Accepted Article
Received Date : 20-Dec-2013 Revised Date : 07-Apr-2014 Accepted Date : 21-Apr-2014 Article type : Systematic Review
Treatment of periodontal-endodontic lesions – a systematic review
a
Julia C. Schmidt*, Clemens Walter* , Mauro Amato and Roland Weiger
*both authors contributed equally to this work
Department of Periodontology, Cariology and Endodontology, University of Basel, Switzerland
Running title: treatment of perio-endo lesions
Keywords: periodontitis, pulp necrosis, root canal treatment, periodontal surgery
Conflict of interest and source of funding statement The authors declare that they have no conflicts of interest. No external funding was obtained for this review.
a
Corresponding author:
Clemens Walter Dept. of Periodontology, Endodontology and Cariology University of Basel Hebelstrasse 3, CH-4056 Basel (Switzerland) Tel.: +41 61 2672628 Fax: +41 61 2672659 Email: [email protected]
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Abstract Background: The treatment of periodontal-endodontic lesions is challenging due to the involvement of both periodontal and endodontic tissues.
Objective: To evaluate the treatment options and outcomes of periodontal-endodontic lesions.
Material and methods: A systematic literature search was performed for articles published by 12 May 2013 using electronic databases and hand search. Two reviewers conducted the study selection, data collection and validity assessment. The PRISMA criteria were applied. From 1087 titles identified by the search strategy, five studies and 18 case reports were included.
Results: Clinical studies and case reports were published from the years 1981 to 2012. A pronounced heterogeneity exists among studies regarding applied treatment protocols and quality of reporting. In all clinical studies, comprising 111 teeth, a non-surgical root canal treatment (RCT) was performed as initial treatment step. Non-surgical and/or a surgical periodontal therapy was applied in some studies without reevaluation of the endodontic healing. Probing pocket depth reductions were reported in all included studies, comprising the data from 74 teeth at follow-up.
Conclusions: A sequential treatment with root canal treatment as a first treatment step appears to be reasonable. An adequate time for tissue healing is suggested prior to reevaluation.
Clinical relevance Scientific rationale for the study: Different therapeutic approaches including endodontic and/or periodontal procedures have been proposed for the treatment of periodontal-endodontic lesions.
Principal findings: In this systematic review, a successful outcome in terms of probing pocket depth reduction of exclusive non-surgical endodontic therapy was identified for teeth with a negative response to pulp sensibility testing combined with increased probing pocket depth.
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Practical implications: The findings from this systematic review may support an initial root canal treatment for the treatment of this kind of periodontal-endodontic lesions. A reasonable time in advance of consideration of further procedures is suggested.
Introduction A communication between the periodontium and the dental pulp exists through different pathways including the apical foramina, lateral and accessory canals or exposed dentinal tubules (Seltzer et al. 1963, Rotstein & Simon 2006). These anatomic structures enable the development of diseases with concurrent periodontal and pulpal tissue involvement, e.g. so called periodontal-endodontic lesions.
An endodontic lesion may elicit an inflammatory response in the adjacent periodontal tissue and thus can cause a retrograde periodontitis (Simring & Goldberg 1964). A periodontal lesion may provoke an extensive pulp pathosis (Langeland et al. 1974, Bergenholtz & Lindhe 1978). In addition, periodontal and endodontic diseases can develop independently. Teeth with a periodontal-endodontic lesion feature an inflamed or necrotic pulp tissue and increased probing pocket depths leading to great variabilty of possible diagnostic findings, e.g. altered response to pulp sensibility testing, multiple or singular increased periodontal probing depth, sinus tract, pus, radiological J-shaped lesion or infrabony defect (Harrington 1979, Abbott 1998). The retrospective identification of the primary cause of a periodontal-endodontic lesion, however, is not possible in most cases.
Several classification systems were applied to describe these lesions according to their pathogenesis or with respect to a suggested therapy sequence (Simon et al. 1972, Guldener 1975, Geurtsen et al. 1985, Dietrich et al. 2002). However, the classification is still under an ongoing scientific debate (Abbott & Salgado 2009, Simon et al. 1972). The current classification of periodontal diseases, even controversely
discussed,
postulates
the
category “combined
periodontal-endodontic
lesion”
irrespective of the suspected pathogenesis of the lesion (Armitage 1999, Lang et al. 1999, Eickholz 2013).
The treatment of these lesions is a challenge and treatment planning needs to consider the involvement of the periodontal and pulpal compartment. A wide spectrum of different therapeutic options and/or therapeutic sequences including endodontic and periodontal treatment with non-
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surgical and/or surgical procedures with or without local or systemic antibiotics have been described in case reports and clinical studies.
Review of Current Literature Objective The purposes of the present systematic review were to identify the treatment options and to evaluate the therapy with respect to the outcomes of combined periodontal-endodontic lesions in humans with respect to tooth loss and probing pocket depth (PPD) reduction.
The specific questions addressed in this systematic review were: In patients with combined periodontal-endodontic lesions: a.
Which treatments/treatment sequences were applied?
b.
In case the treatment was performed at different time points, what was the time interval for reevaluation of the first treatment step?
c.
Which rates of tooth loss occurred after treatment?
d.
Does treatment of combined periodontal-endodontic lesions lead to a PPD reduction?
Methods Protocols The present systematic review considers the PRISMA (Preferred Reporting Items for Systematic Review and Meta-analyses) criteria (Liberati et al. 2009, Moher et al. 2009). The research questions were adapted using the PICO (Patient, Intervention, Comparison, Outcomes) criteria (Miller & Forrest 2001).
Eligibility and ineligibility criteria Publications were considered eligible for inclusion in this systematic review if they presented the following parameters: (1) the presence of a combined periodontal-endodontic lesion defined as the coexistence of a negative or altered pulp vitality test and PPD ≥ 6 mm on at least one tooth site in case reports or a mean probing pocket depth ≥ 6 mm in interventional studies and case series and (2) a follow-up after treatment of at least 6 months. No restrictions in terms of type of publication, i.e. case report, clinical study, review, language and or time point of publication were applied. Review articles
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were screened for the presentation of case reports within the review. A publication considered ineligible for inclusion was hierarchically categorized (Appendix 4, 5).
Outcome measures The primary outcome measure was tooth loss after treatment of combined periodontal-endodontic lesions. Changes in PPD, probing attachment level (PAL), gingival recession (REC) and radiographic findings were evaluated as secondary outcome variables.
Information Sources The electronic databases MEDLINE by OVID and EMBASE and the grey literature (www.opengrey.eu) were searched for studies published prior to May 12, 2013. A hand search was performed on Journal of Clinical Periodontology, Journal of Periodontology, Journal of Endodontics and International Endodontic Journal from January 1990 to May 2013. Moreover, the references of publications examined for inclusion were thoroughly analyzed to search for additional publications.
Literature Search The search protocols in the different databases were validated and created as identical as possible (Appendix 2).
Study Selection The combinations of search terms resulted in a list of 1087 titles from the electronic databases (Fig. 1). Two of the authors (M. A. and J. S.) screened the titles and abstracts for compliance with the inclusion criteria and selected 186 publications for full text analysis. A third reviewer (C. W.) reassessed both the included and excluded studies.
Data Collection Process Data items The relevant data of included publications were collected in data extractions files.
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Risk of Bias in Individual Studies The included studies were evaluated by modified items from the Cochrane Collaboration`s Tool for assessing risk of bias (Graziani et al. 2012) (Appendix 3). Considering the adequacy in the respective studies, the items were graded and the percentage of positively graded items was calculated (Graziani et al. 2012).
Summary Measures Most studies reported on mean PPD with standard deviations at baseline and at follow-up, but also individual values or the range of individual values were presented.
Synthesis of Results Owing to the limited number of randomized controlled clinical trials and the significant heterogeneity in reported treatment protocols, a pooling of data or statistical meta-analyses were not appropriate and therefore not performed.
Results Study selection A total of 1087 titles from the electronic databases were identified (Fig. 1). The titles and abstracts were screened by two reviewers (observed agreement = 90.16%, kappa = 0.773). The full texts of 186 publications (selected by at least one reviewer) were further analyzed. Full text analysis led to exclusion of further 171 studies (Appendix 4 and 5). Finally, 15 publications from the electronic search satisfied the inclusion criteria. Eight additional publications were identified by screening the references of studies evaluated for inclusion.
Description of Characteristics, Results, and Quality assessment The analysis for clinical studies and case reports was performed separately. The characteristics of included studies (Table 1) and case reports (Table 2, Appendix 6) and the assessment of risk of bias (Appendix 7) are summarized in tables.
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Summary of Characteristics (PICO – Population, Intervention/Comparison, Outcomes) Population – Number and characteristics of patients and tooth sites The mean age of patients in two of the included publications amounted 44 and 51.2 years (Haueisen et al. 2000, Li et al. 2012). The patients` age in two other publications ranged from 25 to 53 years (Hassan et al. 1986, Sun & Liu 2009) whereas it was not available in one case series (Ratka-Krüger et al. 2000). The proportion of females and males was provided in two publications including each 18 males and 12 females (Sun & Liu 2009, Li et al. 2012). Two studies stated exclusion criteria in terms of the presence of systemic diseases, increased mobility of teeth, tobacco use, pregnancy, and the use of antibiotics during the observation period (Hassan et al. 1986, Li et al. 2012). Three case series did not assign any exclusion criteria (Haueisen et al. 2000, Ratka-Krüger et al. 2000, Sun & Liu 2009).
The included publications investigated each between 10 and 30 teeth. Overall, the treatment of combined periodontal-endodontic lesions was analyzed in 111 teeth. Most publications examined various tooth types including both single- and multi-rooted teeth (Ratka-Krüger et al. 2000, Sun & Liu 2009, Li et al. 2012). A total of 68 molars, 22 bicuspids and 20 incisors were analyzed. Two case series stated the proportion of upper and lower teeth with a large majority of teeth in the mandibula (Haueisen et al. 2000, Ratka-Krüger et al. 2000).
The mean PPD at baseline ranged from 6.01 ± 0.31 mm to 14.29 ± 1.76 mm (Hassan et al. 1986, Li et al. 2012). The individual PPD values ranged from 9 to 17 mm (Hassan et al. 1986, Haueisen et al. 2000). Clinical symptoms in terms of pain, thermal sensitivity, gingival swelling, sinus tracts, pus discharge from gingival margin, increased mobility and sensitivity to percussion were occasionally reported (Haueisen et al. 2000, Ratka-Krüger et al. 2000, Sun & Liu 2009, Li et al. 2012). The appearance of a sinus tract was reported in some patients (Haueisen et al. 2000, Ratka-Krüger et al. 2000). In two case series, all included teeth demonstrated either a caries profunda treatment combined with a filling or a crown restoration (Haueisen et al. 2000, Ratka-Krüger et al. 2000). The presence of a restoration or a carious lesion was not reported in the remaining publications.
The radiographic findings were described as periapical, lateral and/or interradicular radiolucencies (Haueisen et al. 2000, Ratka-Krüger et al. 2000, Li et al. 2012). Moreover, Ratka-Krüger et al. (2000)
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specified the pattern of bone loss on radiographs as local and narrow, extending to the apex and frequently without any approximal bone loss.
In patients with combined periodontal-endodontic lesions: a.
Which treatments/treatment sequences were applied?
Different treatments of combined periodontal-endodontic lesions, including periodontal and endodontic approaches with non-surgical and surgical methods were performed. In all publications, a non-surgical root canal treatment was performed as initial treatment step. A two-staged RCT with a temporary intracanal medication was applied in two case series. After reevaluation no further endodontic or periodontal therapy was deemed to be necessary in these case series (Haueisen et al. 2000, RatkaKrüger et al. 2000). The remaining publications combined an endodontic with a periodontal treatment. Li et al. (2012) selected a non-surgical approach by combining a root canal treatment with the root debridement of involved teeth with (test group) or without (control group) diode laser irradiation. The laser was applied both during RCT and after initial periodontal treatment in a mode aiming in bacterial reduction. Two publications added periodontal surgery to a conventional non-surgical periodontal and endodontic treatment. Hassan et al. (1986) applied citric acid as conditioning agent to the root surfaces within an open flap debridement. Sun & Liu (2009) used a xenogenous bone graft material and adjuvant systemic antibiotics in addition to surgery.
b.
In case the treatment was performed at different time points, what was the time interval for reevaluation of the first treatment step?
In two retrospective case series non-surgical endodontic treatment was performed as a first treatment step and the decision for any further therapy was left open and performed six months after reevaluation of the healing after RCT (Haueisen et al. 2000, Ratka-Krüger et al. 2000). In both case series in all reevaluated patients no further therapy was deemed necessary since the initial RCT was classified as successful according to clinical and radiographic criteria. In the remaining publications, a combined treatment was initially planned using a research plan and applied without further decision making within the healing process.
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c.
Which rates of tooth loss occurred after treatment?
No tooth loss was reported in either publications. The reported drop-out rate was 2 out of 14 (Hassan et al. 1986), 11 out of 20 (Ratka-Krüger et al. 2000) and 18 out of 37 (Sun & Liu 2008). No drop-outs were reported in the remaining two publications. As reasons were not provided, patients who dropped out were assumed to may have lost their treated teeth and considered as “worst case” for the calculation of tooth loss (Spriet & Dupin-Spriet 1993, Myers et al. 2000). Out of the 111 treated teeth for 74 teeth an outcome was reported, leading to the assumption of 37 teeth may have been lost during follow up, representing a tooth loss rate within the range of 0 to 33.3%.
d.
Does treatment of combined periodontal-endodontic lesions lead to a PPD reduction?
PPD reductions in terms of a decreased mean PPD or a smaller PPD range occurred from baseline to follow up in all included publications for the teeth at follow up. Data is reported after 6 months in all included publications. Three case series provided additional data after 12 months (Haueisen et al. 2000, Ratka-Krüger et al. 2000, Sun & Liu 2009).
The PPD after a follow-up of 6 months decreased from a mean PPD of 14.29 ± 1.76 to 6.125 ± 4.076 mm (Hassan et al. 1986). The individual values of the PPD ranged from 3.8 mm to 15.3 mm (Hassan et al. 1986).
In a randomized controlled trial, Li et al. (2012) reported a significantly different PPD reduction after a follow-up of 6 months from a mean PPD of 6.04 ± 0.37 to 5.64 ± 0.33 mm in the control group and from a mean PPD of 6.01 ± 0.31 to 4.34 ± 0.23 mm in the test group.
The PPD decreased from a mean PPD of 11.3 mm to 3.1 mm after 6 months and to 2.2 mm after 12 months (Ratka-Krüger et al. 2000). After a follow-up of 6 months, the reported PPD range of 9 to 12 mm at baseline declined to 2 to 4 mm with no further changes up to 12 months (Haueisen et al. 2000).
A statistically significant reduction of the PPD after 6 months, i.e. from a mean PPD 6.62 ± 0.230 to 2.83 ± 0.149 mm and after 12 months, i.e. from mean PPD of 6.74 ± 0.285 to 2.42 ± 0.233 was noted by Sun & Liu (2009).
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Discussion Herein, we conducted a systematic review to evaluate the best available external evidence regarding the treatment options and outcomes of periodontal-endodontic lesions. A total of five studies, i.e. one randomized controlled clinical trial, two prospective and two retrospective case series, and 18 case reports were included from a systematic literature search. Due to an assumed scarcity of clinical studies, the initial purpose of this systematic review was to evaluate case reports supposed to be the best external evidence on this subject. As interventional studies and case series, however, were also found fulfilling the inclusion criteria (Fig. 1), the data were presented separately for clinical studies (Table 1) and case reports (Table 2, Appendix 6) according to the suspected hierarchy of best available external evidence.
A plethora of classifications for lesions with periodontal and endodontic tissue involvement has been proposed. Several authors suggested the differentiation between the primary cause(s) of the lesion, i.e. of periodontal or endodontic origin (Simon et al. 1972, Guldener 1975, Geurtsen et al. 1985). However, the correct identification of the disease onset is frequently impeded and remains of speculative nature in many cases, due to an incomplete dental history or critical results of a pulp sensibility test, in particular in multi-rooted teeth. According to recent suggestions (Armitage 1999, Lang et al. 1999, Abbott & Salgado 2009), in this systematic review, only publications that described a well defined feature of periodontal-endodontic lesions, i.e. teeth with a negative or an unclear response to a pulp sensibility test and an increased probing pocket depth, were considered (Appendix 4, 5). Interestingly, three studies included neither used a classification system nor determined the disease onset probably reflecting the difficulties and limitations in differential diagnosis (Hassan et al. 1986, Sun & Liu 2009, Li et al. 2012).
The publications in this systematic review were published within a time frame from 1981 to 2012. As one finding from this review, non-surgical RCT as a sole treatment approach was performed by some early publications whereas guided tissue regeneration (GTR) procedures were more frequently applied in recent publications (Stamas & Johnson 1994, Ghezzi et al. 2012). Time-point of publication needs to be considered as a relevant parameter within a review, because dental treatment options and/or materials have changed dramatically over time (Hassan et al. 1986, Li et al. 2012, Rodriguez et al. 2012), probably leading to difficulties in comparison among the studies.
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Although the English language is commonly accepted as the language of scientific research, relevant external evidence could also arise from studies in languages other than English (Morrison et al. 2012), in particular from members of the BRIC countries (Brazil, Russia, India, China) or findings from the early days of scientific periodontology (Schmidt et al. 2013). In addition, it was suggested that positive research findings are more likely to be published in an international English-language journal whereas negative results may be rather reported in a non English-language journal (Egger et al. 2003). The influence of language restrictions on the outcome of systematic reviews is uncertain in particular fields of medicine (Morrison et al. 2012). The exclusion of non English-language studies from a systematic review, however, may led to a language bias. The literature search of the present systematic review was performed without any language restrictions. Two original studies in Chinese language have been translated. They fulfilled the inclusion criteria and were included comprising 67 teeth out of 111 analyzed teeth (Sun & Liu 2009, Li et al. 2012).
Treatment planning includes the consideration of diagnostic and prognostic factors deemed to influence the treatment outcome of periodontal-endodontic lesions (Lang & Tonetti 2003, Kwok & Caton 2007). However, in addition to mode of endodontic and/or periodontal treatment, potential confounding factors, e.g. patient`s age, gender, tooth type, smoking, periodontal history and chronicity of lesions, were inconsistently considered in the included publications resulting in a high risk of bias (Appendix 7). Further research analysing the impact of these factors on the pathogenesis and the outcome of therapy of periodontal endodontic lesions is required. No tooth loss was reported except for two case reports. In case series and case reports, success and/or survival rates may be subject to a publication bias as a treatment success may be more likely to be published. Therefore, treatment failures could be underrepresented. Several drop-outs occurred in three included publications (Hassan et al. 1986, Ratka-Krüger et al. 2000, Sun & Liu 2009). Such drop-out rates pose a threat to validity of any study (Walter et al. 2012a). In general, there are different possibilities to handle drop-outs including the so-called “worst case” analysis. As reasons for drop-outs were not provided, this method was applied in the present review and patients who dropped were assumed to may have lost their treated teeth (Myers 2000, Sutherland 2001, Wang et al. 2004). The tooth loss rate ranged from 0 to 33% resulting in a survival rate of 66.7 to 100 %. The survival rate may be affected by the eligibility criteria, including the PPD range, applied in the randomized controlled clinical trial and in the case series. For example, the exclusion of hypermobile and multi-rooted teeth seems to be of prognostic
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relevance and may have implications on the treatment outcome (Hassan et al. 1986). The herein reported survival rate is within the previously noted range of survival rates. Schacher et al. found a survival rate of 61% after at least five years to retain teeth with treated periodontal-endodontic lesions (Schacher et al. 2007). In addition, a prospective clinical trial reported a favourable outcome of 77.5% in apicomarginal defects including periodontal-endodontic lesions (Kim et al. 2008). In contrast to the reported tooth loss and/or survival rate, the PPD reduction represents an alternative study end point, possibly representing a success rate from a strictly periodontal point of view. A PPD reduction was achieved in nearly all re-evaluated teeth, but there may be remaining deep probing depth (Hassan et al. 1986, Li et al. 2012). However, the PPD of the included teeth differed remarkably between the clinical studies (Hassan et al. 1986, Li et al. 2012). Keeping in mind, that a narrow localized deep PPD may represent a draining sinus tract of endodontic origin that healed after root canal treatment (Weiger et al. 1995, Abbott & Salgado 2009).
The data from clinical studies and case reports were analyzed separately with respect to the suspected hierarchy of external evidence (Hujoel 2008). In general, the evidence levels refer to the study design suggesting randomized controlled clinical trials as higher available external evidence compared to other study designs (Hujoel 2008). For this reason, some authors feel there is a lack of direct evidence in case an (meta analysis of) RCT`s is missing (Walter et al. 2012b, Schmidt et al. 2013, Walter & Friedmann 2013). In randomized controlled clinical trials, patients need to be assigned to a predefined protocol. This design may exclude the opportunity of alteration of a treatment plan, which may be indicated after evaluation of the tissue response after root canal treatment. Healing of lesions of endodontic origin depends on many modifying factors and may occur within a large time frame (European Society of Endodontology 2006, Ricucci et al. 2009, Walter et al. 2008). Prospective case series or cohort studies permit modifications of the treatment plan and sequence with respect to individual healing responses and findings at different time points. A (prospective) case series seem to be more reasonable to evaluate the treatment of periodontal-endodontic lesions at the current stage of knowledge. Four case series and 18 case reports were included in this review. In two case series and five case reports, a non-surgical endodontic treatment was performed as initial treatment and the decision for further procedures were based on the tissue response at reevaluation (Stamas & Johnson 1994, Haueisen et al. 1999, Ratka-Krüger et al. 1999, Haueisen et al. 2000, Ratka-Krüger et al. 2000, Walter et al. 2008). The remaining publications predefined the treatment sequence, i.e. a combined
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treatment consisting of non surgical endodontic therapy with a non-surgical and/or a surgical periodontal therapy. Periodontal surgery consisted of an open flap debridement alone or in combination with regenerative or resective procedures.
Incomplete tissue healing after evaluation of the first treatment step may lead to the decision of further procedures (Dietrich et al. 2003). Healing of periapical lesions may take up to 4 years (European Society of Endodontology 2006) or longer (Ricucci et al. 2009). This process may be modified by several hereditary, environmental and behavioural risk factors, e.g. a smoking habit (Walter et al. 2008, Rodriguez et al. 2012, Walter et al. 2012b). Similarly, the improvement of periodontal conditions subsequent to scaling and root planing may take several months, with the deeper the initial PPD the longer the time for PPD reduction (Badersten et al. 1984). An observation time of at least 6 to 12 months before reevaluation of the first treatment step was suggested by Zehnder (Zehnder 2001). The publications included in this review reported a follow-up time between six and 12 months. However, with respect to the individual range of the time required for periodontal tissue healing and the absence of radiographic changes in early stages of healing, the interpretation of treatment results after six to 12 months seems to be associated with some bias (Hirsch et al. 1989, Jansson et al. 1997, Kim et al. 2008). The results from included studies and case series may need to be regarded as short-term outcomes. Follow-up examinations after an observation period of several years would be desirable although challenging.
With respect to the uncertain treatment outcome of periodontal-endodontic lesions and the successful outcome of less invasive treatment approaches (Stamas & Johnson 1994, Haueisen et al. 1999, Ratka-Krüger et al. 1999, Haueisen et al. 2000, Ratka-Krüger et al. 2000), the concept of a sequential treatment with re-evaluation at different treatment stages may also be supported from an economic point of view. Financial costs and time efforts increase dramatically with more invasive treatment approaches (Walter et al. 2012c). On the other hand patient-centred outcomes, including quality of life, treatment time and costs, are of increasing importance within clinical trials to ensure an appropriate allocation of resources (Brägger 2005, Walter et al. 2012c).
Conclusions and clinical relevance Taken together this review may provide some evidence for root canal treatment as a first treatment
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step for the treatment of combined periodontal-endodontic lesions with increased PPD and a negative response of pulp sensibility testing. A reasonable time for healing of the endodontic lesion after root canal treatment is suggested to consider before further therapy is applied. The summarized findings from this analysis may support this concept from a biological, i.e. individual range for time for wound healing, and from a clinical perspective, i.e. evidence from two retrospective clinical studies and five case reports.
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Miller, S. A. & Forrest, J. L. (2001) Enhancing your practice through evidence-based decision making: PICO, learning how to ask good questions. The Journal of Evidence-Based Dental Practice 1, 136-141. Moher, D., Liberati, A., Tetzlaff, J. & Altman, D. G. (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Medicine 6, e1000097. Morrison, A., Polisena, J., Husereau, D., Moulton, K., Clark, M., Fiander, M., Mierzwinski-Urban, M., Clifford, T., Hutton, B. & Rabb, D. (2012) The effect of English-language restriction on systematic review-based meta-analyses: a systematic review of empirical studies. International Journal of Technology Assessment in Health Care 28, 138-144. Myers, W. R. (2000) Handling missing data in clinical trials: an overview. Drug Information Journal 34, 525-533. Ratka-Krüger, P., Haueisen, H. & Schacher, B. (1999) Der ungewöhnliche parodontale Einzelbefund Differentialdiagnostische Aspekte. Parodontologie 1, 7-18. Ratka-Krüger, P., Haueisen, H., Schacher, B. & Neukranz, E. (2000) Verlust endodontaler Integrität als Ursache für lokalisierte parodontale Läsionen. Deutsche Zahnärztliche Zeitschrift 55, 417420. Ricucci, D., Lin, L. M. & Spangberg, L. S. (2009) Wound healing of apical tissues after root canal therapy: a long-term clinical, radiographic, and histopathologic observation study. Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology, and Endodontics 108, 609-621. Rodriguez, F. R., Taner, B., Weiger, R. & Walter, C. (2013) Is smoking a predictor of apical periodontitis? Clinical Oral Investigations 17, 1947-1955. Rotstein, I. & Simon, J. H. (2006) The endo-perio lesion: a critical appraisal of the disease condition. Endodontic Topics 13, 34-56. Schacher, B., Haueisen, H. & Ratka-Krüger, P. (2007) The chicken or the egg? Periodontalendodontic lesions. PERIO 4, 15-21. Schmidt, J. C., Sahrmann, P., Weiger, R., Schmidlin, P. R. & Walter, C. (2013) Biologic width dimensions--a systematic review. Journal of Clinical Periodontology 40, 493-504. Seltzer, S., Bender, I. B. & Ziontz, M. (1963) The Interrelationship of Pulp and Periodontal Disease. Oral Surgery, Oral Medicine, and Oral Pathology 16, 1474-1490. Simon, J. H., Glick, D. H. & Frank, A. L. (1972) The relationship of endodontic-periodontic lesions. Journal of Periodontology 43, 202-208. Simring, M. & Goldberg, M. (1964) The pulpal pocket approach: retrograde periodontitis. Journal of Periodontology 35, 22–48. Stamas, A. M. & Johnson, A. B. (1994) Periodontic and endodontic lesions. Five classifications dental clinicians need to know. Dental Teamwork 7, 31-32. Sun, J. & Liu, Q. (2009) [Bio-Oss collagen bone grafting in the treatment of endodontic-periodontic lesion]. Nan fang yi ke da xue xue bao = Journal of Southern Medical University 29, 19051906. Sutherland, S. E. (2001) Evidence-based dentistry: Part VI. Critical appraisal of the dental literature: Papers about diagnosis, etiology and prognosis. Journal of Canadian Dental Association 67, 582-585.
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Walter, C. & Friedmann, A. (2013) Evidence supports the impact of smoking cessation protocols in periodontal therapy. Journal of Evidence-Based Dental Practice 13, 142-144. Walter, C., Kaye, E. K. & Dietrich, T. (2012a) Active and passive smoking: assessment issues in periodontal research. Periodontology 2000 58, 84-92. Walter, C., Krastl, G. & Weiger, R. (2008) Step-wise treatment of two periodontal-endodontic lesions in a heavy smoker. International Endodontic Journal 41, 1015-1023. Walter, C., Rodriguez, F. R., Taner, B., Hecker, H. & Weiger, R. (2012b) Association of tobacco use and periapical pathosis - a systematic review. International Endodontic Journal 45,1065-73. Walter, C., Weiger, R., Dietrich, T., Lang, N. P. & Zitzmann, N. U. (2012c) Does three-dimensional imaging offer a financial benefit for treating maxillary molars with furcation involvement? A pilot clinical case series. Clinical Oral Implants Research 23, 351-358. Wang, N., Knight, K., Dao, T. & Friedman, S. (2004) Treatment outcome in endodontics-The Toronto Study. Phases I and II: apical surgery. Journal of Endodontics 30, 751-761. Weiger, R., Manncke, B., Werner, H. & Lost, C. (1995) Microbial flora of sinus tracts and root canals of non-vital teeth. Endodontics & Dental Traumatology 11, 15-19. Zehnder, M. (2001) Endodontic infection caused by localized aggressive periodontitis: a case report and bacteriologic evaluation. Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology, and Endodontics 92, 440-445.
Table 1. Characteristics of included studies.
Study First author design (year of publica tion)
Hassa n et al. (1986)
Haueis en et al. (2000)
Number of teeth and patients, age, gender, exclusion criteria
prospect 14 teeth ive case 14 patients series 25 - 40 yrs exclusion criteria: systemic diseases, teeth excessivel y mobile/re quiring splinting
retrospe ctive case series
10 teeth 51.2 yrs (mean)
Tooth Clinical type (n) manifestations (n)
Radiograp hic manifestat ions (n)
Additi onal diagn osis (n)
Treatment sequence
Follo # w-up
maxilla • mean PD ry and 14.29 ± 1.76 mandib mm (range ular 12.5 - 17 incisors mm) (14) • no vitality (14)
-
-
SRP + Occl + 6 mo – (2 w) – RCT1 (GP, LC) + PS (RBF, D) + root demineraliz ation (citric acid)
Counf ounding factor s consi dered
To PD at followot up h los s (n)
Additional outcomes
Num ber of drop outs (patient s) and reas ons
2
mean attachment gain 8.16 ± 2.9 mm
tooth 2, NFD type, age, systemi c diseas es
6.125 ± 4.076 mm (mean ± SD) in 10 patients: 3.2 - 5.2 mm (range)
in 10 patients: attachment gain 7.9 - 9.9 mm
in 2 patients: in 2 patients: 14.2 mm attachment 15.3 mm gain 2.8 mm (range) 1.7 mm radiographic signs of partially bone fill, continuity of lamina dura mandib • narrow PD 9 ular - 12 mm (10) molars (10) • pain (1) • pus discharge from gingival margin (3) • FI (7) • mobility
periradicul fistula ar (mesial (4) and/or distal) and interradic ular radiolucen cy (10)
RCT1 – (CD, 3 w) – RCT2 (GP, S, LC)
+6 mo
0
2 - 4 mm (range)
0 + 12
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2 - 4 mm
no inflammation, no FI, no increased mobility, no sensitivity to percussion, radiographic signs of complete bone
0
0
tooth type, age
Accepted Article RatkaKrüger et al. (2000)
Sun & Liu (2009)
mo
grade I (2), grade II (2) • no vitality (7), unclear response to pulp test (3) • sensitivity to percussion (2) • Cp treatment and filling (2), crown or partial crown (8)
retrospe ctive case series
20 teeth
prospect 37 teeth ive case 30 patients series 28 - 53 yrs 18 male, 12 female
repair (2) or advanced bone repair (8) radiographic signs of complete bone repair (except two second molars with horizontal bone loss of 1 - 2 mm)
• mean PD 11.3 mm
fistula local narrow bone loss to apex, • swelling interradic and/or pus ular discharge from gingival and/or periapical margin radiolucen • FI (18) • no vitality or cy without interappro unclear response to ximal pulp test (20) bone loss • sensitivity to in molars, periapical percussion radiolucen sometimes cy (> 0.5 unclear • Cp treatment of root length) and filling (9), crown or with partial crown widened periodont (11) al ligament space bicuspi teeth with 6 mo bone loss ds (13), follow-up (n = molars 29) (24) • mean PD 6.62 ± 0.230 mm • mean CAL 8.76 ± 0.209 mm • mean mobility 1.66 ± 0. 134 mandib ular molars (15), maxilla ry molars (4), other tooth (1)
(range)
RCT1 – (CD, within 2 mo) – RCT2 (GP, S, LC)
+6 mo
5
3.1 mm (mean)
11 2.2 mm (mean)
+ 12 mo
no FI in 10 of 15 molars, radiographic signs of improvement up to complete regeneration in most teeth
RCT1 – (1 w) – Occl + SRP – (4 w) – PS (MWF, a BG , D, AB amox/metr o)
+6 mo
3
2.83 ± 0.149 mm*
18 2.42 ± 0.233 mm*
+ 12 mo
mean CAL 6.79 3, NFD ± 0.182 mm* mean mobility 18, 1.38 ± 0.092* NFD mean CAL 6.58 ± 0.268 mm* mean mobility 1.26 ± 0.104*
• pain • swelling • no vitality (37) Control: • mean PD 6.04 ± 0.37 mm • mean CAL 1.60 ± 0.19 mm • mean mBI 1.86
18 male, 12 female
Control : anterior teeth (2), bicuspi ds (5), molars (8)
exclusion criteria: systemic diseases, smoking, pregnanc y,
Test: Test: anterior • mean PD teeth 6.01 ± 0.31 (4), mm bicuspi • mean CAL ds (4), 1.57 ± 0.20 molars
periapical, lateral and/or interradic ular radiolucen cy
0 Control: • mean CAL 1.15 ± 0.21 mm • mean mBI 0.80
Control: • mean PAI 3.27
Test: • mean 0 CAL 1.06 ± 0.19 mm • mean mBI 0.67
Test: • mean PAI
11, NFD
no FI in 6 of 9 molars, radiographic signs of improvement up to complete regeneration in most teeth
teeth with 12 mo follow-up (n = 19) • mean PD 6.74 ± 0.285 mm • mean CAL 8.79 ± 0.282 mm • mean mobility 1.68 ± 0.172
Li et al. prospect 30 teeth 30 (2012) ive randomi patients zed controlle 44 yrs (mean) d trial
tooth 5, NFD type
to ot h typ e, ag e, sm oki ng , sy ste mi c dis ea
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Control: • 5.43 ± 0.26 mm (mean ± SD)
Test: • 4.77 ± 0.31 mm** (mean ± SD)
Control:
•
tooth type, age, experie nce of therapi st
Accepted Article
antibiotic (7) intake during observatio n period
mm • mean mBI 1.93
3.20
Control: • mean CAL 1.01 ± 0.14 mm • mean mBI 0.60 • mean PAI 3.00
• increased mobility • no vitality (30)
Test: • mean CAL 0.67 ± 0.12 mm** • mean mBI 0.13** • mean PAI 2.47
se • 5.64 ± s, 0.33 mm ex (mean ± pe SD) rie nc e of Test: th • 4.34 ± er 0.23 api mm** st (mean ± SD)
a , xenograft; b, AH26; c, Cortisomol; d, 1,5 W, continuous wave, one application (15 s); e, 1 W, continuous wave, one application daily (15 s) for 5 days; AB, systemic antiobiotics; amox, amoxicillin; BG, bone graft; CAL, clinical attachment loss; CD, calcium hydroxide dressing; Cp, caries profunda; D, periodontal dressing; FI, furcation involvement; GP, gutta percha; LC, lateral condensation; M, membrane; mBI, modified bleeding index; metro, metronidazole; mo, months; MWF, modified Widman flap; NFD, not further described; Occl, occlusal adjustment; PAI, periapical index; PD, probing depth; PS, periodontal surgery; RCT, root canal treatment; RBF, reverse bevel flap; RF, rotary files; S, sealer; SRP, scaling and root planing; w, weeks; yrs, years; #, time related to last treatment step; *, p < 0.05 (difference between baseline and outcome); **, p < 0.05 (difference between control and test group); the wording used in the table was adapted from the publications included.
Table 2. Characteristics of included case reports. First author (year of publication)
Moucachen et al. (1981) Geurtsen et al. (1985) Stamas & Johnson (1994) Haueisen et al. (1999) Haueisen et al. (1999) Ratka-Krüger et al. (1999)
Radiogra phic manifesta tions
Additi Treatment sequence onal diagn osis
Follo PD Additional w-up (mm) outcomes # (mo) at ## follow -up
NV, Per
A, L
-
Extraction
-
-
-
13
NV, R
A, L, IR, wPLS
-
Extraction
-
-
-
M 64 NR NR 26
7
NV, Pu, M0, R
A, L, IR
-
RCT1 + RCT2
12
2-3
BF
M 59 NR NR 36
12
UV, Pu, Per, R
A, L
-
RCT1 + RCT2
18
2
BF
M 56 NR NR 46
12
UV, Pu, Per, R
A, L, IR
-
RCT1 + RCT2
12
2-3
BF
RCT1 + RCT2
6
3
BF
Ge A Peri Sm Too n- ge o# th ode king type r
PD Clinical (mm) manifestations at basel ine##
M 50 NR NR 38
12
F
17 NR NR 46
M 56 NR NR 47
12
NV, Pu, S, R, FI
A, L, IR
Ab, Fis
Wood et al. (2003) M 62 NR NR 46
11
NV, Pa, Per, C, R, FI
A, L, IR
-
RCT1 + RCT2 + SRP
6
4
no FI
Zubery & Machtei F (1993)
23 AgP NR 22
10
NV, Pa, S, M2
A, L
Fis
RCT1 + SRP - (3 mo) - SRP
21
2
BF, M0-1
Zucchelli (2007)
39 P
12
A, L
Fis
36
3
BF, M0
5
BF, M1, AttG 3 mm
F
NR 12
Zehnder et al. (2001)
M 28 AgP NR 15
8
Kresic (1994)
M 70 NR NR 43
11
Zubery & Machtei F 23 AgP NR 11 (1993) Walter et al. M 53 ChP HS 32 (2008) Danesh-Meyer M 40 NR NR 36 (1999) Haueisen & F 62 NR NR 46 Heidemann (2002) John et al. (2004)
F
58 NR NR 21
10 8i
UV, M3, Rec, infraBDh NV, Pu, Pa, Per, M3 NV, R NV, Pa, S, M2, bBLh NV, R, Feh, h infraBD
12 14
NV, Pu, R, FI , h infraBD NV, Pu, Pa, Per, h S, M2, R, FI
Ghezzi et al. (2012)
M 38 NR NR 21
9
Oh et al. (2009)
F
9
Politis et al. (1986) F
19 NR NR 12
A, L
-
A, L
Fis
A, L
-
L
-
10
NV, S, bBL , h infraBD h NV, Pu, infraBD , bBLh NV, M2, R, Rec, FIh, infraBD h NV, M2
6.5
RCT1 + SRP - (6 mo) - PS
22
RCT1 + SRP - (3 mo) - SRP - (9 mo) 12 – PS + ES RCT1 + RCT2 - (14 mo) - PS (BG a, 32 b f M , AB ) c
d
4
BF, nPLS
2
BF, M0-1
4
BF
2
BF, AttG 8 mm
f
RCT1 + PS (BG , M , AB ) + RCT2 (4 mo) - RCT3
6
-
RCT1 + PS (Res) + Spl
12
1
BF, M1
-
RCT1 + Spl + PS (EMD, BGa, ABf)
9
4
BF, M1
A, L, AccR
Fis
RCT1 + RCT2 + PS (Res, BG , AB ) 12
3-4
BF
L
-
RCT1 + SRP + PS (BGa,e, Mb, ABf)
24
3
BF
A, L
-
RCT1 + SRP + PS (BGe, Md, ABk) (12 mo) - PS (BGi, Mb, ABk)
10
3
BF, no BOP
A
-
RCT1 + PS (BGc) + ES
12
2
BF, M0
A, L, IR
NV, M2, infraBDh L h
7
16
Fis
h
12
Yavuz et al. (2008) M 25 NR NR 22
50 NR NS
L
RCT1 + SRP + Spl - (4 mo) - PS (EMD, BGa, ABf) RCT1 + SRP + RCT2 + RCT3 - (4 mo) - PS
e
a
g
, xenograft; b, bioabsorbable; c, alloplast; d, nonresorbable; e, autograft; f, systemic application; g, local application; h, intraoperative finding; i, data from patients record; j, allograft; k, local and systemic application; A, apical radiolucency; Ab, abscess; AB, antibiotics; AccR, accessory root; AgP, aggressive periodontitis; AttG, attachment gain; bBL, buccal bone loss; BF, radiographic signs of bone fill; BG, bone graft; BOP, bleeding on probing;
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C, caries; ChP, chronic periodontitis; EMD, enamel matrix derivates; ES, endodontic surgery; F, female; Fe, fenestration; Fis, fistula; FI, furcation involvement; HS, heavy smoker; infraBD, infrabony defect; IR, interradicular radiolucency; L, lateral radiolucency; M, male; Me, membrane; M, mobility (grade 0-3); nPLS, normal periodontal ligament space; NR, not reported; NS, non-smoker; NV, negative vitality test response; P, periodontitis (not further specified); Pa, pain; Per, positive percussion test; PS, periodontal surgery; Pu, pus; R, restoration; RCT, root canal treatment; Rec, recession; Res, root resection; S, swelling; Spl, splint; SRP, scaling and root planing; UV, unclear or delayed vitality test response; wPLS, widened periodontal ligament space; #, general periodontal conditions; ##, highest reported PD; ###, time related to last treatment step; +, time between various treatment steps < 3 months; for more details see Appendix 6.
Figure legend
Fig. 1.
Selection process of the studies included (Moher et al. 2009).
Appendix 1
PRISMA 2009 Checklist.
Appendix 2
Electronic search strategy for the databases MEDLINE and EMBASE.
Appendix 3
Scores for assessment of methodological and reporting quality.
Appendix 4
Studies and case series excluded based on full text analysis, and reason for exclusion.
Appendix 5
Case reports and reviews based on full text analysis, and reason for exclusion.
Appendix 6
Characteristics of included case reports in detail.
Appendix 7
Quality assessment of included studies.
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Selection process of the studies included (Moher et al. 2009).
Accepted Article
Fig. 1.
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Received Date : 20-Dec-2013 Revised Date : 07-Apr-2014 Accepted Date : 21-Apr-2014 Article type : Systematic Review
Treatment of periodontal-endodontic lesions – a systematic review
a
Julia C. Schmidt*, Clemens Walter* , Mauro Amato and Roland Weiger
*both authors contributed equally to this work
Department of Periodontology, Cariology and Endodontology, University of Basel, Switzerland
Running title: treatment of perio-endo lesions
Keywords: periodontitis, pulp necrosis, root canal treatment, periodontal surgery
Conflict of interest and source of funding statement The authors declare that they have no conflicts of interest. No external funding was obtained for this review.
a
Corresponding author:
Clemens Walter Dept. of Periodontology, Endodontology and Cariology University of Basel Hebelstrasse 3, CH-4056 Basel (Switzerland) Tel.: +41 61 2672628 Fax: +41 61 2672659 Email: [email protected]
This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. Please cite this article as doi: 10.1111/jcpe.12265 This article is protected by copyright. All rights reserved.
Accepted Article
Abstract Background: The treatment of periodontal-endodontic lesions is challenging due to the involvement of both periodontal and endodontic tissues.
Objective: To evaluate the treatment options and outcomes of periodontal-endodontic lesions.
Material and methods: A systematic literature search was performed for articles published by 12 May 2013 using electronic databases and hand search. Two reviewers conducted the study selection, data collection and validity assessment. The PRISMA criteria were applied. From 1087 titles identified by the search strategy, five studies and 18 case reports were included.
Results: Clinical studies and case reports were published from the years 1981 to 2012. A pronounced heterogeneity exists among studies regarding applied treatment protocols and quality of reporting. In all clinical studies, comprising 111 teeth, a non-surgical root canal treatment (RCT) was performed as initial treatment step. Non-surgical and/or a surgical periodontal therapy was applied in some studies without reevaluation of the endodontic healing. Probing pocket depth reductions were reported in all included studies, comprising the data from 74 teeth at follow-up.
Conclusions: A sequential treatment with root canal treatment as a first treatment step appears to be reasonable. An adequate time for tissue healing is suggested prior to reevaluation.
Clinical relevance Scientific rationale for the study: Different therapeutic approaches including endodontic and/or periodontal procedures have been proposed for the treatment of periodontal-endodontic lesions.
Principal findings: In this systematic review, a successful outcome in terms of probing pocket depth reduction of exclusive non-surgical endodontic therapy was identified for teeth with a negative response to pulp sensibility testing combined with increased probing pocket depth.
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Practical implications: The findings from this systematic review may support an initial root canal treatment for the treatment of this kind of periodontal-endodontic lesions. A reasonable time in advance of consideration of further procedures is suggested.
Introduction A communication between the periodontium and the dental pulp exists through different pathways including the apical foramina, lateral and accessory canals or exposed dentinal tubules (Seltzer et al. 1963, Rotstein & Simon 2006). These anatomic structures enable the development of diseases with concurrent periodontal and pulpal tissue involvement, e.g. so called periodontal-endodontic lesions.
An endodontic lesion may elicit an inflammatory response in the adjacent periodontal tissue and thus can cause a retrograde periodontitis (Simring & Goldberg 1964). A periodontal lesion may provoke an extensive pulp pathosis (Langeland et al. 1974, Bergenholtz & Lindhe 1978). In addition, periodontal and endodontic diseases can develop independently. Teeth with a periodontal-endodontic lesion feature an inflamed or necrotic pulp tissue and increased probing pocket depths leading to great variabilty of possible diagnostic findings, e.g. altered response to pulp sensibility testing, multiple or singular increased periodontal probing depth, sinus tract, pus, radiological J-shaped lesion or infrabony defect (Harrington 1979, Abbott 1998). The retrospective identification of the primary cause of a periodontal-endodontic lesion, however, is not possible in most cases.
Several classification systems were applied to describe these lesions according to their pathogenesis or with respect to a suggested therapy sequence (Simon et al. 1972, Guldener 1975, Geurtsen et al. 1985, Dietrich et al. 2002). However, the classification is still under an ongoing scientific debate (Abbott & Salgado 2009, Simon et al. 1972). The current classification of periodontal diseases, even controversely
discussed,
postulates
the
category “combined
periodontal-endodontic
lesion”
irrespective of the suspected pathogenesis of the lesion (Armitage 1999, Lang et al. 1999, Eickholz 2013).
The treatment of these lesions is a challenge and treatment planning needs to consider the involvement of the periodontal and pulpal compartment. A wide spectrum of different therapeutic options and/or therapeutic sequences including endodontic and periodontal treatment with non-
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Accepted Article
surgical and/or surgical procedures with or without local or systemic antibiotics have been described in case reports and clinical studies.
Review of Current Literature Objective The purposes of the present systematic review were to identify the treatment options and to evaluate the therapy with respect to the outcomes of combined periodontal-endodontic lesions in humans with respect to tooth loss and probing pocket depth (PPD) reduction.
The specific questions addressed in this systematic review were: In patients with combined periodontal-endodontic lesions: a.
Which treatments/treatment sequences were applied?
b.
In case the treatment was performed at different time points, what was the time interval for reevaluation of the first treatment step?
c.
Which rates of tooth loss occurred after treatment?
d.
Does treatment of combined periodontal-endodontic lesions lead to a PPD reduction?
Methods Protocols The present systematic review considers the PRISMA (Preferred Reporting Items for Systematic Review and Meta-analyses) criteria (Liberati et al. 2009, Moher et al. 2009). The research questions were adapted using the PICO (Patient, Intervention, Comparison, Outcomes) criteria (Miller & Forrest 2001).
Eligibility and ineligibility criteria Publications were considered eligible for inclusion in this systematic review if they presented the following parameters: (1) the presence of a combined periodontal-endodontic lesion defined as the coexistence of a negative or altered pulp vitality test and PPD ≥ 6 mm on at least one tooth site in case reports or a mean probing pocket depth ≥ 6 mm in interventional studies and case series and (2) a follow-up after treatment of at least 6 months. No restrictions in terms of type of publication, i.e. case report, clinical study, review, language and or time point of publication were applied. Review articles
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were screened for the presentation of case reports within the review. A publication considered ineligible for inclusion was hierarchically categorized (Appendix 4, 5).
Outcome measures The primary outcome measure was tooth loss after treatment of combined periodontal-endodontic lesions. Changes in PPD, probing attachment level (PAL), gingival recession (REC) and radiographic findings were evaluated as secondary outcome variables.
Information Sources The electronic databases MEDLINE by OVID and EMBASE and the grey literature (www.opengrey.eu) were searched for studies published prior to May 12, 2013. A hand search was performed on Journal of Clinical Periodontology, Journal of Periodontology, Journal of Endodontics and International Endodontic Journal from January 1990 to May 2013. Moreover, the references of publications examined for inclusion were thoroughly analyzed to search for additional publications.
Literature Search The search protocols in the different databases were validated and created as identical as possible (Appendix 2).
Study Selection The combinations of search terms resulted in a list of 1087 titles from the electronic databases (Fig. 1). Two of the authors (M. A. and J. S.) screened the titles and abstracts for compliance with the inclusion criteria and selected 186 publications for full text analysis. A third reviewer (C. W.) reassessed both the included and excluded studies.
Data Collection Process Data items The relevant data of included publications were collected in data extractions files.
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Accepted Article
Risk of Bias in Individual Studies The included studies were evaluated by modified items from the Cochrane Collaboration`s Tool for assessing risk of bias (Graziani et al. 2012) (Appendix 3). Considering the adequacy in the respective studies, the items were graded and the percentage of positively graded items was calculated (Graziani et al. 2012).
Summary Measures Most studies reported on mean PPD with standard deviations at baseline and at follow-up, but also individual values or the range of individual values were presented.
Synthesis of Results Owing to the limited number of randomized controlled clinical trials and the significant heterogeneity in reported treatment protocols, a pooling of data or statistical meta-analyses were not appropriate and therefore not performed.
Results Study selection A total of 1087 titles from the electronic databases were identified (Fig. 1). The titles and abstracts were screened by two reviewers (observed agreement = 90.16%, kappa = 0.773). The full texts of 186 publications (selected by at least one reviewer) were further analyzed. Full text analysis led to exclusion of further 171 studies (Appendix 4 and 5). Finally, 15 publications from the electronic search satisfied the inclusion criteria. Eight additional publications were identified by screening the references of studies evaluated for inclusion.
Description of Characteristics, Results, and Quality assessment The analysis for clinical studies and case reports was performed separately. The characteristics of included studies (Table 1) and case reports (Table 2, Appendix 6) and the assessment of risk of bias (Appendix 7) are summarized in tables.
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Summary of Characteristics (PICO – Population, Intervention/Comparison, Outcomes) Population – Number and characteristics of patients and tooth sites The mean age of patients in two of the included publications amounted 44 and 51.2 years (Haueisen et al. 2000, Li et al. 2012). The patients` age in two other publications ranged from 25 to 53 years (Hassan et al. 1986, Sun & Liu 2009) whereas it was not available in one case series (Ratka-Krüger et al. 2000). The proportion of females and males was provided in two publications including each 18 males and 12 females (Sun & Liu 2009, Li et al. 2012). Two studies stated exclusion criteria in terms of the presence of systemic diseases, increased mobility of teeth, tobacco use, pregnancy, and the use of antibiotics during the observation period (Hassan et al. 1986, Li et al. 2012). Three case series did not assign any exclusion criteria (Haueisen et al. 2000, Ratka-Krüger et al. 2000, Sun & Liu 2009).
The included publications investigated each between 10 and 30 teeth. Overall, the treatment of combined periodontal-endodontic lesions was analyzed in 111 teeth. Most publications examined various tooth types including both single- and multi-rooted teeth (Ratka-Krüger et al. 2000, Sun & Liu 2009, Li et al. 2012). A total of 68 molars, 22 bicuspids and 20 incisors were analyzed. Two case series stated the proportion of upper and lower teeth with a large majority of teeth in the mandibula (Haueisen et al. 2000, Ratka-Krüger et al. 2000).
The mean PPD at baseline ranged from 6.01 ± 0.31 mm to 14.29 ± 1.76 mm (Hassan et al. 1986, Li et al. 2012). The individual PPD values ranged from 9 to 17 mm (Hassan et al. 1986, Haueisen et al. 2000). Clinical symptoms in terms of pain, thermal sensitivity, gingival swelling, sinus tracts, pus discharge from gingival margin, increased mobility and sensitivity to percussion were occasionally reported (Haueisen et al. 2000, Ratka-Krüger et al. 2000, Sun & Liu 2009, Li et al. 2012). The appearance of a sinus tract was reported in some patients (Haueisen et al. 2000, Ratka-Krüger et al. 2000). In two case series, all included teeth demonstrated either a caries profunda treatment combined with a filling or a crown restoration (Haueisen et al. 2000, Ratka-Krüger et al. 2000). The presence of a restoration or a carious lesion was not reported in the remaining publications.
The radiographic findings were described as periapical, lateral and/or interradicular radiolucencies (Haueisen et al. 2000, Ratka-Krüger et al. 2000, Li et al. 2012). Moreover, Ratka-Krüger et al. (2000)
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specified the pattern of bone loss on radiographs as local and narrow, extending to the apex and frequently without any approximal bone loss.
In patients with combined periodontal-endodontic lesions: a.
Which treatments/treatment sequences were applied?
Different treatments of combined periodontal-endodontic lesions, including periodontal and endodontic approaches with non-surgical and surgical methods were performed. In all publications, a non-surgical root canal treatment was performed as initial treatment step. A two-staged RCT with a temporary intracanal medication was applied in two case series. After reevaluation no further endodontic or periodontal therapy was deemed to be necessary in these case series (Haueisen et al. 2000, RatkaKrüger et al. 2000). The remaining publications combined an endodontic with a periodontal treatment. Li et al. (2012) selected a non-surgical approach by combining a root canal treatment with the root debridement of involved teeth with (test group) or without (control group) diode laser irradiation. The laser was applied both during RCT and after initial periodontal treatment in a mode aiming in bacterial reduction. Two publications added periodontal surgery to a conventional non-surgical periodontal and endodontic treatment. Hassan et al. (1986) applied citric acid as conditioning agent to the root surfaces within an open flap debridement. Sun & Liu (2009) used a xenogenous bone graft material and adjuvant systemic antibiotics in addition to surgery.
b.
In case the treatment was performed at different time points, what was the time interval for reevaluation of the first treatment step?
In two retrospective case series non-surgical endodontic treatment was performed as a first treatment step and the decision for any further therapy was left open and performed six months after reevaluation of the healing after RCT (Haueisen et al. 2000, Ratka-Krüger et al. 2000). In both case series in all reevaluated patients no further therapy was deemed necessary since the initial RCT was classified as successful according to clinical and radiographic criteria. In the remaining publications, a combined treatment was initially planned using a research plan and applied without further decision making within the healing process.
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c.
Which rates of tooth loss occurred after treatment?
No tooth loss was reported in either publications. The reported drop-out rate was 2 out of 14 (Hassan et al. 1986), 11 out of 20 (Ratka-Krüger et al. 2000) and 18 out of 37 (Sun & Liu 2008). No drop-outs were reported in the remaining two publications. As reasons were not provided, patients who dropped out were assumed to may have lost their treated teeth and considered as “worst case” for the calculation of tooth loss (Spriet & Dupin-Spriet 1993, Myers et al. 2000). Out of the 111 treated teeth for 74 teeth an outcome was reported, leading to the assumption of 37 teeth may have been lost during follow up, representing a tooth loss rate within the range of 0 to 33.3%.
d.
Does treatment of combined periodontal-endodontic lesions lead to a PPD reduction?
PPD reductions in terms of a decreased mean PPD or a smaller PPD range occurred from baseline to follow up in all included publications for the teeth at follow up. Data is reported after 6 months in all included publications. Three case series provided additional data after 12 months (Haueisen et al. 2000, Ratka-Krüger et al. 2000, Sun & Liu 2009).
The PPD after a follow-up of 6 months decreased from a mean PPD of 14.29 ± 1.76 to 6.125 ± 4.076 mm (Hassan et al. 1986). The individual values of the PPD ranged from 3.8 mm to 15.3 mm (Hassan et al. 1986).
In a randomized controlled trial, Li et al. (2012) reported a significantly different PPD reduction after a follow-up of 6 months from a mean PPD of 6.04 ± 0.37 to 5.64 ± 0.33 mm in the control group and from a mean PPD of 6.01 ± 0.31 to 4.34 ± 0.23 mm in the test group.
The PPD decreased from a mean PPD of 11.3 mm to 3.1 mm after 6 months and to 2.2 mm after 12 months (Ratka-Krüger et al. 2000). After a follow-up of 6 months, the reported PPD range of 9 to 12 mm at baseline declined to 2 to 4 mm with no further changes up to 12 months (Haueisen et al. 2000).
A statistically significant reduction of the PPD after 6 months, i.e. from a mean PPD 6.62 ± 0.230 to 2.83 ± 0.149 mm and after 12 months, i.e. from mean PPD of 6.74 ± 0.285 to 2.42 ± 0.233 was noted by Sun & Liu (2009).
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Discussion Herein, we conducted a systematic review to evaluate the best available external evidence regarding the treatment options and outcomes of periodontal-endodontic lesions. A total of five studies, i.e. one randomized controlled clinical trial, two prospective and two retrospective case series, and 18 case reports were included from a systematic literature search. Due to an assumed scarcity of clinical studies, the initial purpose of this systematic review was to evaluate case reports supposed to be the best external evidence on this subject. As interventional studies and case series, however, were also found fulfilling the inclusion criteria (Fig. 1), the data were presented separately for clinical studies (Table 1) and case reports (Table 2, Appendix 6) according to the suspected hierarchy of best available external evidence.
A plethora of classifications for lesions with periodontal and endodontic tissue involvement has been proposed. Several authors suggested the differentiation between the primary cause(s) of the lesion, i.e. of periodontal or endodontic origin (Simon et al. 1972, Guldener 1975, Geurtsen et al. 1985). However, the correct identification of the disease onset is frequently impeded and remains of speculative nature in many cases, due to an incomplete dental history or critical results of a pulp sensibility test, in particular in multi-rooted teeth. According to recent suggestions (Armitage 1999, Lang et al. 1999, Abbott & Salgado 2009), in this systematic review, only publications that described a well defined feature of periodontal-endodontic lesions, i.e. teeth with a negative or an unclear response to a pulp sensibility test and an increased probing pocket depth, were considered (Appendix 4, 5). Interestingly, three studies included neither used a classification system nor determined the disease onset probably reflecting the difficulties and limitations in differential diagnosis (Hassan et al. 1986, Sun & Liu 2009, Li et al. 2012).
The publications in this systematic review were published within a time frame from 1981 to 2012. As one finding from this review, non-surgical RCT as a sole treatment approach was performed by some early publications whereas guided tissue regeneration (GTR) procedures were more frequently applied in recent publications (Stamas & Johnson 1994, Ghezzi et al. 2012). Time-point of publication needs to be considered as a relevant parameter within a review, because dental treatment options and/or materials have changed dramatically over time (Hassan et al. 1986, Li et al. 2012, Rodriguez et al. 2012), probably leading to difficulties in comparison among the studies.
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Although the English language is commonly accepted as the language of scientific research, relevant external evidence could also arise from studies in languages other than English (Morrison et al. 2012), in particular from members of the BRIC countries (Brazil, Russia, India, China) or findings from the early days of scientific periodontology (Schmidt et al. 2013). In addition, it was suggested that positive research findings are more likely to be published in an international English-language journal whereas negative results may be rather reported in a non English-language journal (Egger et al. 2003). The influence of language restrictions on the outcome of systematic reviews is uncertain in particular fields of medicine (Morrison et al. 2012). The exclusion of non English-language studies from a systematic review, however, may led to a language bias. The literature search of the present systematic review was performed without any language restrictions. Two original studies in Chinese language have been translated. They fulfilled the inclusion criteria and were included comprising 67 teeth out of 111 analyzed teeth (Sun & Liu 2009, Li et al. 2012).
Treatment planning includes the consideration of diagnostic and prognostic factors deemed to influence the treatment outcome of periodontal-endodontic lesions (Lang & Tonetti 2003, Kwok & Caton 2007). However, in addition to mode of endodontic and/or periodontal treatment, potential confounding factors, e.g. patient`s age, gender, tooth type, smoking, periodontal history and chronicity of lesions, were inconsistently considered in the included publications resulting in a high risk of bias (Appendix 7). Further research analysing the impact of these factors on the pathogenesis and the outcome of therapy of periodontal endodontic lesions is required. No tooth loss was reported except for two case reports. In case series and case reports, success and/or survival rates may be subject to a publication bias as a treatment success may be more likely to be published. Therefore, treatment failures could be underrepresented. Several drop-outs occurred in three included publications (Hassan et al. 1986, Ratka-Krüger et al. 2000, Sun & Liu 2009). Such drop-out rates pose a threat to validity of any study (Walter et al. 2012a). In general, there are different possibilities to handle drop-outs including the so-called “worst case” analysis. As reasons for drop-outs were not provided, this method was applied in the present review and patients who dropped were assumed to may have lost their treated teeth (Myers 2000, Sutherland 2001, Wang et al. 2004). The tooth loss rate ranged from 0 to 33% resulting in a survival rate of 66.7 to 100 %. The survival rate may be affected by the eligibility criteria, including the PPD range, applied in the randomized controlled clinical trial and in the case series. For example, the exclusion of hypermobile and multi-rooted teeth seems to be of prognostic
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relevance and may have implications on the treatment outcome (Hassan et al. 1986). The herein reported survival rate is within the previously noted range of survival rates. Schacher et al. found a survival rate of 61% after at least five years to retain teeth with treated periodontal-endodontic lesions (Schacher et al. 2007). In addition, a prospective clinical trial reported a favourable outcome of 77.5% in apicomarginal defects including periodontal-endodontic lesions (Kim et al. 2008). In contrast to the reported tooth loss and/or survival rate, the PPD reduction represents an alternative study end point, possibly representing a success rate from a strictly periodontal point of view. A PPD reduction was achieved in nearly all re-evaluated teeth, but there may be remaining deep probing depth (Hassan et al. 1986, Li et al. 2012). However, the PPD of the included teeth differed remarkably between the clinical studies (Hassan et al. 1986, Li et al. 2012). Keeping in mind, that a narrow localized deep PPD may represent a draining sinus tract of endodontic origin that healed after root canal treatment (Weiger et al. 1995, Abbott & Salgado 2009).
The data from clinical studies and case reports were analyzed separately with respect to the suspected hierarchy of external evidence (Hujoel 2008). In general, the evidence levels refer to the study design suggesting randomized controlled clinical trials as higher available external evidence compared to other study designs (Hujoel 2008). For this reason, some authors feel there is a lack of direct evidence in case an (meta analysis of) RCT`s is missing (Walter et al. 2012b, Schmidt et al. 2013, Walter & Friedmann 2013). In randomized controlled clinical trials, patients need to be assigned to a predefined protocol. This design may exclude the opportunity of alteration of a treatment plan, which may be indicated after evaluation of the tissue response after root canal treatment. Healing of lesions of endodontic origin depends on many modifying factors and may occur within a large time frame (European Society of Endodontology 2006, Ricucci et al. 2009, Walter et al. 2008). Prospective case series or cohort studies permit modifications of the treatment plan and sequence with respect to individual healing responses and findings at different time points. A (prospective) case series seem to be more reasonable to evaluate the treatment of periodontal-endodontic lesions at the current stage of knowledge. Four case series and 18 case reports were included in this review. In two case series and five case reports, a non-surgical endodontic treatment was performed as initial treatment and the decision for further procedures were based on the tissue response at reevaluation (Stamas & Johnson 1994, Haueisen et al. 1999, Ratka-Krüger et al. 1999, Haueisen et al. 2000, Ratka-Krüger et al. 2000, Walter et al. 2008). The remaining publications predefined the treatment sequence, i.e. a combined
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treatment consisting of non surgical endodontic therapy with a non-surgical and/or a surgical periodontal therapy. Periodontal surgery consisted of an open flap debridement alone or in combination with regenerative or resective procedures.
Incomplete tissue healing after evaluation of the first treatment step may lead to the decision of further procedures (Dietrich et al. 2003). Healing of periapical lesions may take up to 4 years (European Society of Endodontology 2006) or longer (Ricucci et al. 2009). This process may be modified by several hereditary, environmental and behavioural risk factors, e.g. a smoking habit (Walter et al. 2008, Rodriguez et al. 2012, Walter et al. 2012b). Similarly, the improvement of periodontal conditions subsequent to scaling and root planing may take several months, with the deeper the initial PPD the longer the time for PPD reduction (Badersten et al. 1984). An observation time of at least 6 to 12 months before reevaluation of the first treatment step was suggested by Zehnder (Zehnder 2001). The publications included in this review reported a follow-up time between six and 12 months. However, with respect to the individual range of the time required for periodontal tissue healing and the absence of radiographic changes in early stages of healing, the interpretation of treatment results after six to 12 months seems to be associated with some bias (Hirsch et al. 1989, Jansson et al. 1997, Kim et al. 2008). The results from included studies and case series may need to be regarded as short-term outcomes. Follow-up examinations after an observation period of several years would be desirable although challenging.
With respect to the uncertain treatment outcome of periodontal-endodontic lesions and the successful outcome of less invasive treatment approaches (Stamas & Johnson 1994, Haueisen et al. 1999, Ratka-Krüger et al. 1999, Haueisen et al. 2000, Ratka-Krüger et al. 2000), the concept of a sequential treatment with re-evaluation at different treatment stages may also be supported from an economic point of view. Financial costs and time efforts increase dramatically with more invasive treatment approaches (Walter et al. 2012c). On the other hand patient-centred outcomes, including quality of life, treatment time and costs, are of increasing importance within clinical trials to ensure an appropriate allocation of resources (Brägger 2005, Walter et al. 2012c).
Conclusions and clinical relevance Taken together this review may provide some evidence for root canal treatment as a first treatment
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step for the treatment of combined periodontal-endodontic lesions with increased PPD and a negative response of pulp sensibility testing. A reasonable time for healing of the endodontic lesion after root canal treatment is suggested to consider before further therapy is applied. The summarized findings from this analysis may support this concept from a biological, i.e. individual range for time for wound healing, and from a clinical perspective, i.e. evidence from two retrospective clinical studies and five case reports.
References
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Table 1. Characteristics of included studies.
Study First author design (year of publica tion)
Hassa n et al. (1986)
Haueis en et al. (2000)
Number of teeth and patients, age, gender, exclusion criteria
prospect 14 teeth ive case 14 patients series 25 - 40 yrs exclusion criteria: systemic diseases, teeth excessivel y mobile/re quiring splinting
retrospe ctive case series
10 teeth 51.2 yrs (mean)
Tooth Clinical type (n) manifestations (n)
Radiograp hic manifestat ions (n)
Additi onal diagn osis (n)
Treatment sequence
Follo # w-up
maxilla • mean PD ry and 14.29 ± 1.76 mandib mm (range ular 12.5 - 17 incisors mm) (14) • no vitality (14)
-
-
SRP + Occl + 6 mo – (2 w) – RCT1 (GP, LC) + PS (RBF, D) + root demineraliz ation (citric acid)
Counf ounding factor s consi dered
To PD at followot up h los s (n)
Additional outcomes
Num ber of drop outs (patient s) and reas ons
2
mean attachment gain 8.16 ± 2.9 mm
tooth 2, NFD type, age, systemi c diseas es
6.125 ± 4.076 mm (mean ± SD) in 10 patients: 3.2 - 5.2 mm (range)
in 10 patients: attachment gain 7.9 - 9.9 mm
in 2 patients: in 2 patients: 14.2 mm attachment 15.3 mm gain 2.8 mm (range) 1.7 mm radiographic signs of partially bone fill, continuity of lamina dura mandib • narrow PD 9 ular - 12 mm (10) molars (10) • pain (1) • pus discharge from gingival margin (3) • FI (7) • mobility
periradicul fistula ar (mesial (4) and/or distal) and interradic ular radiolucen cy (10)
RCT1 – (CD, 3 w) – RCT2 (GP, S, LC)
+6 mo
0
2 - 4 mm (range)
0 + 12
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2 - 4 mm
no inflammation, no FI, no increased mobility, no sensitivity to percussion, radiographic signs of complete bone
0
0
tooth type, age
Accepted Article RatkaKrüger et al. (2000)
Sun & Liu (2009)
mo
grade I (2), grade II (2) • no vitality (7), unclear response to pulp test (3) • sensitivity to percussion (2) • Cp treatment and filling (2), crown or partial crown (8)
retrospe ctive case series
20 teeth
prospect 37 teeth ive case 30 patients series 28 - 53 yrs 18 male, 12 female
repair (2) or advanced bone repair (8) radiographic signs of complete bone repair (except two second molars with horizontal bone loss of 1 - 2 mm)
• mean PD 11.3 mm
fistula local narrow bone loss to apex, • swelling interradic and/or pus ular discharge from gingival and/or periapical margin radiolucen • FI (18) • no vitality or cy without interappro unclear response to ximal pulp test (20) bone loss • sensitivity to in molars, periapical percussion radiolucen sometimes cy (> 0.5 unclear • Cp treatment of root length) and filling (9), crown or with partial crown widened periodont (11) al ligament space bicuspi teeth with 6 mo bone loss ds (13), follow-up (n = molars 29) (24) • mean PD 6.62 ± 0.230 mm • mean CAL 8.76 ± 0.209 mm • mean mobility 1.66 ± 0. 134 mandib ular molars (15), maxilla ry molars (4), other tooth (1)
(range)
RCT1 – (CD, within 2 mo) – RCT2 (GP, S, LC)
+6 mo
5
3.1 mm (mean)
11 2.2 mm (mean)
+ 12 mo
no FI in 10 of 15 molars, radiographic signs of improvement up to complete regeneration in most teeth
RCT1 – (1 w) – Occl + SRP – (4 w) – PS (MWF, a BG , D, AB amox/metr o)
+6 mo
3
2.83 ± 0.149 mm*
18 2.42 ± 0.233 mm*
+ 12 mo
mean CAL 6.79 3, NFD ± 0.182 mm* mean mobility 18, 1.38 ± 0.092* NFD mean CAL 6.58 ± 0.268 mm* mean mobility 1.26 ± 0.104*
• pain • swelling • no vitality (37) Control: • mean PD 6.04 ± 0.37 mm • mean CAL 1.60 ± 0.19 mm • mean mBI 1.86
18 male, 12 female
Control : anterior teeth (2), bicuspi ds (5), molars (8)
exclusion criteria: systemic diseases, smoking, pregnanc y,
Test: Test: anterior • mean PD teeth 6.01 ± 0.31 (4), mm bicuspi • mean CAL ds (4), 1.57 ± 0.20 molars
periapical, lateral and/or interradic ular radiolucen cy
0 Control: • mean CAL 1.15 ± 0.21 mm • mean mBI 0.80
Control: • mean PAI 3.27
Test: • mean 0 CAL 1.06 ± 0.19 mm • mean mBI 0.67
Test: • mean PAI
11, NFD
no FI in 6 of 9 molars, radiographic signs of improvement up to complete regeneration in most teeth
teeth with 12 mo follow-up (n = 19) • mean PD 6.74 ± 0.285 mm • mean CAL 8.79 ± 0.282 mm • mean mobility 1.68 ± 0.172
Li et al. prospect 30 teeth 30 (2012) ive randomi patients zed controlle 44 yrs (mean) d trial
tooth 5, NFD type
to ot h typ e, ag e, sm oki ng , sy ste mi c dis ea
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Control: • 5.43 ± 0.26 mm (mean ± SD)
Test: • 4.77 ± 0.31 mm** (mean ± SD)
Control:
•
tooth type, age, experie nce of therapi st
Accepted Article
antibiotic (7) intake during observatio n period
mm • mean mBI 1.93
3.20
Control: • mean CAL 1.01 ± 0.14 mm • mean mBI 0.60 • mean PAI 3.00
• increased mobility • no vitality (30)
Test: • mean CAL 0.67 ± 0.12 mm** • mean mBI 0.13** • mean PAI 2.47
se • 5.64 ± s, 0.33 mm ex (mean ± pe SD) rie nc e of Test: th • 4.34 ± er 0.23 api mm** st (mean ± SD)
a , xenograft; b, AH26; c, Cortisomol; d, 1,5 W, continuous wave, one application (15 s); e, 1 W, continuous wave, one application daily (15 s) for 5 days; AB, systemic antiobiotics; amox, amoxicillin; BG, bone graft; CAL, clinical attachment loss; CD, calcium hydroxide dressing; Cp, caries profunda; D, periodontal dressing; FI, furcation involvement; GP, gutta percha; LC, lateral condensation; M, membrane; mBI, modified bleeding index; metro, metronidazole; mo, months; MWF, modified Widman flap; NFD, not further described; Occl, occlusal adjustment; PAI, periapical index; PD, probing depth; PS, periodontal surgery; RCT, root canal treatment; RBF, reverse bevel flap; RF, rotary files; S, sealer; SRP, scaling and root planing; w, weeks; yrs, years; #, time related to last treatment step; *, p < 0.05 (difference between baseline and outcome); **, p < 0.05 (difference between control and test group); the wording used in the table was adapted from the publications included.
Table 2. Characteristics of included case reports. First author (year of publication)
Moucachen et al. (1981) Geurtsen et al. (1985) Stamas & Johnson (1994) Haueisen et al. (1999) Haueisen et al. (1999) Ratka-Krüger et al. (1999)
Radiogra phic manifesta tions
Additi Treatment sequence onal diagn osis
Follo PD Additional w-up (mm) outcomes # (mo) at ## follow -up
NV, Per
A, L
-
Extraction
-
-
-
13
NV, R
A, L, IR, wPLS
-
Extraction
-
-
-
M 64 NR NR 26
7
NV, Pu, M0, R
A, L, IR
-
RCT1 + RCT2
12
2-3
BF
M 59 NR NR 36
12
UV, Pu, Per, R
A, L
-
RCT1 + RCT2
18
2
BF
M 56 NR NR 46
12
UV, Pu, Per, R
A, L, IR
-
RCT1 + RCT2
12
2-3
BF
RCT1 + RCT2
6
3
BF
Ge A Peri Sm Too n- ge o# th ode king type r
PD Clinical (mm) manifestations at basel ine##
M 50 NR NR 38
12
F
17 NR NR 46
M 56 NR NR 47
12
NV, Pu, S, R, FI
A, L, IR
Ab, Fis
Wood et al. (2003) M 62 NR NR 46
11
NV, Pa, Per, C, R, FI
A, L, IR
-
RCT1 + RCT2 + SRP
6
4
no FI
Zubery & Machtei F (1993)
23 AgP NR 22
10
NV, Pa, S, M2
A, L
Fis
RCT1 + SRP - (3 mo) - SRP
21
2
BF, M0-1
Zucchelli (2007)
39 P
12
A, L
Fis
36
3
BF, M0
5
BF, M1, AttG 3 mm
F
NR 12
Zehnder et al. (2001)
M 28 AgP NR 15
8
Kresic (1994)
M 70 NR NR 43
11
Zubery & Machtei F 23 AgP NR 11 (1993) Walter et al. M 53 ChP HS 32 (2008) Danesh-Meyer M 40 NR NR 36 (1999) Haueisen & F 62 NR NR 46 Heidemann (2002) John et al. (2004)
F
58 NR NR 21
10 8i
UV, M3, Rec, infraBDh NV, Pu, Pa, Per, M3 NV, R NV, Pa, S, M2, bBLh NV, R, Feh, h infraBD
12 14
NV, Pu, R, FI , h infraBD NV, Pu, Pa, Per, h S, M2, R, FI
Ghezzi et al. (2012)
M 38 NR NR 21
9
Oh et al. (2009)
F
9
Politis et al. (1986) F
19 NR NR 12
A, L
-
A, L
Fis
A, L
-
L
-
10
NV, S, bBL , h infraBD h NV, Pu, infraBD , bBLh NV, M2, R, Rec, FIh, infraBD h NV, M2
6.5
RCT1 + SRP - (6 mo) - PS
22
RCT1 + SRP - (3 mo) - SRP - (9 mo) 12 – PS + ES RCT1 + RCT2 - (14 mo) - PS (BG a, 32 b f M , AB ) c
d
4
BF, nPLS
2
BF, M0-1
4
BF
2
BF, AttG 8 mm
f
RCT1 + PS (BG , M , AB ) + RCT2 (4 mo) - RCT3
6
-
RCT1 + PS (Res) + Spl
12
1
BF, M1
-
RCT1 + Spl + PS (EMD, BGa, ABf)
9
4
BF, M1
A, L, AccR
Fis
RCT1 + RCT2 + PS (Res, BG , AB ) 12
3-4
BF
L
-
RCT1 + SRP + PS (BGa,e, Mb, ABf)
24
3
BF
A, L
-
RCT1 + SRP + PS (BGe, Md, ABk) (12 mo) - PS (BGi, Mb, ABk)
10
3
BF, no BOP
A
-
RCT1 + PS (BGc) + ES
12
2
BF, M0
A, L, IR
NV, M2, infraBDh L h
7
16
Fis
h
12
Yavuz et al. (2008) M 25 NR NR 22
50 NR NS
L
RCT1 + SRP + Spl - (4 mo) - PS (EMD, BGa, ABf) RCT1 + SRP + RCT2 + RCT3 - (4 mo) - PS
e
a
g
, xenograft; b, bioabsorbable; c, alloplast; d, nonresorbable; e, autograft; f, systemic application; g, local application; h, intraoperative finding; i, data from patients record; j, allograft; k, local and systemic application; A, apical radiolucency; Ab, abscess; AB, antibiotics; AccR, accessory root; AgP, aggressive periodontitis; AttG, attachment gain; bBL, buccal bone loss; BF, radiographic signs of bone fill; BG, bone graft; BOP, bleeding on probing;
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Accepted Article
C, caries; ChP, chronic periodontitis; EMD, enamel matrix derivates; ES, endodontic surgery; F, female; Fe, fenestration; Fis, fistula; FI, furcation involvement; HS, heavy smoker; infraBD, infrabony defect; IR, interradicular radiolucency; L, lateral radiolucency; M, male; Me, membrane; M, mobility (grade 0-3); nPLS, normal periodontal ligament space; NR, not reported; NS, non-smoker; NV, negative vitality test response; P, periodontitis (not further specified); Pa, pain; Per, positive percussion test; PS, periodontal surgery; Pu, pus; R, restoration; RCT, root canal treatment; Rec, recession; Res, root resection; S, swelling; Spl, splint; SRP, scaling and root planing; UV, unclear or delayed vitality test response; wPLS, widened periodontal ligament space; #, general periodontal conditions; ##, highest reported PD; ###, time related to last treatment step; +, time between various treatment steps < 3 months; for more details see Appendix 6.
Figure legend
Fig. 1.
Selection process of the studies included (Moher et al. 2009).
Appendix 1
PRISMA 2009 Checklist.
Appendix 2
Electronic search strategy for the databases MEDLINE and EMBASE.
Appendix 3
Scores for assessment of methodological and reporting quality.
Appendix 4
Studies and case series excluded based on full text analysis, and reason for exclusion.
Appendix 5
Case reports and reviews based on full text analysis, and reason for exclusion.
Appendix 6
Characteristics of included case reports in detail.
Appendix 7
Quality assessment of included studies.
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Selection process of the studies included (Moher et al. 2009).
Accepted Article
Fig. 1.
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