Clinical Research
The Influence of Periodontal Status on Endodontically Treated Teeth: 9-year Survival Analysis Navid Khalighinejad, DDS, Anita Aminoshariae, DDS, MS, James C. Kulild, DDS, MS, Jeannie Wang, DMD, and Andre Mickel, DDS, MS Abstract Introduction: The aim of this study was to investigate the effect of periodontal status at the time of nonsurgical root canal treatment (NSRCT) on the survival rate of endodontically treated teeth (ETT). Methods: In this retrospective investigation, molars that received NSRCT in an advanced specialty education program in endodontics from 2009 through 2017 were initially recruited. After the application of inclusion and exclusion criteria, 315 teeth were included in the study. Inclusion criteria were ETT with an acceptable quality of NSRCT; ETT that received an adequate crown within 3 months after NSRCT; and ETT with complete periodontal charting before NSRCT including pocket depths, clinical attachment loss, and bone loss. The periodontal status of all included teeth was assessed based on American Academy of Periodontology guidelines. All included ETT were divided into 3 groups as follows: healthy group, mild periodontitis, and moderate periodontitis. The survival rate of ETT was analyzed using univariate Kaplan-Meier and log-rank tests for differences between groups (P < .05). A Cox regression model was used to assess the effect of independent variables on the survival rate. Results: Teeth that were diagnosed with mild periodontitis were almost 2 times more likely to be extracted compared with ETT diagnosed with normal periodontium at the time of NSRCT (odds ratio [OR] = 1.9, P < .05). This increased risk of tooth loss was 3.1 (OR = 3.1, P < .05) for ETT diagnosed with moderate periodontitis. Smokers were twice as likely to have tooth loss compared with nonsmokers (OR = 2.2, P < .05). Conclusions: Patients’ periodontal health, being 1 of the prognostic determinants of the outcome of NSRCT, requires attention before and subsequent to NSRCT. This may improve the survival of ETT and help patients maintain their natural dentition. (J Endod 2017;-:1–5)
Key Words Endodontic, nonsurgical root canal treatment, outcome, periodontal disease, periodontitis, survival rate
T
he aim of endodontic Significance and periodontal treatOne of the prognostic determinants of NSRCT is ment therapies is to retain patients' periodontal health. The results of this the natural dentition in a investigation reported that attention before and healthy and functional subsequent to NSRCT is required to optimize endstate (1). These treatments odontic survival rate. are both predictable and have high survival rates (2, 3). In order to enhance the effectiveness of these treatments, it may be prudent to recognize related factors that could influence the long-term survival of these teeth (4, 5). Previous studies have detailed the influence of concurrent endodontic and periodontal treatments on the long-term survival of molars (3, 5, 6). Pretzl et al (1) reported that ‘‘root canal treatments contribute significantly to the loss of molars in patients under periodontal treatment.’’ However, confounding variables such as the quality of nonsurgical root canal treatment (NSRCT) (7) and postendodontic restoration (2) that could have influenced the survival of endodontically treated teeth (ETT) were not considered in these studies. This might affect the reliability of these studies. Therefore, the current investigation was designed to investigate the concurrent effect of endodontic and periodontal treatment on the long-term survival of ETT while controlling for confounding variables. Periodontal disease is known as 1 of the main reasons for tooth extraction after NSRCT (8–11). Only a few studies have assessed the effect of preoperative periodontal status of a tooth on the survival of ETT (10, 12). It was reported that probing depths deeper than 5 mm are associated with an increased risk of tooth loss after NSRCT (12). However, in this study, only pocket depth was used, and other periodontal prognostic factors such as clinical attachment loss and bone loss (6) were not included in the analysis. Furthermore, supportive periodontal treatments are significantly associated with higher long-term survival of molars (1, 3, 5). Despite this fact, no study has assessed the effect of supportive periodontal therapy (SPT) on the survival of ETT. According to the American Academy of Periodontology (13), periodontal disease severity can be categorized based on the amount of clinical attachment loss and bone loss. Therefore, the aim of the present study was to investigate the effect of periodontal
From the Department of Endodontics, Case Western Reserve University, School of Dental Medicine, Cleveland, Ohio. Address requests for reprints to Dr Anita Aminoshariae, Case School of Dental Medicine, 2123 Abington Road A 280, Cleveland, OH 44106. E-mail address:
[email protected] 0099-2399/$ - see front matter Copyright ª 2017 American Association of Endodontists. http://dx.doi.org/10.1016/j.joen.2017.06.022
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Clinical Research status of a tooth at the time of NSRCT and the role of supportive periodontal treatment on the survival rate of ETT.
Materials and Methods The protocol of the present retrospective study was approved by the Committee on Research Involving Human Subjects, Case Western Reserve University (CWRU), Cleveland, OH. Study data were collected and managed using General Systems Design Group (Cedar Rapids, IA) academic data capture tools hosted at CWRU. Existing patients’ electronic records based on the American Dental Association Code on Dental Procedure and Nomenclature identified all mature permanent molars that had received NSRCT at the endodontic department performed by postgraduate students using a dental operating microscope between January 1, 2008, and January 1, 2017. Records were restricted to active school patients. These patients were initially treated at the CWRU screening dental clinic and received a complete periodontal assessment before NSRCT. Also, screened patients were active school patients who regularly came to CWRU School of Dental Medicine for recall visits. These preliminary inclusion criteria resulted in 635 ETT from 754 patients. Patients’ records, radiographs, and computerized databases were retrospectively examined to identify samples that matched the final inclusion criteria in the present study. Inclusion data for ETT were as follows: 1. Patients between 18 and 75 years of age in good health (American Society of Anesthesiologists classification I or II). 2. ETT with an acceptable quality of NSRCT according to the criteria suggested by Tronstad et al (14) and Farzaneh et al (15). 3. ETT with a preoperative diagnosis of irreversible pulpitis. In order to standardize the results of the data and to minimize the risk of pulpal status as a confounding variable, the authors limited the investigation to only irreversible pulpitis (16). 4. ETT with complete periodontal charting before NSRCT including pocket depths and clinical attachment loss, degree of mobility, and radiographic bone loss. 5. Restorable teeth with at least a 2-mm coronal dentin height and at least a 1-mm dentinal thickness have been included to provide an adequate ferrule effect as described by Ferrari et al (17). 6. ETT that received an adequate crown within 3 months after NSRCT, which was confirmed by the absence of open/defective margins based on a clinical and radiographic examination. 7. Teeth with no detectable crack(s) under a dental operating microscope during the NSRCT. Teeth with no preoperative radiographs before the initial NSRCT, teeth lost to follow-up, and cases with true combined endodonticperiodontal lesions that need advanced periodontal therapy were excluded (18). Also, ETT teeth with suspected vertical root fracture (19) and with any operative mishaps such as a perforation and/or a separated file were excluded. After the application of the inclusion criteria, all included ETT were divided into 3 groups to assess the influence of various periodontal statuses on the survival of ETT: 1. ETT with no periodontal disease at the time of NSRCT (healthy/control group, n = 125) 2. ETT diagnosed with mild periodontitis (mild group, n = 100) 3. ETT diagnosed with moderate periodontitis (moderate group, n = 90) The periodontal status of all ETT was assessed based on the criteria of the American Academy of Periodontology (13). According to this guideline, teeth with less than a 5-mm probing depth, 1- to 2-mm attachment 2
Khalighinejad et al.
loss, and up to 15% radiographic bone loss were diagnosed with mild periodontitis. Also, teeth with probing depths between 5 and 7 mm, 3- to 4-mm attachment loss, and less than 30% bone loss were diagnosed with moderate periodontitis. ETT diagnosed with severe periodontitis at the time of NSRCT were excluded from the study (n = 13). Finally, screening of the ETT that met the inclusion criteria yielded 315 ETT (1 tooth per patient) included in the final analysis. The following characteristics were collected from the patients’ records: 1. Patient’s age, sex, and the dental arch of the ETT (maxilla v mandible) 2. Self-reported smoking status was assessed using 2 categories (ie, never smoked or former smoker who quit >5 years previously) or current smoker as described by Lang and Tonetti (20) 3. Date of NSRCT initiation and completion 4. Date and reason of an extraction if available 5. Status of periodontal health (normal periodontal status, mild periodontitis, or moderate periodontitis) at the time of NSRCT 6. Whether or not patients participated in the SPT at the periodontal department after NSRCT on a regular basis; SPT included clinical measurements, assessment of the plaque control record (21), and, if necessary, subgingival reinstrumentation of sites with a probing pocket depth of 4 mm that also had bleeding on probing or pocket depths of 5 mm and more (5) In the present study, survival was defined as the presence of the ETT in the oral cavity by the end of the study (January 1, 2017). The time lapse between NSRCT and extraction was registered if the ETT were extracted during the study period. ETT with no extraction codes were considered to have survived, and the time lapse between NSRCT and the end of this study was calculated for these teeth. The date of the last recall visit of the patient was also recorded as the censoring date for ETT that were not extracted during the study period. Statistical analysis was performed using SPSS 19 (SPSS Inc, Chicago, IL) and R version 2.8.0 (Foundation for Statistical Computing, Vienna, Austria). The survival rate of ETT was analyzed using univariate Kaplan-Meier and log-rank tests for differences between groups (P < .05). The annual failure rates were calculated from life tables. A multivariate Cox regression model was performed to analyze the imposed risk of independent variables such as periodontal status (normal/mild periodontitis/moderate periodontitis) and regular SPT (yes/no) on the outcome variable (survival/extraction), controlling for the confounding variables at a significance level of 0.05.
Results In the present study, 315 teeth from 315 individuals with a mean age of 54 years were included for analysis. Of these patients, 125 teeth (39.6%) were diagnosed with a healthy periodontium, 100 teeth (31.7%) were diagnosed with mild periodontitis, and 95 teeth (30.1%) were diagnosed with moderate periodontitis at the time of NSRCT. Table 1 details the distribution and characteristics of the included teeth. In this 9-year retrospective study, 20 ETT (6.3%) were extracted, and 295 (93.7%) survived to the end of the follow-up time or study (January 1, 2017). Prognostic variables for univariate survival analysis included periodontal diagnosis at the time of NSRCT (healthy/mild periodontitis/moderate periodontitis), receiving SPT (yes/no), dental arch, sex, and history of smoking. Three factors that were significantly (P < .05) correlated with the survival of the ETT were as follows: periodontal diagnosis, SPT provided, and smoking. JOE — Volume -, Number -, - 2017
Clinical Research TABLE 1. Tooth-level and Patient-level Characteristics of Endodontically Treated Teeth in Different Groups Characteristics Age (y) Sex Male Female Smoking Active Never/former Dental arch Maxilla Mandible Supportive periodontal treatment Yes No
Healthy periodontium (n = 125), n (%)
Mild periodontitis (n = 10), n (%)
Moderate periodontitis (n = 95), n (%)
P value (t test and chi-square)
49
53
60
.67
73 (58.4) 52 (41.6)
56 (56) 44 (44)
46 (48.4) 49 (51.6)
.08
49 (39.2) 76 (60.8)
38 (38) 62 (62)
40 (42.1) 55 (57.9)
.44
64 (51.2) 61 (48.8)
41 (41) 59 (59)
38 (40) 57 (60)
.12
70 (56) 55 (44)
51 (51) 49 (49)
48 (50.5) 42 (49.5)
.7
The significance level is P = .05.
Kaplan-Meier survival curves as a function of independent periodontal parameters are shown in Figures 1 and 2. The 9-year survival rate after NSRCT was 90% for teeth with a healthy periodontium at the time of NSRCT. For ETT with mild periodontitis, the 9-year survival rate after NSRCT was 71%. Also, teeth with moderate periodontitis showed the lowest 9-year survival rate at 59%. This difference was statistically significant between groups (P < .05). Patients who underwent SPT in the periodontal department during the follow-up period were reported to have significantly higher survival rates. ETT that received SPT showed an 85% survival rate during the 9-year investigation time. This number dropped to 61% for patients who did not participate in SPT during the follow-up time (P < .05) (Fig. 2).
A Cox proportional hazard model was further used to assess the weighted risk of tooth loss based on different periodontal parameters. Table 2 details the effect of different clinical variables on the survival rate of ETT. Teeth that were diagnosed with mild periodontitis were almost 2 times more likely to be extracted compared with ETT diagnosed with a normal periodontium at the time of NSRCT (odds ratio [OR] = 1.9, P < .05). This increased risk of tooth loss was 3.1 (OR = 3.1, P < .05) for ETT diagnosed with moderate periodontitis. Furthermore, patients who failed to return for the follow-up SPT after NSRCT were 2.7 times more likely to lose the tooth compared with individuals who received SPT regardless of the periodontal diagnosis (pooled OR = 2.73, P < .05). However, the stratified OR for patients in the moderate group was 5 (OR = 5.02, P < 05). This means that patients with
Figure 1. A Kaplan-Meier survival curve as a function of different periodontal diagnosis at the time of NSRCT.
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Clinical Research
Figure 2. A Kaplan-Meier survival curve as a function of receiving supportive periodontal treatment after NSRCT.
moderate periodontitis who did not receive SPT were 5 times more likely to lose the tooth compared with individuals who received SPT (Table 2). Our data reveal that smoking status is a significant predictor of tooth loss after endodontic treatment. ETT in active smokers were 2 times more likely to be extracted by the end of the study compared with none/former smokers (OR = 2.2, P < .05).
Discussion For the first time, the present study investigated the effect of periodontal prognostic factors on the survival rate of ETT. Different studies TABLE 2. Multivariate Cox Proportional Hazard Regression Analysis of Tooth Loss (Dependent Variable) according to Patient- and Periodontal-level Factors (Predictor Variables) Predictor Variable Periodontal diagnosis (reference healthy) Mild periodontitis Moderate periodontitis Supportive periodontal therapy (reference no) Pooled effect (regardless of periodontal diagnosis) Healthy group Mild group Moderate group Smoking status (reference never/former) The significance level is P = .05. *P < .05.
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OR (95% CI)
P value
1.9 (0.6–4.3) 3.1 (2.1–7.4)
.04* .006*
2.73 (1.1–5.34)
.038*
1.04 (0.4–3.2) 2.16 (1.4–4.6) 5.02 (2.1–8.4) 2.2 (0.34–6.12)
.379 .012* .025* .01*
have investigated the long-term survival rate of ETT considering various tooth-related and patient-related factors (22–24). However, there is no study that has investigated the effect of the periodontal status of a tooth at the time of NSRCT based on the criteria established by the American Academy of Periodontology (13) while controlling for the confounding variables. In the present study, it was shown that both the periodontal status of a tooth at the time of NSRCT and receiving SPT after NSRCT can significantly affect the survival rate of ETT. Teeth that were diagnosed with mild and moderate periodontitis were more likely to be extracted at the end of the study period compared with ETT with a healthy periodontium. Also, patients’ compliance in receiving supportive periodontal therapy was a significant prognostic factor in the survival rate of ETT. In order to precisely reflect the effect of periodontal diagnostic and therapeutic factors on the survival rate, the effect of preoperative, intraoperative, and postoperative factors were controlled. Only ETT with a preoperative diagnosis of irreversible pulpitis and an acceptable quality of NSRCT were included. Also, to minimize the effect of microleakage and post-NSRCT fracture, only ETT that received a full-coverage crown in a timely manner were included (2). The effect of patient-related factors on the survival rate of ETT was also assessed. None of the patient-related factors such as sex and age affected the outcome of NSRCT, which is consistent with previous studies (24, 25). However, smoking was significantly associated with the survival rate of ETT. According to our data, we report that current smokers are at an increased risk of losing ETT compared with nonsmokers or former smokers. This finding is in agreement with other studies that reported smoking can be a significant prognostic factor for tooth loss in long-term studies (3, 5). JOE — Volume -, Number -, - 2017
Clinical Research For the first time, in the present study, the American Academy of Periodontology (13) diagnostic criteria such as clinical attachment loss and bone loss were used for accurate periodontal diagnosis at the time of NSRCT. Only 1 study investigated the effect of periodontal status on the survival of ETT (12). However, pocket depth was not a valid predictor of periodontal disease severity (13). Also, none of the root canal–related factors or postoperative restoration was considered in that study. We reported that teeth with mild and moderate periodontitis are almost 2 and 3 times more likely to get extracted, respectively. This finding could highlight the importance of periodontal integrity at the time of NSRCT as 1 of the significant prognostic factors. This finding may be a reasonable explanation for studies that consider periodontal disease as 1 of the main reasons for extraction after NSRCT (9, 10). It has been reported that the risk of tooth loss was significantly lower in patients with chronic periodontitis who undergo SPT (6). In this study, we reported that patients who do not receive SPT such as scaling and root planning are 2 times more likely to lose ETT compared with patients who benefit from routine periodontal treatments. Different studies in the field of periodontics have reported that endodontic treatment influences tooth loss (1, 3, 5). However, this statement may falsely affect the oral health care providers’ perception regarding root canal treatment and the effect of endodontic treatment on the long-term retention of teeth. This study further confirms the high predictable survival rate of teeth after NSRCT in cases with a healthy periodontium. We conclude that patients’ periodontal health, being 1 of the prognostic determinants of NSRCT, requires more attention before and subsequent to NSRCT. This may improve the survival of ETT and help patients maintain their natural dentition.
Acknowledgments The authors deny any conflicts of interest related to this study.
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