessation of smoking. Local ethics committee of Istanbul University, Medical Faculty approved the study protocol (Project no. 2008/954), and informed written consent was obtained from all individuals prior to participation.
Assessment of COPD severity and lung function Forced expiratory volume in 1 second (FEV1), forced vital capacity (FVC) and FEV1/FVC ratio of the patients were measured via spirometry by trained and certified technicians and the results noted as percentages of the predicted values (FEV1% predicted). Later, the patients were divided into two subgroups, group-I (patients with mild-moderate COPD) and group-II (patients with severevery severe COPD) on the basis of FEV1% predicted values with regard to GOLD classification (1) (mild COPD: characterized by airflow limitation with FEV1 ≥80% predicted; moderate COPD: airflow limitation with ≤50% FEV1 < 80% predicted; severe COPD: airflow limitation with ≤30% FEV1 < 50% predicted; very severe COPD: airflow limitation with FEV1 < 30% predicted).
Periodontal examination The periodontal measurements including plaque index (PI) (19), gingival index (GI) (20), % of sites that had bleeding on probing (BoP), probing depth (PD), space between the cemento-enamel junction and gingival margin (SCG) and clinical attachment (CA) level were performed by the same blinded researcher (GO). An intraclass correlation coefficient of 0.85 for PD measurements indicated that the examiner reliability was high. PD and SCG were measured by William’s periodontal probe (Hu-Friedy, Chicago, IL) at six sites of all teeth (excluding third molars) and were recorded in millimeters. SCG was recorded as a positive value where the free gingival margin occurred apical to the cemento-enamel junction. CA level was calculated by CA level = PD + SCG formula.
425
COPD Downloaded from informahealthcare.com by University of Newcastle on 09/28/14 For personal use only.
426
Öztekin et al.
Gingival crevicular fluid and blood sampling The inflamed non-adjacent pocket sites of patients and controls were selected for gingival crevicular fluid (GCF) collections among the incisors and premolars with at least 4-mm depth. A total of 3 samples were collected to evaluate GCF level of IL-1β, PGE2 and hs-CRP from each patient. One sample was collected for each biomarker and analyzed separately. Sample collections were performed one week after the clinical measurements. Sample collections were performed 1 week after the clinical measurements. Briefly, after isolating the tooth with a cotton roll, the supragingival plaque was removed without touching the marginal gingival site and the crevicular site was gently air-dried. In order to avoid the contamination of saliva optimal effort was made. GCF was collected by paper strips (Periopaper, Oraflow Inc., NY, USA) positioned at the orifice of sulcus for 30 seconds. Strips with blood marks were discarded. The volume for each strip was measured with a calibrated meter (Periotron 6000, Oraflow Inc., NY, USA). The paper strips were immediately transferred to a plastic tube and stored at −80°C until analysis. For each assay, separate samples were collected and analyzed. The strips were not pooled. Fasting blood samples were collected in the anticoagulant-free vacutainer tubes by trained assistants and samples were immediately directed to the central biochemistry laboratory of Istanbul Medical Faculty for hs-CRP measurement. Biochemical analysis GCF was retrieved from the filter strips by eluting in 100-μl phosphate buffered saline solution-Tween buffer for 30 minutes and incubation on a shaking platform overnight (minimum 18 hours) for each parameter. GCF samples were analyzed for IL-1β, PGE2 (Invitrogen Co., Camarillo, CA, USA) and hs-CRP (R&D systems, Minneapolis, MN, USA), using commercially available sandwich enzyme linked immunosorbent assays according to the manufacturer’s instructions. The results of crevicular IL-1β and hs-CRP were expressed as ng/site and PGE2 as pg/site. Serum hs-CRP levels were measured by latexenhanced immuneturbidimetric assay using the Roche Modular P800 analyzer (Roche Diagnostics GmbH Mannheim, Germany) and results were expressed as mg/L. Statistical analysis The ideal sample size to assure adequate power for this cross-sectional study was calculated after a pilot experiment, and a 20% difference was obtained. With a power of 80% and α = 0.05, the minimum number of individuals required for the comparisons was 36 for each group. The data were evaluated with statistical software (SPSS Inc. Chicago, IL) and the results were presented as mean ± SD. Each patient was considered as an observation unit for periodontal clinical measurements and for each clinical parameter the average of the whole mouth measurements (excluding the third molars)
were used for statistical calculations. Demographic data analyses were done by using Pearson’s chi-square and independent sample t-test. The correlation between biochemical and clinical parameters were performed between the site that was sampled and the site’s clinical parameters. The comparison of demographical and clinical and biochemical parameters were performed by Mann–Whitney U-test. The relation between variables was evaluated by the Pearson correlation test.
Results Table 1 shows the demographical and clinical characteristics of COPD patients and the controls. The age, sex, time since the cessation of smoking and education status of the controls and COPD patients were similar. The number of teeth in COPD patients was significantly lower than the controls ( p < 0.001). PI and GI were significantly higher in COPD patients ( p < 0.001, p = 0.023 respectively). There was not a significant difference between the BoP and CAL scores of COPD patients and the controls. The number of sites with PD ≥ 4 mm was higher in the controls ( p < 0.04) but percentage of PD ≥ 4 mm was similar in both controls and COPD patients ( p = 0.14). GCF IL-1β and PGE2 levels, serum and GCF hs-CRP levels are presented in Table 2. The result of IL-1β levels and PGE2 levels were higher in COPD patients than the controls ( p < 0.001). The hs-CRP levels were significantly higher, both in GCF and serum of COPD patients when compared to the controls ( p = 0.01 and p = 0.035 respectively).
Table 1. Demographic and clinical variables of patients with COPD vs. controls Variable Age in years (mean ± SD)
Control (n = 38)
COPD Patients (n = 52)
p value
53.5 ± 9.2
57.5 ± 9.7
0.08
0.1
Gender (n; male/female)
32/6
49/3
(%; male)
85%
92%
6.8 ± 6.3
4.9 ± 4.3
0.07
Primary School
18
28
0.3
High School
9
11
Time since cessation of smoking in years (mean ± SD) Education (n)
Bachelor’s degree Number of teeth (mean ± SD)
11
13
22.2 ± 4.2
17.9 ± 5.1
ORIGINAL RESEARCH
The Association between Periodontal Disease and Chronic Obstructive Pulmonary Disease: A Case Control Study
COPD Downloaded from informahealthcare.com by University of Newcastle on 09/28/14 For personal use only.
Görkem Öztekin,1 Ulku Baser,1 Meric Kucukcoskun,1 Sevda Tanrikulu-Kucuk,2 Evin Ademoglu,3 Gulden Isik,1 Gulcihan Ozkan,4 Funda Yalcin,1 and Esen Kiyan5 1
Department of Periodontology, Faculty of Dentistry, Istanbul University, Istanbul, Turkey
2
Department of Biochemistry, Faculty of Medicine, Istanbul Bilim University, Istanbul, Turkey
3
Department of Biochemistry, Istanbul Faculty of Medicine, Istanbul University, Istanbul, Turkey
4
Yedikule Chest Diseases and Thoracic Surgery Training and Research Hospital, Istanbul, Turkey
5
Department of Pulmonary Diseases, Istanbul Faculty of Medicine, Istanbul University, Istanbul, Turkey
Abstract Introduction: Although there are studies evaluating the effects of periodontal health on chronic obstructive pulmonary disease (COPD), the effects of COPD – a systemic disease, on periodontal tissue is unknown. The aim of this study is to evaluate the effects of COPD on periodontal tissues by comparing COPD patients and controls. Methods: Fifty-two COPD patients and 38 non-COPD controls were included in this case-control study. Number of teeth, plaque index (PI), gingival index (GI), bleeding on probing, clinical attachment level and probing depth were included in the periodontal examination. In addition to clinical evaluations, gingival crevicular fluid (GCF) levels of high-sensitive C-reactive protein (hs-CRP), interleukin-1 beta (IL-l) and prostaglandin-E2 (PGE2), and serum hs-CRP levels were measured in COPD patients and the controls. Results: The number of teeth was significantly lower while PI and GI were significantly higher in COPD patients when compared to the controls. As well as serum hs-CRP levels, the GCF levels of hs-CRP, IL-1 and PGE2 were significantly higher in COPD patients than the controls. Conclusion: Our results demonstrated that COPD may be associated with periodontal disease as manifested by lower number of teeth and higher levels of inflammatory mediators especially CRP in GCF. This finding may be a reflection of systemic effects of COPD on periodontal tissues. Poor oral health behavior of COPD patients have to be considered in larger size group studies in the future.
Introduction
Keywords: pulmonary disease, chronic obstructive, periodontal disease, periodontitis, C-reactive protein, interleukin-1beta Correspondence to: Dr. Ulku Baser, Istanbul University, Faculty of Dentistry, Department of Periodontology, 34390 Capa, Istanbul, Turkey, Phone: +902124142020/ 30253, Fax: +902125340807, email: baserulku@ hotmail.com
424
Chronic obstructive pulmonary disease (COPD) is a chronic progressive disease characterized by airflow limitation that is not fully reversible, and is associated with an abnormal inflammatory response of the lungs to inhaled noxious particles or gases. It is a major cause of morbidity and mortality in the World (1). COPD is associated with inflammation, both in the stable phase of the disease and during exacerbations. Inflammation in the lung is also associated with a certain degree of systemic inflammation (2). For this reason, COPD has been considered as a systemic disease in recent years and some inflammatory mediators are responsible for COPD-related systemic manifestations (3, 4). A meta-analysis done by Gan et al. has shown that even patients with stable COPD have increased white blood cell count and elevated C-reactive protein (CRP), fibrinogen and cytokines (e.g. interleukin-1 beta, interleukin-6,tumor necrosis factor-alpha) levels (5). High levels of Prostaglandin E2 (PGE2), which is a pro-inflammatory mediator, correlates with the severity of airflow limitation in stable COPD (6). Therefore, PGE2 may be one of the major contributors to the pathogenesis of inflammation in COPD.
COPD Downloaded from informahealthcare.com by University of Newcastle on 09/28/14 For personal use only.
Effect of COPD on periodontal tissues
Periodontitis is a chronic inflammatory disease which serves as a reservoir of Gram-negative anaerobic organisms, lipopolysaccharides and some proinflammatory mediators (7). Among the pro-inflammatory mediators, PGE2 and interleukin-1 beta (IL-lβ) play critical roles in inflammatory processes leading to alveolar bone and connective tissue loss in periodontal disease (8–10). In periodontitis, the local destruction of the periodontal tissues causes a large surface area of ulcerated pocket epithelium which allows exchange between bacterial and host products (11). It has been suggested that while periodontitis may have systemic effects, some systemic diseases such as cardiovascular diseases, diabetes, respiratory diseases, adverse pregnancy outcomes and osteoporosis have negative effects on periodontal tissue (12–14). The relation between periodontal and systemic diseases is believed to be mediated through systemic inflammatory reactants such as acute-phase proteins and immune effectors, but the underlying biological mechanisms are yet unclear, and speculative (2, 13). The association between periodontal diseases and respiratory diseases has been discussed for years. Large-scale studies have been performed in patients with different respiratory diseases including COPD. These studies were designed to observe the effects of periodontal health on COPD (15–18). There is little information known about the effect of COPD and systemic inflammation in COPD in particular, on periodontal health. Our hypothesis was that COPD patients might have higher inflammatory response and worse periodontal health due to the subsequent pro-inflammatory events that occur in COPD when compared to non-COPD patients. The aim of this case-control study was to evaluate the effects of COPD on periodontal tissues by measuring clinical parameters and gingival crevicular fluid (GCF) IL-1β, PGE2 in addition to serum and GCF high-sensitive C-reactive protein (hs-CRP) levels.
Material and Methods Subjects and study design We screened the medical records of COPD patients (560 cases) who were followed on an outpatient basis by three chest clinics in Istanbul (Istanbul Medical Faculty Department of Respiratory Diseases, Yedikule Chest Diseases and Thoracic Surgery Training and Research Hospital and Sureyyapasa Chest Diseases and Thoracic Surgery Training and Research Hospital) between August 2008 and October 2011. Of 560 COPD patients, 440 who fulfilled the GOLD diagnostic criteria (1) were evaluated with regard to exclusion criteria. Patients with less than 8 teeth (n = 55) or who were edentulous (n = 288), as well as those who had significant respiratory diseases in addition to COPD (n = 6), a history of significant cardiovascular disorders or diabetes (n = 37), www.copdjournal.com
or a history of smoking in the last 2 years (n = 2) were excluded. As a result, 52 stable COPD patients fulfilling the inclusion criteria participated in the study. All patients were stable when included in the study (no infective exacerbation within one month prior to being included in the study). The COPD group (n = 52) was divided into two subgroups with regard to the disease severity; patients with mild and moderate COPD were included in group I and the patients with severe and very severe COPD were included in group II. Thirty-eight non-COPD controls who attended to Istanbul University, Faculty of Dentistry Department of Periodontology with matching age and gender constituted the control group. The controls with less than 8 teeth or who were edentulous or who had any respiratory diseases, significant cardiovascular disorders or diabetes were excluded. All controls were former smokers at least 2 years post-cessation of smoking. Local ethics committee of Istanbul University, Medical Faculty approved the study protocol (Project no. 2008/954), and informed written consent was obtained from all individuals prior to participation.
Assessment of COPD severity and lung function Forced expiratory volume in 1 second (FEV1), forced vital capacity (FVC) and FEV1/FVC ratio of the patients were measured via spirometry by trained and certified technicians and the results noted as percentages of the predicted values (FEV1% predicted). Later, the patients were divided into two subgroups, group-I (patients with mild-moderate COPD) and group-II (patients with severevery severe COPD) on the basis of FEV1% predicted values with regard to GOLD classification (1) (mild COPD: characterized by airflow limitation with FEV1 ≥80% predicted; moderate COPD: airflow limitation with ≤50% FEV1 < 80% predicted; severe COPD: airflow limitation with ≤30% FEV1 < 50% predicted; very severe COPD: airflow limitation with FEV1 < 30% predicted).
Periodontal examination The periodontal measurements including plaque index (PI) (19), gingival index (GI) (20), % of sites that had bleeding on probing (BoP), probing depth (PD), space between the cemento-enamel junction and gingival margin (SCG) and clinical attachment (CA) level were performed by the same blinded researcher (GO). An intraclass correlation coefficient of 0.85 for PD measurements indicated that the examiner reliability was high. PD and SCG were measured by William’s periodontal probe (Hu-Friedy, Chicago, IL) at six sites of all teeth (excluding third molars) and were recorded in millimeters. SCG was recorded as a positive value where the free gingival margin occurred apical to the cemento-enamel junction. CA level was calculated by CA level = PD + SCG formula.
425
COPD Downloaded from informahealthcare.com by University of Newcastle on 09/28/14 For personal use only.
426
Öztekin et al.
Gingival crevicular fluid and blood sampling The inflamed non-adjacent pocket sites of patients and controls were selected for gingival crevicular fluid (GCF) collections among the incisors and premolars with at least 4-mm depth. A total of 3 samples were collected to evaluate GCF level of IL-1β, PGE2 and hs-CRP from each patient. One sample was collected for each biomarker and analyzed separately. Sample collections were performed one week after the clinical measurements. Sample collections were performed 1 week after the clinical measurements. Briefly, after isolating the tooth with a cotton roll, the supragingival plaque was removed without touching the marginal gingival site and the crevicular site was gently air-dried. In order to avoid the contamination of saliva optimal effort was made. GCF was collected by paper strips (Periopaper, Oraflow Inc., NY, USA) positioned at the orifice of sulcus for 30 seconds. Strips with blood marks were discarded. The volume for each strip was measured with a calibrated meter (Periotron 6000, Oraflow Inc., NY, USA). The paper strips were immediately transferred to a plastic tube and stored at −80°C until analysis. For each assay, separate samples were collected and analyzed. The strips were not pooled. Fasting blood samples were collected in the anticoagulant-free vacutainer tubes by trained assistants and samples were immediately directed to the central biochemistry laboratory of Istanbul Medical Faculty for hs-CRP measurement. Biochemical analysis GCF was retrieved from the filter strips by eluting in 100-μl phosphate buffered saline solution-Tween buffer for 30 minutes and incubation on a shaking platform overnight (minimum 18 hours) for each parameter. GCF samples were analyzed for IL-1β, PGE2 (Invitrogen Co., Camarillo, CA, USA) and hs-CRP (R&D systems, Minneapolis, MN, USA), using commercially available sandwich enzyme linked immunosorbent assays according to the manufacturer’s instructions. The results of crevicular IL-1β and hs-CRP were expressed as ng/site and PGE2 as pg/site. Serum hs-CRP levels were measured by latexenhanced immuneturbidimetric assay using the Roche Modular P800 analyzer (Roche Diagnostics GmbH Mannheim, Germany) and results were expressed as mg/L. Statistical analysis The ideal sample size to assure adequate power for this cross-sectional study was calculated after a pilot experiment, and a 20% difference was obtained. With a power of 80% and α = 0.05, the minimum number of individuals required for the comparisons was 36 for each group. The data were evaluated with statistical software (SPSS Inc. Chicago, IL) and the results were presented as mean ± SD. Each patient was considered as an observation unit for periodontal clinical measurements and for each clinical parameter the average of the whole mouth measurements (excluding the third molars)
were used for statistical calculations. Demographic data analyses were done by using Pearson’s chi-square and independent sample t-test. The correlation between biochemical and clinical parameters were performed between the site that was sampled and the site’s clinical parameters. The comparison of demographical and clinical and biochemical parameters were performed by Mann–Whitney U-test. The relation between variables was evaluated by the Pearson correlation test.
Results Table 1 shows the demographical and clinical characteristics of COPD patients and the controls. The age, sex, time since the cessation of smoking and education status of the controls and COPD patients were similar. The number of teeth in COPD patients was significantly lower than the controls ( p < 0.001). PI and GI were significantly higher in COPD patients ( p < 0.001, p = 0.023 respectively). There was not a significant difference between the BoP and CAL scores of COPD patients and the controls. The number of sites with PD ≥ 4 mm was higher in the controls ( p < 0.04) but percentage of PD ≥ 4 mm was similar in both controls and COPD patients ( p = 0.14). GCF IL-1β and PGE2 levels, serum and GCF hs-CRP levels are presented in Table 2. The result of IL-1β levels and PGE2 levels were higher in COPD patients than the controls ( p < 0.001). The hs-CRP levels were significantly higher, both in GCF and serum of COPD patients when compared to the controls ( p = 0.01 and p = 0.035 respectively).
Table 1. Demographic and clinical variables of patients with COPD vs. controls Variable Age in years (mean ± SD)
Control (n = 38)
COPD Patients (n = 52)
p value
53.5 ± 9.2
57.5 ± 9.7
0.08
0.1
Gender (n; male/female)
32/6
49/3
(%; male)
85%
92%
6.8 ± 6.3
4.9 ± 4.3
0.07
Primary School
18
28
0.3
High School
9
11
Time since cessation of smoking in years (mean ± SD) Education (n)
Bachelor’s degree Number of teeth (mean ± SD)
11
13
22.2 ± 4.2
17.9 ± 5.1
