|Year : 2016 | Volume
| Issue : 3 | Page : 100-106
Assessment of role of Porphyromonas gingivalis as an aggravating factor for chronic obstructive pulmonary disease patients with periodontitis
Roopa Madalli1, Supriya Kheur1, Mamatha G. S. Reddy1, Mohit Kheur2, Aditi Mahalle1
1 Department of Oral Pathology and Microbiology, Dr. D.Y. Patil Vidyapeeth's, Dr. D.Y. Patil Dental College and Hospital, Pune, Maharashtra, India
2 Department of Prosthodontics, M A Rangoonwala Dental College, Camp, Pune, Maharashtra, India
|Date of Web Publication||14-Sep-2016|
Department of Oral Pathology and Microbiology, Dr. D.Y. Patil Vidyapeeth's, Dr. D.Y. Patil Dental College and Hospital, Pimpri, Pune, Maharashtra
Source of Support: None, Conflict of Interest: None
Introduction: Periodontitis is a chronic inflammatory disease associated with a number of lung conditions such as chronic obstructive pulmonary disease (COPD) and pneumonia. Both chronic periodontitis (CP) and COPD share similar risk factor profiles. Thus, recognition of interaction between periodontitis and COPD could lead to establishment of better preventive and therapeutic approaches. The microbial analysis of sputum from COPD patients with CP to detect periodontal pathogen Porphyromonas gingivalis (P. gingivalis) both before and after nonsurgical periodontal therapy. Materials and Methods: The study group comprised 30 individuals diagnosed as COPD with CP. Periodontal indices, lung function test, and P. gingivalis in sputum were assessed before and 6 months after nonsurgical periodontal therapy. Results: A decrease in the count of P. gingivalis and decreased periodontal indices values were observed in COPD patients with periodontitis after nonsurgical periodontal therapy. Lung function test (forced expiratory volume in the first/forced vital capacity) was improved in COPD patients with periodontitis after nonsurgical periodontal therapy. Conclusions: The study results suggest that nonsurgical periodontal therapy can be a part of treatment protocol in COPD patients because it helps in reducing the P. gingivalis count and improving the lung function.
Keywords: Chronic obstructive pulmonary disease, oral prophylaxis, periodontal disease, P. gingivalis
|How to cite this article:|
Madalli R, Kheur S, Reddy MG, Kheur M, Mahalle A. Assessment of role of Porphyromonas gingivalis as an aggravating factor for chronic obstructive pulmonary disease patients with periodontitis. Dent Hypotheses 2016;7:100-6
|How to cite this URL:|
Madalli R, Kheur S, Reddy MG, Kheur M, Mahalle A. Assessment of role of Porphyromonas gingivalis as an aggravating factor for chronic obstructive pulmonary disease patients with periodontitis. Dent Hypotheses [serial online] 2016 [cited 2021 Sep 19];7:100-6. Available from: http://www.dentalhypotheses.com/text.asp?2016/7/3/100/190485
| Introduction|| |
The oral cavity is connected with the trachea and the entire respiratory apparatus. It has been considered to be a portal of exit and entry for respiratory pathogen colonization as it is a potential reservoir for respiratory pathogens. , Respiratory diseases include conditions from common cold to conditions such as bacterial pneumonia or chronic obstructive pulmonary disease (COPD), some of which constitute an important cause of death reported worldwide. 
COPD is a condition in which chronic obstruction to airflow occurs, with excess production of sputum as a result of chronic bronchitis and/or emphysema. , It is caused by failure of the host to clear the bacteria which is caused by the microaspiration of oropharyngeal secretions containing bacteria into the lung.  Depending on the relationship between the anatomical position of oral cavity and pulmonary infection, oral bacteria can be easily carried into the lung.  Periodontal disease (PD) is a putrid festering infection of the mouth. Bacteria and inflammatory particles can enter the blood stream through ulcerated and bleeding gums and can travel to other vital organs such as the heart and lungs. PD and COPD share the same risk factors, including smoking, age, obesity, socioeconomic status, and living conditions. 
Poor oral hygiene is an ignored, neglected, and unsolved problem which in the Indian population is an alarming situation. The people with poor oral hygiene were 4.5-fold more likely to have a chronic respiratory diseases than those with normal oral hygiene. , Dental plaque can be colonized by respiratory pathogens, which may be aspirated from the oropharynx into the upper airway and then reach the lower airway and adhere to the bronchial or alveolar epithelium. , Exacerbation and progression of COPD depend on the initial colonization of microbial pathogens to oral/pharyngeal surfaces. The pathogens are subsequently shed into salivary secretions, together with oral bacteria and proinflammatory enzymes. Thus, the contents of this secretion may contaminate and cause changes in the respiratory epithelium. ,,
Porphyromonas gingivalis, a gram-negative asaccharolytic bacterium, has been recognized as a key causative microbe in the pathogenesis of destructive chronic periodontitis. , Virulence factors of P. gingivalis such as lipopolysaccharides (LPS), fimbriae, toxic products of metabolism, and proteases have been identified to activate defensive response processes of host cells, leading to release of inflammatory mediators and chronic inflammation.  Many proposed mechanisms of oral bacteria in the pathogenesis of respiratory infection have already been suggested. ,,,, In addition, the extensiveness of periodontitis increases together with the severity of COPD. Mortality and morbidity caused by COPD is quite alarming affecting the quality of life.
Improved oral hygiene has been shown to decrease the incidence and progression of pulmonary infection in both mechanically ventilated hospital patients and nursing home elderly residents. It is conceivable that oral interventions that improve oral health status may prove to lower the extremity of lung infection in susceptible populations. There is increasing evidence suggesting improvement in the respiratory symptoms of patients with COPD after oral prophylactic treatment. ,,,,
Hence, the present study aims at assessing the periodontal pathogen P.gingivalis in the sputum of COPD patients and correlating it with respiratory symptoms and periodontitis so as to possibly help in designing treatment strategies to improve quality of life in the patients suffering from debilitating respiratory ailments.
| Materials and Methods|| |
The study group comprised 30 individuals diagnosed with COPD and chronic periodontitis from the outpatient Department of Pulmonology, Dr. D.Y. Patil Medical College. Informed consent was obtained from the participants before the start of the study. The study was divided into two main groups; group A consisting of 30 individuals diagnosed with COPD suffering from chronic periodontitis before oral prophylaxis as baseline; group B consisting of 30 individuals diagnosed with COPD and suffering from chronic periodontitis after oral prophylaxis.
Patient screening and selection
Patients with COPD were screened in the Department of Pulmonology, Dr. D.Y. Patil Medical College. Criteria used for the diagnosis of COPD were based on the Global Initiative for Chronic Obstructive Lung Disease (GOLD) spirometry guidelines (Rabe et al. 2007). 
Individuals suffering from COPD with chronic periodontitis, aged ≥40 years. Presence of at least 20 teeth in the mouth and patients willing to give consent for the study.
COPD patients suffering from other systemic diseases such as diabetes, cardiovascular disease; COPD patients suffering from tuberculosis; COPD patients on immunosuppressant therapy; and patients unwilling to give consent for the study.
Assessment of lung function by Spirometry
Lung function was recorded using spirometry, which was conducted by trained and certified technicians. The severity of COPD was graded according to the "GOLD COPD" staging system,  as Stage-I Mild Forced Expiratory Volume 1 /Forced Vital Capacity (FEV 1 /FVC<80%), Stage-II Moderate FEV 1 /FVC<79-50%, Stage-III Severe FEV 1 /FVC<49-30%), Stage-IV Very severe FEV 1 /FVC<30%. Diagnostic criteria for COPD: FEV 1 /FVC<70%.
Diagnostic criteria for chronic periodontitis: Community Periodontal Index (CPI) score of 3 or above; loss of attachment (LOA) score of 1 or above.
Sputum samples were collected from COPD patients in a sterile glass tube by the "spitting method." Immediately after collection, it was transferred to Eppendorf tubes containing transport media: Reduced Transport Fluid (RTF). Collected samples were taken to the research laboratory for further processing.
All dental treatment was performed by Periodontists in the Department of Periodontology. CPI and LOA for periodontitis, lung function parameters FEV 1 /FVC were recorded, and sputum samples were collected for P. gingivalis assessment before treatment. Supragingival scaling was done and oral hygiene instructions were given to all the patients. Because there can be bacterial contamination via aerosols during dental treatment, it requires to be done along with preprocedural antibiotics and high volume suction.  Thus, to avoid any complications, the study involved thorough supragingival cleaning. The same patients were followed up after 3-5 months as part of the study protocol, and all the above clinical CPI and LOA for periodontitis were re-recorded. Sputum samples were collected again for P. gingivalis analysis.
Analysis of Porphyromonas gingivalis
DNA extraction procedure (Modified Proteinase-K method) was used. Following set of polymerase chain reaction (PCR) primers were used which are specific to P. gingivalis as Forward primer: AGG CAG CTT GCC ATA CTG CG, and Reverse primer: ACT GTT AGC AAC TAC CGA TGT.  Amplified products were subjected to electrophoresis through 2% Agarose gel containing 1 × TAE, 20 μl of each amplified product were mixed with 3 μl of bromophenol blue loading dye, and electrophoresis was performed at 25 V for 2 h. The gel was visualized under ultraviolet (UV) light illuminator after staining with ethidium bromide (0.5μg/ml). P. gingivalis was recognized at base pair 500bp. 
Same method of data collection was used to collect the sputum samples 3-5 months after nonsurgical periodontal therapy and the same abovementioned methods were performed.
All the values were recorded and tabulated for both the study groups. The values were analyzed statistically using paired t-test and Wilcoxon signed Rank test.
Two patients were lost to follow-up, and hence sample size was reduced to 28 patients.
| Results|| |
Majority of the COPD patients were males (M = 82.14%; F = 17.86%). Age range of the patients was from 40 to 80 years. Patients in the 6 th decade showed high incidence of COPD (39.29%). A complete history of tobacco abuse was taken from all the patients. The 28 patients being evaluated 6 (21.43%) did not give history of any form of adverse habit. Most of the patients 19 (67.86%) gave history of smoking cigarettes.
When the CPI values were compared, before and after the treatment, the mean and standard deviation were decreased, however, it was noted that mean value was not significantly different (P > 0.05) [Table 1]. The mean and standard deviation for LOA was not altered in both the groups, and hence it was noted that mean value was not significantly different between the pre and post-treatment groups (P > 0.05) [Table 2].
|Table 1: Comparison of pre and post-treatment community periodontal index and loss in attachment in study groups|
Click here to view
|Table 2: Comparison of pre and post-scaling P. gingivalis by polymerase chain reaction method in study group|
Click here to view
Mean value of FEV 1 /FVC increased between the two groups [Table 3], however, there were no statistical significant differences (P > 0.05).
Out of 28 patients, it was noted that 50% of the cases (n = 14) were positive for P. gingivalis before treatment, and after treatment 28.57% (n = 8) were positive for P. gingivalis. Comparison between P. gingivalis from the sputum of COPD patients before and after treatment showed a decrease in the bacterial load. Wilcoxon signed Rank test was applied which showed Z = 1.73 [Table 2]. The culture of the sputum samples for P. gingivalis was also done along with PCR. PCR analysis yielded better results than culture.
| Discussion|| |
COPD is one of the most frequent respiratory diseases. The high prevalence and mortality of COPD worldwide constitutes an enormous public health and medical challenge for the development and implementation of effective preventive and treatment strategies.  The association between periodontitis and COPD has been increasingly recognized over the last two decades. In line with the relationship between the anatomical position of oral cavity and pulmonary infection, oral bacteria can be easily carried into the lung and may seed the infection. 
Patients with COPD in our study showed a male predominance (M = 82.14%; F = 17.86%). Patients in the 6 th decade showed high incidence of COPD (39.29%). A complete history of tobacco abuse was taken from all the patients enrolled. Most of the patients 19 (67.86%) gave history of smoking cigarettes. The 28 patients being evaluated 6 (21.43%) did not give history of any form of adverse habit. Most of the studies have shown a strong association between smokers and periodontitis associated with COPD. ,,, However, few studies have shown a strong link of PD-COPD among study group comprising 63% of nonsmokers. 
There are many studies that show that smoking is a major environmental factor associated with accelerated periodontal destruction ., The main risk factor for COPD is smoking. The cross-sectional study carried out by Hyman et al. on a large group of adults revealed a strong association of smoking with COPD and periodontitis.  A detailed observational study by Peter et al. also suggested that a strong correlation exists between poor periodontal health and lung obstructive disease.  However, the study carried out by Thomsen et al. reported that never-smokers with COPD had different characteristics and milder disease, limited to the lungs. However, the morbidity levels were substantial in never-smokers with COPD. 
To reduce the bias created by smoking as a contributing factor we did a rescaling and post-scaling analysis correlating smoking with the presence of P. gingivalis in our study group [Table 4] and [Table 5], which was not significant.
|Table 4: Comparison of P. gingivalis with smoking and nonsmoking in pre-scaling study groups|
Click here to view
|Table 5: Comparison of P. gingivalis with smoking and nonsmoking in post-scaling study groups|
Click here to view
Air pollution, second-hand smoke, history of childhood respiratory infections, genetic factors, and heredity are among other risk factors for COPD. ,
Mean values of FEV 1 /FVC increased between the two study groups [Table 3]. The mean was 48.08% in group A and 51.25% in group B. Overall, there were no significant differences in FEV 1 /FVC between the two treatment groups, however, an improvement in the lung function test was noted. Scannapieco et al. showed that lung function decreased with increasing periodontal attachment loss. Therefore, they concluded that a potential association between periodontitis and chronic pulmonary diseases such as COPD may exist. , According to the study by Zhou et al.,  the means of pulmonary function test FEV 1 and FEV 1 /FVC increased at 1-year and at 2-year follow-up in both therapy groups. Ghana et al.  showed that as clinical attachment loss (CAL) levels increases, mean FEV 1 /FVC ratio decreases-an inverse relation between CAL (periodontal disease) and FEV 1 /FVC% (COPD). As our study was of short a duration of 3-5 months, we could not notice much significant changes in the lung function values, as the abovementioned study by Zhou et al.
In the present study, it was seen that when the CPI values were compared between pre and post-treatment group, it was noted that the mean value was decreased. The mean and standard deviation for LOA was not altered in both the groups, and hence the mean value was not significantly different between the pre and post-treatment groups (P > 0.05). The treatment protocol followed for the study was oral prophylaxis, i.e., supragingival scaling without any surgical intervention with the oral hygiene instructions, and the follow-up period was of short duration of 3-5 months, such that we could not get significant changes in the value of CPI and LOA.
Zhou et al. found that there were significant improvements in lung function and a reduction in the frequency of COPD exacerbations as a result of periodontal treatments such as scaling and root planning.  Kucukcoskun et al. studied periodontal parameters measured at baseline and 6 and 12 months. The test group showed a significant reduction in the exacerbation frequency during the follow-up period (P = 0.01). Therefore, they pointed that initial periodontal therapy in patients with COPD and CP may decrease the exacerbation frequency.  Benazir Ghani et al. showed that the mean levels of oral hygiene index (OHI), plaque index (PI), gingival index (GI), probing pocket depth (PPD), and clinical attachment level (CAL) were significantly (P < 0.001) higher in cases whereas FEV 1 /FVC ratio was significantly (P < 0.001) lower as compared to controls.  In one of the studies by Scannapieco et al., they found a nearly five-fold increase in chronic respiratory diseases in individuals who had poor oral hygiene when compared to those with good oral hygiene.  Azarpazhooh et al. in their systematic review stated that oropharyngeal decontamination with different antimicrobial interventions reduces the progression or occurrence of respiratory diseases.  Scannapieco et al. in their systematic review stated that results associating periodontal diseases in COPD are preliminary, and more epidemiological and interventional studies are required to prove the confirmatory-based association. 
Poor oral hygiene results in an increase in mass and complexity of dental plaque, which may foster bacterial interactions between indigenous plaque bacteria (P. gingivalis, Fusobacterium nucleatum) and acknowledged respiratory pathogens (Pseudomonas aeruginosa, Klebsiella pneumoniae), which are shed into saliva.  In a retrospective longitudinal study, it has been shown that dental plaque can serve as a reservoir for potential respiratory pathogens.
Several mechanisms may be considered for the effect of periodontal therapy on COPD. First, periodontal therapies can reduce plaque and oral mucosa colonization with respiratory pathogens. Second, periodontal therapies may decrease periodontal pathogens. The products of periodontal pathogens can promote airway inflammation and exacerbations. A large number of inflammatory factors are released continuously from periodontal lesions and peripheral mononuclear cells, which may induce a more severe inflammatory response in COPD. ,
Measuring periodontitis-related antibody titers might be useful for identifying patients with susceptibility to frequent exacerbations so that an aggressive prevention strategy can be designed. ,,,
This study compared the levels of P. gingivalis from the sputum of COPD patients before and after oral prophylaxis, which showed a decrease in the level of microorganism. Wilcoxon signed Rank test was applied which showed Z = 1.73 [Table 3]. It was noted in our study that 50% of the patients (14 patients) were positive for P. gingivalis in the pretreated cases and (28.57%) were positive in the post-treated cases; P > 0.05 which was not significant.
The results suggest that the oral prophylactic treatments may have removed large numbers of plaque bacteria, including both periodontal and respiratory pathogens, reducing the bacterial load in the saliva. Furthermore, considering the fact that the scaling is a relatively simple treatment without any surgical intervention and with no side effect, we suggest that it may be a cost-effective periodontal treatment for COPD patients.
| Conclusion|| |
Periodontal disease and the systemic interlink, although well-researched in the scientific community, is not universally accepted among clinicians. Many of the periodontal pathogens are also implicated in the etiology of several systemic diseases, which are caused by the microaspiration of oropharyngeal secretions containing bacteria into the lung and failure of the host to clear the bacteria. A cause and effect relationship between the health condition of the oral cavity and some systemic diseases is attributed to the presence of dental plaque and periodontal infection .
Oral prophylaxis is a relatively simple and noninvasive procedure, with no known side effect; we suggest that it may be a cost-effective periodontal adjunct treatment for COPD patients. The procedure reduces bacterial load, thereby significantly reducing the systemic bacteremia. In the present study, the oral prophylaxis was performed by different qualified dentists. Thus, one of the limitations of the present study was an absence of interexaminer reliability test.
A future treatment strategy can be designed by including effective oral hygiene protocol, frequent recare intervals, as essential paradigm for maintaining oral and systemic health in patients with COPD. Thus, it can be hypothesized that effective periodontal therapy can in turn reduce sputum contamination and eventual spread in the respiratory system. Moreover, because we had tried to do microbiological culture and PCR, it is possible that we lost the bacterial DNA as a procedural drawback. Typing and sequencing, as the next step with cytokine profiling will enable us to see a clear picture regarding the association of the P. gingivalis contamination with the overall health of COPD patients.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Paju S, Scannapieco FA. Oral biofilms, periodontitis and pulmonary infections. Oral Dis 2007;13:508-12.
Wang Z, Zhou X, Zhang J, Zhang L, Song Y, Hu FB, et al
. Periodontal health, oral health behavior and chronic obstructive pulmonary disease. J Clin Periodontal 2009;36:750-5.
Donald S. The link between periodontal disease and upper respiratory diseases. Inside Dent 2011;7.
Georgiou TO, Marshall RI, Barlod PM. Prevalence of systemic diseases in Brisbane general and periodontal practice patients. Aust Dent J 2004;49:177-84.
Gomes-Filho IS, Passos JS, Seixas da Cruz S. Respiratory disease and the role of oral bacteria.
J Oral Microbiol 2010;2.
Cullinan MP, Ford PJ, Seymour GJ. Periodontal disease and systemic health: Current status. Aust Dent J 2009;54:S62-9.
Maeda H, Kokeguchi S, Fujimoto C, Tanimoto I, Yoshizumi W, Nishimura F, et al
. Detection of periodontal pathogen Porphyromonas gingivalis by loop-mediated isothermal amplification method. FEMS Immunol Med Microbiol 2005;43:233-9.
Gomes-Filho IS, Santos CM, Cruz SS, Passos Jde S, Cerqueira Ede M, Costa Mda C, et al
. Periodontitis and nosocomial lower respiratory tract infection: Preliminary findings. J Clin Periodontal 2009;36:380-7.
Gurenlian JR. Periodontal Disease and Respiratory disease. Academy of Laser Dentistry Meeting, April 2009; 22-25.
Wadzicha, Seemungal TA. COPD exacerbations: Defining their cause and prevention. Lancet 2007;370:786-96.
Bansal M, Khatri M, Taneja V. Potential role of periodontal infection in respiratory diseases-a review. J Med Life 2013;6:244-8.
Zaghloul MZ. The Contribution of Anaerobic Bacteria that Causes Periodontitis in the Pathogenesis of Chronic Obstructive Pulmonary Disease (COPD). Air Water Borne Diseases 2014;3:e128.
Rabe KF, Hurd S, Auzueto A, Barnes PJ, Buist SA, Calverly P, et al
. Global strategy for the diagnosis, management and prevention of Chronic Obstructive Pulmonary Disease. GOLD executive summary. Am J Respir Crit Care Med 2007;176:532-55.
Zhou X, J Han, Liu Z, Song Y, Wang Z, Sun Z. Effects of periodontal treatment on lung function and exacerbation frequency in patients with chronic obstructive pulmonary disease and chronic periodontitis: A 2-year pilot randomized controlled trial. J Clin Periodontol 2014;41:564-72.
Deo V, Bhongade ML, Ansari S, Chavan RS. Periodontitis as a potential risk factor for chronic obstructive pulmonary disease: A retrospective study. Indian J Dent Res 2009;20:466-70.
Ghani B, Bhattacharya HS. To evaluate association between periodontal disease and chronic obstructive pulmonary disease. Indian J Dent Sci 2014;1:41-4.
Sharma N, Shamsuddin H. Association between respiratory disease in hospitalized patients and periodontal disease: A cross-sectional study. J Periodontol 2011;82:1155-60.
Agado B, Bowen DM.
Does the link between COPD and periodontitis affect dental hygiene treatment? Access 2009;23:19-21.
Pelt Verkuil EV, Belkum AV, Hays JP. The Different Types and Varieties of Nucleic Acid Target Molecules. In: Verkuil P EV, Belkum AV, Hays JP, editors. Principals and Technical aspects of PCR amplification. The Netherland: Springer Science; 2008. p. 34-43.
D′Ercole S, Piccolomini R, Capaldo G, Catamo G, Perinetti G, Guida L. Effectiveness of ultrasonic instruments in the therapy of severe periodontitis: A comparative clinical-microbiological assessment with curettes. New Microbiol 2006;29:101-10.
Azarpazhooh A, Leake JL. Systematic review of the association between respiratory diseases and oral health. J Periodontol 2006;77:1465-82.
Haffajee AD, Socransky SS. Relationship of cigarette smoking to attachment level profiles. J Clin Periodontol 2001;28:283-95.
Bergström J, Cederlund K, Dahlén B, Lantz AS, Skedinger M, Palmberg L, et al
. Dental health in smokers with and without COPD. PLoS One 2013;8:e59492.
Hyman JJ, Reid BC. Cigarette smoking, periodontal disease: And chronic obstructive pulmonary disease. J Periodontal 2004;75:9-15.
Peter KP, Mute BR, Doiphode SS, Bardapurkar SJ, Borkar MS, Raje DV. Association between periodontal disease and chronic obstructive pulmonary disease: A reality or just a dogma? J Periodontol 2013;84:1717-23.
Thomsen M, Nordestgaard BG, Vestbo J, Lange P. Characteristics and outcomes of chronic obstructive pulmonary disease in never smokers in Denmark: A prospective population study. Lancet Respir Med 2013;1:543-50.
Scannapieco FA, Bush RB, Paju S. Association between periodontal diseases and risk for nosocomial bacterial pneumonia and chronic obstructive pulmonary disease: A systematic review. Ann Periodontol 2003;8:54-69.
Kucukcoskun M, Baser U, Oztekin G, Kiyan E, Yalcin F. Initial periodontal treatment for prevention of chronic obstructive pulmonary disease exacerbations. J Periodontol 2013;84:863-70.
El-Solh AA, Pietrantoni C, Bhat A, Okada M, Zambon J, Aquilina A, et al
. Colonization of dental plaques: A reservoir of respiratory pathogens for hospital acquired pneumonia in institutionalized elders. Chest 2004;126:1575-82.
Senpuku H, Sogame A, Inoshita E, Tsuha Y, Miyazaki H, Hanada N. Systemic diseases in association with microbial species in oral biofilm from elderly requiring care. Gerontology 2003;49:301-9.
Takahashi T, Muro S, Tanabe N, Terada K, Kiyokawa H, Sato S, et al
. Relationship between periodontitis-related antibody and frequent exacerbations in chronic obstructive pulmonary disease. PLoS One 2012;7:40570.
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5]
|This article has been cited by|
||Effect of periodontal therapy on COPD outcomes: a systematic review
| ||Ioulianos Apessos,Athanasios Voulgaris,Michalis Agrafiotis,Dimitrios Andreadis,Paschalis Steiropoulos |
| ||BMC Pulmonary Medicine. 2021; 21(1) |
|[Pubmed] | [DOI]|
||Relación entre la enfermedad periodontal y la enfermedad pulmonar obstructiva crónica: revisión de la literatura
| ||Sandra Milena Moreno Correa,Andrés Felipe Bolaños,Juan José Jaramillo,Alexandra Jimenez,Freddy Moreno |
| ||Universitas Médica. 2020; 61(3) |
|[Pubmed] | [DOI]|
||A Clinical and Radiographical Study to Assess and Correlate Chronic Obstructive Pulmonary Disease and Periodontitis
| ||Sai Darshana Nair,Alluri Siddhartha Varma,Girish Suragimath,Sameer A Zope,Apurva Pisal,Rashmi Gangavati |
| ||World Journal of Dentistry. 2019; 10(5): 354 |
|[Pubmed] | [DOI]|