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Clinical Outcome of Endodontic Microsurgery That Uses EndoSequence BC Root Repair Material as the Root-end Filling Material
Clinical Research
Clinical Outcome of Endodontic Microsurgery That Uses EndoSequence BC Root Repair Material as the Root-end Filling Material Nicole Shinbori, DDS,* Ana Maria Grama, DDS,† Yogesh Patel, DDS,*‡ Karl Woodmansey, DDS,* and Jianing He, DMD, PhD*‡ Abstract Introduction: The purpose of this retrospective study was to determine the clinical and radiographic outcome of root-end surgery when EndoSequence BC Root Repair (ES-BCRR) was used as the root-end filling material and to identify any possible prognostic factors that may have affected the healing outcome. Methods: Clinical records and periapical radiographs were collected from patients who had undergone endodontic microsurgery between 2009 and 2013 in a private endodontic office and had a minimum 1-year follow-up. All surgical procedures were performed by a single endodontist. ES-BCRR was used as the root-end filling material in all cases. Outcome was categorized into healed, healing, and non-healing on the basis of clinical and radiographic findings. The healed and healing cases were pooled and considered as success, and non-healing cases were considered failure. For statistical analysis of the prognostic factors, the dependent variable was the dichotomous outcome (ie, success versus failure). Results: Ninety-four patients with 113 teeth met the inclusion criteria and were included in the study. The overall success rate was 92.0%. None of the prognostic factors, including age, sex, tooth position, size of periapical radiolucency, presence of a sinus tract, preoperative symptoms, and retreatment previous to surgery, appeared to have any significant effects on the outcome (P > .05). Conclusions: This current study suggests that ES-BCRR is a suitable root-end filling material to be used in endodontic surgery. (J Endod 2015;-:1–6)
Key Words BC Root Repair material, bioceramics, clinical outcome, endodontic microsurgery, prognostic factors
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ith the advancements in endodontic surgery such as the use of the operating microscope and microsurgical techniques, the success rate of modern endodontic surgery has been reported to be as high as 94% (1–4) compared with 60% success rate with traditional root-end surgery techniques (5, 6). Root-end filling materials used in endodontic surgery have advanced over the years. The ideal root-end filling material seals the contents of the root canal system within the canal, preventing egress of any bacteria, bacterial by-products, or toxic material into the surrounding periradicular tissues. The material should be nonresorbable, biocompatible, and dimensionally stable over time. It should be able to induce regeneration of the periodontal ligament complex, specifically cementogenesis over the root-end filling itself. The handling properties and working time should allow the placement of the material with sufficient ease (7). Mineral trioxide aggregate (MTA) is a widely used root-end filling material because of its excellent sealing ability and biocompatibility (8). Unfortunately, MTA has many disadvantages that include a long setting time, low washout resistance, and difficult handling properties (9). It is also technique sensitive and may cause tooth discoloration (9). A more ideal root-end filling material is still needed to improve on these properties. Bioceramic-based materials have been recently introduced to endodontic practice because of their advantageous physical and biological properties. Bioceramics are the result of the combination between calcium silicate and calcium phosphate that are applicable for biomedical and dental use (10). EndoSequence BC Root Repair (ESBCRR) (Brassler USA, Savannah, GA) material is a bioceramic-based material available to endodontists since 2010. It can be used as a root-end filling material as well as a root repair material. EndoSequence BC sealer is a similar bioceramic-based material used for root canal obturation. The manufacturer lists the composition of ES-BCRR as calcium silicates, calcium phosphate monobasic, zirconium oxide, tantalum oxide, along with filler and thickening agents. Many in vitro and in vivo studies have shown that ESBCRR is biocompatible, nontoxic, nonshrinking, and chemically stable within the biological environment (11–13). It also exhibits antibacterial activities against Enterococcus faecalis possibly because of its alkaline pH (14, 15). In addition, ESBCRR has many desirable clinical properties; it is premixed, has intermediate restorative material–like handling characteristics, has optimal radiopacity (10), and does not cause tooth discoloration (16). It has been proposed that bioceramic-based materials are able to form hydroxyapatite when in contact with moisture and ultimately form a bond between dentin and the filling material (10). The reported setting time of ESBCRR has been inconsistent and ranges from 4 hours to more than 48 hours (17). Despite the encouraging evidence from in vitro and animal studies, patient-based studies on the clinical performance of ES-BCRR are still lacking. Currently there are no
From the *Department of Endodontics, Baylor College of Dentistry, Texas A&M University System Health Science Center, Dallas; †Advanced Education in General Dentistry, Lutheran Medical Center, El Paso; and ‡Private Practice, Dallas, Texas. Address requests for reprints to Dr Jianing He, Department of Endodontics, Baylor College of Dentistry, 3302 Gaston Avenue, Dallas, TX 75246. E-mail address: jhe@ bcd.tamhsc.edu 0099-2399/$ - see front matter Copyright ª 2015 American Association of Endodontists. http://dx.doi.org/10.1016/j.joen.2014.12.028
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Surgery Outcome with BC Putty
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Clinical Research published clinical studies on the success rate of endodontic microsurgeries when ES-BCRR is used as a retrograde filling material. Previous studies suggest that the type of root-end filling material can have an impact on the outcome of apical surgery (18, 19). Therefore, the purpose of this retrospective study was to determine the clinical and radiographic outcome of root-end surgery when ES-BCRR was used as the root-end filling material and to identify any possible prognostic factors that may have affected the healing outcome.
Materials and Methods Case Selection and Surgical Procedure A search of all patients treated in an endodontic private practice setting from 2009 through 2013 was performed. Patients were selected on the basis of the following inclusion criteria: 1. A tooth that had surgical root canal treatment where ES-BCRR was used as the retrofilling material 2. Adequate existing root canal treatment 3. American Society of Anesthesiologists I or II 4. Radiographs documenting pretreatment, post-treatment, and follow-up of good diagnostic quality 5. Documented 1-year minimum recall Patients were excluded from the study if there was evidence of a preexisting vertical root fracture, which was seen radiographically as a J-shaped radiolucency. All clinical procedures were performed by a single operator (Y.P.) who used a surgical operating microscope (Opmi PROergo; Carl Zeiss, Gottingen, Germany). Patients were anesthetized with 2% lidocaine with 1:100,000 epinephrine and 2% lidocaine with 1:50,000 epinephrine (Septodont, Brampton, ON, Canada). A full-thickness flap was reflected to 2 teeth mesial and 1 tooth distal of the surgery site. If the surgical site involved the aesthetic zone, a papilla-based flap was reflected. Osteotomies were performed with a size 4 round bur in an Impact Air 45 handpiece (NSK; Nakanishi Inc, Kanuma-shi Tochigi-ken, Japan) under copious sterile water spray. A minimum of a 3-mm root section, depending on the curvature, was performed with a 7025 long shank fissure bur (Brassler USA) under copious sterile saline irrigation. Removal of the root tip and granulation tissue was performed with a large curette and sent for biopsy. The resected root surfaces were stained with methylene blue (Sigma-Aldrich, St Louis, MO) and inspected with micromirrors (Hu-Friedly, Los Angeles, CA) under high magnification to examine the cleanliness of the root-end resection and to identify any cracks or missed canals. Root-end cavity preparations, extending at least 3 mm into the canal space, were made by using reverse angle ultrasonic root-end preparation tips (Satelec Corp, Bordeaux, France). Epinephrine pellets were placed in the osteotomy for hemostasis for 10 minutes, while a radiograph was taken to check the root-end resection and Retro-prep (MicroMega, Besanc¸on, France). The epinephrine pellets were removed, and the canals were dried by using a Stropko irrigator (SybronEndo, Orange, CA) and paper points. In all cases, root-end filling was performed by using ES-BC sealer and ES-BCRR putty. The sealer was placed in the Retro-prep with a Vista Visco-Tip (Inter-Med, Inc, Racine, WI), and the BC putty was rolled into small, 2- to 3-mm cones and delivered into the Retroprep in increments by using the back end of a small spoon. The retrofilling material was then compacted with angled or straight condensers. For deeper preps, the back end of a paper point was used to achieve further compaction. More BC putty cones were placed into the canals until an adequate fill was achieved. The area was rinsed copiously with 30 mL sterile water. A freeze-dried cortical bone graft 2
Shinbori et al.
(Maxxeus Dental, Kettering, OH) was placed into the osteotomy. If a sinus exposure had occurred during the surgical procedure, calcium sulfate BonePlast QuickSet (BioMet Osteobiologics, Oakville, ON, Canada) was placed (2 cases). A resorbable bilayer collagen Bio-Gide (Geistlich Pharma, Princeton, NJ) membrane and Emdogain (Straumann USA LLC, Andover, MA) were used in cases with furcation involvement (2 cases), sinus tract communication (1 case), or if less than 4 mm of crestal bone remained (1 case). A sling suture around the involved teeth and a continuous locking in the vertical incision by using 5-0 gut sutures were used to close the wound site. If a membrane was used, 5-0 Vicryl was used instead. A postoperative radiograph was taken, and the patient was given postoperative instructions and prescriptions.
Clinical and Radiographic Evaluation The patients were followed up at 1 week, 3 months, 6 months, 1 year, and every year thereafter. The recall visits included a routine examination and periapical radiographs. The clinical data, including the signs and/or symptoms or loss of function, tenderness to percussion or palpation, subjective discomfort, mobility, sinus tract formation or periodontal pocket formation, postoperative complications, and type of restoration at follow-ups, were included in the recall record form. The postoperative radiographs were evaluated independently by 2 board-certified endodontic faculty members at Texas A&M Health Science Center, Baylor College of Dentistry by using the criteria established by Rud et al (20) and Molven et al (21). If there was disagreement on a radiograph, the 2 evaluators would have a discussion until an agreement on the outcome was reached. The radiographic healing classifications were as follows: 1. Complete healing: The reestablishment of the lamina dura 2. Incomplete healing: Some reduction of the former radiolucency 3. Unsatisfactory healing: No reduction or enlargement of the former radiolucency
Assessment of Outcome Outcome was categorized into healed, healing, and non-healing on the basis of clinical and radiographic findings. Cases with radiographic classification of complete healing and no clinical signs or symptoms were considered healed, cases with a radiographic classification of incomplete healing and no clinical signs or symptoms were considered healing, and cases with a radiographic classification of unsatisfactory healing or presence of any clinical signs or symptoms were considered non-healing. Both healed and healing cases were considered successful. Non-healing was considered failure (22). Patient-related factors and tooth-related factors were examined to identify any prognostic factor that may affect the treatment outcome. Patient-related factors included patient age and sex. Tooth-related factors included tooth position, presence or absence of sinus tract, size/ presence of periapical radiolucency, preoperative symptoms, and if retreatment was completed before surgery. The periapical radiolucencies were divided into 3 subgroups: large lesions with mean diameter >5 mm, small lesions with mean diameter <5 mm, or no lesion present at the time of surgery. Statistical Analysis For statistical analysis of the prognostic factors, the dichotomous outcome (ie, success versus failure) was used as the dependent variable. A univariate description with the percentage frequencies was generated to characterize the study material. Significant associations between the outcome and all the variables were examined by using the JOE — Volume -, Number -, - 2015
Clinical Research TABLE 1. Treatment Outcome by Patient and Preoperative Factors Factors
No. of healed
Healing
Failed
Success rate (%)
44/50 48/63
2/50 10/63
4/50 5/63
92.0 92.1
41/50 51/63
4/50 8/63
5/50 4/63
90.0 93.7
32/45 60/68
8/45 4/68
5/45 4/68
88.9 94.1
19/21 15/17 26/30 5/6 9/11 18/28
1/21 1/17 2/30 1/6 1/11 6/28
1/21 1/17 2/30 0/6 1/11 4/28
95.2 94.1 93.3 100 90.9 85.7
9/12 83/101
1/12 11/101
2/12 7/101
83.3 93.0
7/10 38/47 47/56
1/10 6/47 5/56
2/10 3/47 4/56
80.0 93.6 92.9
51/62 41/51
8/62 4/51
3/62 6/51
95.2 88.2
78/96 14/17
11/96 1/17
7/96 2/17
92.7 88.2
Gender Male Female Age (y) #45 >45 Arch type Mandibular Maxillary Tooth position Maxillary anterior Maxillary premolar Maxillary molar Mandibular anterior Mandibular premolar Mandibular posterior Retreatment Retreatment No retreatment Size of lesion No lesion #5 mm >5 mm Preoperative pain No pain Pain Sinus tract None Present
P value .732 .592 .064 .422
.494 .631
.305 .674
Fisher exact tests to identify the potential prognostic factors. All statistical tests were performed as two-tailed, and the level of significance was set at P < .05. All statistical analyses were performed with SPSS v19.0 software (IBM Corp, Somers, NY).
Results Ninety-four subjects with 113 treated teeth from June 2009 to January 2013 were included in this study. The study population comprised 53 women (63 teeth) and 41 men (50 teeth) with an age range of 20–88 years (mean, 49 years). Follow-up time ranged from 12 to 33 months, with a mean of 14.5 months. The demographic characteristics of the study subjects are summarized in Table 1. Of the 113 cases recalled, 104 were deemed successful, with an overall success rate of 92.0%. Of the 9 teeth that were deemed failures, 5 were radiographic failures, and 4 were clinically symptomatic teeth that had pain to percussion or palpation or still had a sinus tract present. Figure 1 shows examples of healed (Fig. 1A–C), healing (Fig. 1D– F), and non-healing cases (Fig. 1G–L). Table 1 presents the outcome categories according to the patient factors and tooth factors. None of the patient or treatment factors examined had any significant influence on outcome (P > .05).
Discussion Persistent periapical disease after nonsurgical endodontic treatment is frustrating for the clinician and the patient. A decision must be made to choose between nonsurgical retreatment and surgical treatment to retain the tooth. Information on treatment outcomes is essential for the decision-making process. With new materials being constantly introduced, it is necessary to collect clinical evidence on the performance of these materials to help the clinicians and the patients to make an informed decision. ES-BCRR has shown promising biological JOE — Volume -, Number -, - 2015
and physical properties as a new root-end filling material on the basis of in vitro and animal studies (11–16). The present retrospective study assessed the surgery outcome after a minimum of 1 year by using ES-BCRR as the retrofilling material. All surgeries were performed by a single operator, thus reducing treatment-related variables that may affect the outcome. We found an overall success rate of 92.0%, which was consistent with the range of success rates reported by previous studies that used similar modern surgical techniques (2, 23). In the present study, modern microsurgical technique was used for all cases. This technique included the use of surgical microscopes, ultrasonic root-end cavity preparation, and the use of a bioceramic-based root-end filling material. Previous studies have shown that modern microsurgical techniques significantly improve the outcome compared with traditional root-end surgery (4, 23, 24). The probability of success for endodontic microsurgery was 1.58 times higher than that for traditional root-end surgery (23). The follow-up period in this present study ranged from 1 to 3 years. A recent study (2) evaluated clinical outcome of endodontic microsurgery after 1 year and 4 years. They found no significant differences in the success rate between the 1-year or 4-year period; therefore, the 1-year recall appears to be sufficient in predicting healing after surgery. The retrofilling material provides a hermetic seal to prevent egress of bacteria and toxins from the periapical tissues. ES-BCRR was used as the retrofilling material in all the cases in the present study. The material is biocompatible, nontoxic, nonshrinking, and chemically stable within the biological environment (11, 12). Studies have shown that the material sets at a highly alkaline pH and has antibacterial activity (14, 15). Bioceramics have the advantage of forming hydroxyapatite and ultimately a bond between dentin and filling material (16). All of these characteristics can explain the high level of success when used as a retrofilling material. ES-BCRR comes premixed with an intermediate restorative
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Clinical Research
Figure 1. Representative periapical radiographs of cases in each outcome category. (A–C) Example showing complete healing. (A) Preoperative radiograph of case 30. (B) Postoperative radiograph of case 30. (C) Two-year follow-up radiograph of case 30 showing complete resolution of radiolucency and reattachment of periodontal ligament. (D–F) Example showing incomplete healing. (D) Preoperative radiograph of case 19. (E) Postoperative radiograph of case 19. (F) One-year follow-up radiograph of case 19 showing reduced periapical radiolucency. (G–I) Example showing unsatisfactory healing. (G) Preoperative radiograph of case 4. (H) Postoperative radiograph of case 4. (I) One-year follow-up radiograph of case 4 showing persistent periapical radiolucency. (J–L) Example of unsatisfactory healing. (J) Preoperative radiograph of case 3. (K) Postoperative radiograph of case 3. (L) One-year follow-up radiograph of case 3 showing persistent periapical radioluency around the mesiobuccal root.
material–like consistency and therefore is easier to handle (17). Although the popularity of ES-BCRR has grown significantly, the evidence supporting its clinical use as a root-end filling material is still lacking. This retrospective study shows promising results of ES-BCRR used in endodontic microsurgery. The high success rate observed in this study is comparable to that reported when MTA is used as the retrofilling material (1, 2), suggesting ES-BCRR is a viable alternative to MTA as a root-end filling material. Making an accurate preoperative diagnosis and appropriate case selection can influence surgical success. Patient-related and tooth-related factors need to be taken into consideration as important determinants when planning apical surgery against other treatment 4
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alternatives. Von Arx et al (18) published a thorough meta-analysis to assess potential prognostic factors for healing outcome in apical surgery. The outcome was found to be better in those cases without preoperative pain or signs, cases with good density of root canal filling, and cases with absence or size <5 mm of periapical lesion. Potential patient and treatment factors examined in this study included age, sex, tooth position, arch, size of periapical radiolucency, and retreatment previous to surgery. None of these factors were shown to be significant prognostic factors for treatment outcome. Regarding the patient-related factors, our findings are in agreement with the majority of previous studies (18, 19, 22) and suggest that healing after apical surgery does not seem to differ significantly JOE — Volume -, Number -, - 2015
Clinical Research between male and female patients or between younger and older patients. Outcome studies have looked at the success rate of teeth on the basis of tooth position and arch type. A prospective study by Song et al (25) found that tooth position (anterior) and arch type (maxilla) were found to be positive predictors. The maxillary anterior teeth tended to have a higher success rate than the other tooth groups, which they attributed to the relatively easy access and less complicated root anatomy. In the present study, molars had the lowest rate of success (86.5%) compared with premolars and anteriors (96.1%), but no significant difference was found possibly because of the uneven distribution of the number of teeth in different groups. This finding is consistent with 2 other previous reports (26, 27). Our present study showed no difference for healing rates for no lesions or lesions # or > 5 mm, which disagrees with the findings in the meta-analysis by Von Arx et al (18); however, it is in agreement with a number of other studies (3, 28). Larger lesions may be less likely and take longer to heal because of the lower number of progenitor cells present for bone regeneration. The lack of significance found in our present study may be attributed to a relatively small sample size and uneven sample distribution. A sinus tract was present in 17 cases (15%), and only 2 of those cases failed (88.2% success). The presence of a preoperative sinus tract did not significantly influence the success rate. These results agree with another study (3) that found cases with a preoperative sinus tract also had a high success rate of 94.1%. Two studies (19, 29) found that patients who have preoperative signs or symptoms have a significantly lower healing rate. However, patients included in our study who presented with pain at the initial examination were not significantly different in healing rates compared with patients without pain. This may be related to the different patient population and sample size in the different studies. Studies have shown that the success rate for apical surgery improves when orthograde root canal retreatment is combined with apical surgery (30). However, orthograde retreatment is not always a costeffective or realistic option for patients. In the present study, 101 teeth did not have retreatment before apical surgery, and these teeth had a success rate of 93%. Whether nonsurgical retreatment was performed before surgery did not appear to have an influence on the surgical success. In this retrospective study, the diagnosis, treatment planning, and surgical procedures were all performed by the same single operator. Although this may only reflect the clinical judgment and skills of a single endodontist and may not be truly representative, it does represent the scenario of the real-world private practice setting. The results provide important preliminary data that can be used to design future prospective cohort or randomized controlled trials. One limitation of the present study is the radiographic evaluation of treatment outcome. Although preoperative cone-beam computed tomography (CBCT) was performed to assist with surgical treatment planning, it was not routinely used to assess outcome. CBCT has become widely available and is able to detect periapical lesions with higher sensitivity; therefore, success rate determined by conventional radiographs may be overestimated compared with when it is evaluated with CBCT (31). However, the increased cost and radiation exposure need to be justified before CBCT can become a standard tool used for treatment follow-up. In conclusion, the use of ES-BCRR as a root-end filling material resulted in a high healing rate of 92.0% in endodontic microsurgery at a minimum 1-year recall examination. This evidence suggests that ES-BCRR is a suitable root-end filling material to be used in endodontic surgery. Future studies with a larger sample size are needed to confirm JOE — Volume -, Number -, - 2015
the findings and to identify potential prognostic factors that may impact the treatment outcome.
Acknowledgments The authors deny any conflicts of interest related to this study.
References 1. Song M, Kim E. A prospective randomized controlled study of mineral trioxide aggregate and super ethoxy–benzoic acid as root-end filling materials in endodontic microsurgery. J Endod 2012;38:875–9. 2. Song M, Nam T, Shin S, Kim E. Comparison of clinical outcomes of endodontic microsurgery: 1 year versus long-term follow-up. J Endod 2014;40:490–4. 3. Li H, Zhai F, Zhang R, Hou B. Evaluation of microsurgery with superEBA as root-end filling material for treating post-treatment endodontic disease: a 2-year retrospective study. J Endod 2014;40:345–50. 4. Setzer FC, Kohli MR, Shah SB, et al. Outcome of endodontic surgery: a meta-analysis of the literature—part 2: comparison of endodontic microsurgical techniques with and without the use of higher magnification. J Endod 2012;38:1–10. 5. Kvist T, Reit C. Results of endodontic retreatment: a randomized clinical study comparing surgical and nonsurgical procedures. J Endod 1999;25:814–7. 6. Setzer FC, Shah SB, Kohli MR, et al. Outcome of endodontic surgery: a meta-analysis of the literature—part 1: comparison of traditional root-end surgery and endodontic microsurgery. J Endod 2010;36:1757–65. 7. Johnson BR, Fayad MI, Witherspoon DE. Periradicular surgery. In: Cohen S, Hargreaves K, eds. Pathways of the Pulp, 10th ed. St Louis, MO: Mosby Elsevier; 2010:720–76. 8. Torabinejad M, Parirokh M. Mineral trioxide aggregate: a comprehensive literature review—part II: leakage and biocompatibility investigations. J Endod 2010;36: 190–202. 9. Parirokh M, Torabinejad M. Mineral trioxide aggregate: a comprehensive literature review—part III: clinical applications, drawbacks, and mechanism of action. J Endod 2010;36:400–13. 10. Candeiro GT, Correia FC, Duarte MA, et al. Evaluation of radiopacity, pH, release of calcium ions, and flow of a bioceramic root canal sealer. J Endod 2012;38: 842–5. 11. Ma J, Shen Y, Stojicic S, Haapasalo M. Biocompatibility of two novel root repair materials. J Endod 2011;37:793–8. 12. Damas BA, Wheater MA, Bringas JS, Hoen MM. Cytotoxicity comparison of mineral trioxide aggregates and EndoSequence Bioceramic root repair materials. J Endod 2011;37:372–5. 13. Bosio CC, Felippe GS, Bortoluzzi EA, et al. Subcutaneous connective tissue reactions to iRoot SP, mineral trioxide aggregate (MTA) Fillapex, DiaRoot BioAggregate and MTA. Int Endod J 2014;47:667–74. 14. Lovato KF, Sedgley CM. Antibacterial activity of EndoSequence Root Repair Material and ProRoot MTA against clinical isolates of Enterococcus faecalis. J Endod 2011; 37:1542–6. 15. Nair U, Ghattas S, Saber M, et al. A comparative evaluation of the sealing ability of 2 root-end filling materials: an in vitro leakage study using Enterococcus faecalis. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2011;112:e74–7. 16. Walsh RM, Woodmansey KF, Glickman GN, He J. Evaluation of compressive strength of hydraulic silicate-based root-end filling materials. J Endod 2014;40:969–72. 17. Charland T, Hartwell GR, Hirschberg C, Patel R. An evaluation of setting time of mineral trioxide aggregate and EndoSequence root repair material in the presence of human blood and minimal essential media. J Endod 2013;39:1071–2. 18. von Arx T, Pe~narrocha M, Jensen S. Prognostic factors in apical surgery with rootend filling: a meta-analysis. J Endod 2010;36:957–73. 19. von Arx T, H€anni S, Jensen SS. Clinical and radiographic assessment of various predictors for healing outcome one year after periapical surgery. J Endod 2007;33: 123–8. 20. Rud J, Andreasen JO, Jensen JE. Radiographic criteria for the assessment of healing after endodontic surgery. Int J Oral Surg 1972;1:195–214. 21. Molven O, Halse A, Grung B. Observer strategy and the radiographic classification of healing after endodontic surgery. Int J Oral Maxillofac Surg 1987;16:432–9. 22. Wang N, Knight K, Dao T, Friedman S. Treatment outcome in endodontics: the Toronto study—phases I and II: apical surgery. J Endod 2004;3:751–61. 23. Tsesis I, Rosen E, Taschieri S, et al. Outcome of surgical endodontic treatment performed by a modern technique: an updated meta-analysis of literature. J Endod 2013;39:332–9. 24. Kim S, Kratchman S. Modern endodontic surgery concepts and practice: a review. J Endod 2006;32:601–23. 25. Song M, Kim SG, Lee SJ, et al. Prognostic factors of clinical outcomes in endodontic microsurgery: a prospective study. J Endod 2013;39:1491–7.
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Clinical Research 26. Friedman S, Lustmann J, Shaharabany V. Treatment results of apical surgery in premolar and molar teeth. J Endod 1991;17:30–3. 27. Taschieri S, del Fabbro M, Testori T, et al. Endodontic surgery with ultrasonic retrotips: one-year follow-up. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2005; 100:380–7. 28. Barone C, Dao TT, Basrani BB, et al. Treatment outcome in endodontics: the Toronto study—phases 3, 4, and 5: apical surgery. J Endod 2010;36:28–35.
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29. Lustmann J, Friedman S, Shaharabany V. Relation of pre- and intraoperative factors to prognosis of posterior apical surgery. J Endod 1991;17:239–41. 30. Wu MK, Wesselink PR. Timeliness and effectiveness in the surgical management of persistent post-treatment periapical pathosis. Endod Top 2005;11:25–31. 31. Patel S, Wilson R, Dawood A, et al. The detection of periapical pathosis using digital periapical radiography and cone beam computed tomography: part 2—a 1-year post-treatment follow-up. Int Endod J 2012;45:711–23.
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Clinical Outcome of Endodontic Microsurgery That Uses EndoSequence BC Root Repair Material as the Root-end Filling Material Nicole Shinbori, DDS,* Ana Maria Grama, DDS,† Yogesh Patel, DDS,*‡ Karl Woodmansey, DDS,* and Jianing He, DMD, PhD*‡ Abstract Introduction: The purpose of this retrospective study was to determine the clinical and radiographic outcome of root-end surgery when EndoSequence BC Root Repair (ES-BCRR) was used as the root-end filling material and to identify any possible prognostic factors that may have affected the healing outcome. Methods: Clinical records and periapical radiographs were collected from patients who had undergone endodontic microsurgery between 2009 and 2013 in a private endodontic office and had a minimum 1-year follow-up. All surgical procedures were performed by a single endodontist. ES-BCRR was used as the root-end filling material in all cases. Outcome was categorized into healed, healing, and non-healing on the basis of clinical and radiographic findings. The healed and healing cases were pooled and considered as success, and non-healing cases were considered failure. For statistical analysis of the prognostic factors, the dependent variable was the dichotomous outcome (ie, success versus failure). Results: Ninety-four patients with 113 teeth met the inclusion criteria and were included in the study. The overall success rate was 92.0%. None of the prognostic factors, including age, sex, tooth position, size of periapical radiolucency, presence of a sinus tract, preoperative symptoms, and retreatment previous to surgery, appeared to have any significant effects on the outcome (P > .05). Conclusions: This current study suggests that ES-BCRR is a suitable root-end filling material to be used in endodontic surgery. (J Endod 2015;-:1–6)
Key Words BC Root Repair material, bioceramics, clinical outcome, endodontic microsurgery, prognostic factors
W
ith the advancements in endodontic surgery such as the use of the operating microscope and microsurgical techniques, the success rate of modern endodontic surgery has been reported to be as high as 94% (1–4) compared with 60% success rate with traditional root-end surgery techniques (5, 6). Root-end filling materials used in endodontic surgery have advanced over the years. The ideal root-end filling material seals the contents of the root canal system within the canal, preventing egress of any bacteria, bacterial by-products, or toxic material into the surrounding periradicular tissues. The material should be nonresorbable, biocompatible, and dimensionally stable over time. It should be able to induce regeneration of the periodontal ligament complex, specifically cementogenesis over the root-end filling itself. The handling properties and working time should allow the placement of the material with sufficient ease (7). Mineral trioxide aggregate (MTA) is a widely used root-end filling material because of its excellent sealing ability and biocompatibility (8). Unfortunately, MTA has many disadvantages that include a long setting time, low washout resistance, and difficult handling properties (9). It is also technique sensitive and may cause tooth discoloration (9). A more ideal root-end filling material is still needed to improve on these properties. Bioceramic-based materials have been recently introduced to endodontic practice because of their advantageous physical and biological properties. Bioceramics are the result of the combination between calcium silicate and calcium phosphate that are applicable for biomedical and dental use (10). EndoSequence BC Root Repair (ESBCRR) (Brassler USA, Savannah, GA) material is a bioceramic-based material available to endodontists since 2010. It can be used as a root-end filling material as well as a root repair material. EndoSequence BC sealer is a similar bioceramic-based material used for root canal obturation. The manufacturer lists the composition of ES-BCRR as calcium silicates, calcium phosphate monobasic, zirconium oxide, tantalum oxide, along with filler and thickening agents. Many in vitro and in vivo studies have shown that ESBCRR is biocompatible, nontoxic, nonshrinking, and chemically stable within the biological environment (11–13). It also exhibits antibacterial activities against Enterococcus faecalis possibly because of its alkaline pH (14, 15). In addition, ESBCRR has many desirable clinical properties; it is premixed, has intermediate restorative material–like handling characteristics, has optimal radiopacity (10), and does not cause tooth discoloration (16). It has been proposed that bioceramic-based materials are able to form hydroxyapatite when in contact with moisture and ultimately form a bond between dentin and the filling material (10). The reported setting time of ESBCRR has been inconsistent and ranges from 4 hours to more than 48 hours (17). Despite the encouraging evidence from in vitro and animal studies, patient-based studies on the clinical performance of ES-BCRR are still lacking. Currently there are no
From the *Department of Endodontics, Baylor College of Dentistry, Texas A&M University System Health Science Center, Dallas; †Advanced Education in General Dentistry, Lutheran Medical Center, El Paso; and ‡Private Practice, Dallas, Texas. Address requests for reprints to Dr Jianing He, Department of Endodontics, Baylor College of Dentistry, 3302 Gaston Avenue, Dallas, TX 75246. E-mail address: jhe@ bcd.tamhsc.edu 0099-2399/$ - see front matter Copyright ª 2015 American Association of Endodontists. http://dx.doi.org/10.1016/j.joen.2014.12.028
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Surgery Outcome with BC Putty
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Clinical Research published clinical studies on the success rate of endodontic microsurgeries when ES-BCRR is used as a retrograde filling material. Previous studies suggest that the type of root-end filling material can have an impact on the outcome of apical surgery (18, 19). Therefore, the purpose of this retrospective study was to determine the clinical and radiographic outcome of root-end surgery when ES-BCRR was used as the root-end filling material and to identify any possible prognostic factors that may have affected the healing outcome.
Materials and Methods Case Selection and Surgical Procedure A search of all patients treated in an endodontic private practice setting from 2009 through 2013 was performed. Patients were selected on the basis of the following inclusion criteria: 1. A tooth that had surgical root canal treatment where ES-BCRR was used as the retrofilling material 2. Adequate existing root canal treatment 3. American Society of Anesthesiologists I or II 4. Radiographs documenting pretreatment, post-treatment, and follow-up of good diagnostic quality 5. Documented 1-year minimum recall Patients were excluded from the study if there was evidence of a preexisting vertical root fracture, which was seen radiographically as a J-shaped radiolucency. All clinical procedures were performed by a single operator (Y.P.) who used a surgical operating microscope (Opmi PROergo; Carl Zeiss, Gottingen, Germany). Patients were anesthetized with 2% lidocaine with 1:100,000 epinephrine and 2% lidocaine with 1:50,000 epinephrine (Septodont, Brampton, ON, Canada). A full-thickness flap was reflected to 2 teeth mesial and 1 tooth distal of the surgery site. If the surgical site involved the aesthetic zone, a papilla-based flap was reflected. Osteotomies were performed with a size 4 round bur in an Impact Air 45 handpiece (NSK; Nakanishi Inc, Kanuma-shi Tochigi-ken, Japan) under copious sterile water spray. A minimum of a 3-mm root section, depending on the curvature, was performed with a 7025 long shank fissure bur (Brassler USA) under copious sterile saline irrigation. Removal of the root tip and granulation tissue was performed with a large curette and sent for biopsy. The resected root surfaces were stained with methylene blue (Sigma-Aldrich, St Louis, MO) and inspected with micromirrors (Hu-Friedly, Los Angeles, CA) under high magnification to examine the cleanliness of the root-end resection and to identify any cracks or missed canals. Root-end cavity preparations, extending at least 3 mm into the canal space, were made by using reverse angle ultrasonic root-end preparation tips (Satelec Corp, Bordeaux, France). Epinephrine pellets were placed in the osteotomy for hemostasis for 10 minutes, while a radiograph was taken to check the root-end resection and Retro-prep (MicroMega, Besanc¸on, France). The epinephrine pellets were removed, and the canals were dried by using a Stropko irrigator (SybronEndo, Orange, CA) and paper points. In all cases, root-end filling was performed by using ES-BC sealer and ES-BCRR putty. The sealer was placed in the Retro-prep with a Vista Visco-Tip (Inter-Med, Inc, Racine, WI), and the BC putty was rolled into small, 2- to 3-mm cones and delivered into the Retroprep in increments by using the back end of a small spoon. The retrofilling material was then compacted with angled or straight condensers. For deeper preps, the back end of a paper point was used to achieve further compaction. More BC putty cones were placed into the canals until an adequate fill was achieved. The area was rinsed copiously with 30 mL sterile water. A freeze-dried cortical bone graft 2
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(Maxxeus Dental, Kettering, OH) was placed into the osteotomy. If a sinus exposure had occurred during the surgical procedure, calcium sulfate BonePlast QuickSet (BioMet Osteobiologics, Oakville, ON, Canada) was placed (2 cases). A resorbable bilayer collagen Bio-Gide (Geistlich Pharma, Princeton, NJ) membrane and Emdogain (Straumann USA LLC, Andover, MA) were used in cases with furcation involvement (2 cases), sinus tract communication (1 case), or if less than 4 mm of crestal bone remained (1 case). A sling suture around the involved teeth and a continuous locking in the vertical incision by using 5-0 gut sutures were used to close the wound site. If a membrane was used, 5-0 Vicryl was used instead. A postoperative radiograph was taken, and the patient was given postoperative instructions and prescriptions.
Clinical and Radiographic Evaluation The patients were followed up at 1 week, 3 months, 6 months, 1 year, and every year thereafter. The recall visits included a routine examination and periapical radiographs. The clinical data, including the signs and/or symptoms or loss of function, tenderness to percussion or palpation, subjective discomfort, mobility, sinus tract formation or periodontal pocket formation, postoperative complications, and type of restoration at follow-ups, were included in the recall record form. The postoperative radiographs were evaluated independently by 2 board-certified endodontic faculty members at Texas A&M Health Science Center, Baylor College of Dentistry by using the criteria established by Rud et al (20) and Molven et al (21). If there was disagreement on a radiograph, the 2 evaluators would have a discussion until an agreement on the outcome was reached. The radiographic healing classifications were as follows: 1. Complete healing: The reestablishment of the lamina dura 2. Incomplete healing: Some reduction of the former radiolucency 3. Unsatisfactory healing: No reduction or enlargement of the former radiolucency
Assessment of Outcome Outcome was categorized into healed, healing, and non-healing on the basis of clinical and radiographic findings. Cases with radiographic classification of complete healing and no clinical signs or symptoms were considered healed, cases with a radiographic classification of incomplete healing and no clinical signs or symptoms were considered healing, and cases with a radiographic classification of unsatisfactory healing or presence of any clinical signs or symptoms were considered non-healing. Both healed and healing cases were considered successful. Non-healing was considered failure (22). Patient-related factors and tooth-related factors were examined to identify any prognostic factor that may affect the treatment outcome. Patient-related factors included patient age and sex. Tooth-related factors included tooth position, presence or absence of sinus tract, size/ presence of periapical radiolucency, preoperative symptoms, and if retreatment was completed before surgery. The periapical radiolucencies were divided into 3 subgroups: large lesions with mean diameter >5 mm, small lesions with mean diameter <5 mm, or no lesion present at the time of surgery. Statistical Analysis For statistical analysis of the prognostic factors, the dichotomous outcome (ie, success versus failure) was used as the dependent variable. A univariate description with the percentage frequencies was generated to characterize the study material. Significant associations between the outcome and all the variables were examined by using the JOE — Volume -, Number -, - 2015
Clinical Research TABLE 1. Treatment Outcome by Patient and Preoperative Factors Factors
No. of healed
Healing
Failed
Success rate (%)
44/50 48/63
2/50 10/63
4/50 5/63
92.0 92.1
41/50 51/63
4/50 8/63
5/50 4/63
90.0 93.7
32/45 60/68
8/45 4/68
5/45 4/68
88.9 94.1
19/21 15/17 26/30 5/6 9/11 18/28
1/21 1/17 2/30 1/6 1/11 6/28
1/21 1/17 2/30 0/6 1/11 4/28
95.2 94.1 93.3 100 90.9 85.7
9/12 83/101
1/12 11/101
2/12 7/101
83.3 93.0
7/10 38/47 47/56
1/10 6/47 5/56
2/10 3/47 4/56
80.0 93.6 92.9
51/62 41/51
8/62 4/51
3/62 6/51
95.2 88.2
78/96 14/17
11/96 1/17
7/96 2/17
92.7 88.2
Gender Male Female Age (y) #45 >45 Arch type Mandibular Maxillary Tooth position Maxillary anterior Maxillary premolar Maxillary molar Mandibular anterior Mandibular premolar Mandibular posterior Retreatment Retreatment No retreatment Size of lesion No lesion #5 mm >5 mm Preoperative pain No pain Pain Sinus tract None Present
P value .732 .592 .064 .422
.494 .631
.305 .674
Fisher exact tests to identify the potential prognostic factors. All statistical tests were performed as two-tailed, and the level of significance was set at P < .05. All statistical analyses were performed with SPSS v19.0 software (IBM Corp, Somers, NY).
Results Ninety-four subjects with 113 treated teeth from June 2009 to January 2013 were included in this study. The study population comprised 53 women (63 teeth) and 41 men (50 teeth) with an age range of 20–88 years (mean, 49 years). Follow-up time ranged from 12 to 33 months, with a mean of 14.5 months. The demographic characteristics of the study subjects are summarized in Table 1. Of the 113 cases recalled, 104 were deemed successful, with an overall success rate of 92.0%. Of the 9 teeth that were deemed failures, 5 were radiographic failures, and 4 were clinically symptomatic teeth that had pain to percussion or palpation or still had a sinus tract present. Figure 1 shows examples of healed (Fig. 1A–C), healing (Fig. 1D– F), and non-healing cases (Fig. 1G–L). Table 1 presents the outcome categories according to the patient factors and tooth factors. None of the patient or treatment factors examined had any significant influence on outcome (P > .05).
Discussion Persistent periapical disease after nonsurgical endodontic treatment is frustrating for the clinician and the patient. A decision must be made to choose between nonsurgical retreatment and surgical treatment to retain the tooth. Information on treatment outcomes is essential for the decision-making process. With new materials being constantly introduced, it is necessary to collect clinical evidence on the performance of these materials to help the clinicians and the patients to make an informed decision. ES-BCRR has shown promising biological JOE — Volume -, Number -, - 2015
and physical properties as a new root-end filling material on the basis of in vitro and animal studies (11–16). The present retrospective study assessed the surgery outcome after a minimum of 1 year by using ES-BCRR as the retrofilling material. All surgeries were performed by a single operator, thus reducing treatment-related variables that may affect the outcome. We found an overall success rate of 92.0%, which was consistent with the range of success rates reported by previous studies that used similar modern surgical techniques (2, 23). In the present study, modern microsurgical technique was used for all cases. This technique included the use of surgical microscopes, ultrasonic root-end cavity preparation, and the use of a bioceramic-based root-end filling material. Previous studies have shown that modern microsurgical techniques significantly improve the outcome compared with traditional root-end surgery (4, 23, 24). The probability of success for endodontic microsurgery was 1.58 times higher than that for traditional root-end surgery (23). The follow-up period in this present study ranged from 1 to 3 years. A recent study (2) evaluated clinical outcome of endodontic microsurgery after 1 year and 4 years. They found no significant differences in the success rate between the 1-year or 4-year period; therefore, the 1-year recall appears to be sufficient in predicting healing after surgery. The retrofilling material provides a hermetic seal to prevent egress of bacteria and toxins from the periapical tissues. ES-BCRR was used as the retrofilling material in all the cases in the present study. The material is biocompatible, nontoxic, nonshrinking, and chemically stable within the biological environment (11, 12). Studies have shown that the material sets at a highly alkaline pH and has antibacterial activity (14, 15). Bioceramics have the advantage of forming hydroxyapatite and ultimately a bond between dentin and filling material (16). All of these characteristics can explain the high level of success when used as a retrofilling material. ES-BCRR comes premixed with an intermediate restorative
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Figure 1. Representative periapical radiographs of cases in each outcome category. (A–C) Example showing complete healing. (A) Preoperative radiograph of case 30. (B) Postoperative radiograph of case 30. (C) Two-year follow-up radiograph of case 30 showing complete resolution of radiolucency and reattachment of periodontal ligament. (D–F) Example showing incomplete healing. (D) Preoperative radiograph of case 19. (E) Postoperative radiograph of case 19. (F) One-year follow-up radiograph of case 19 showing reduced periapical radiolucency. (G–I) Example showing unsatisfactory healing. (G) Preoperative radiograph of case 4. (H) Postoperative radiograph of case 4. (I) One-year follow-up radiograph of case 4 showing persistent periapical radiolucency. (J–L) Example of unsatisfactory healing. (J) Preoperative radiograph of case 3. (K) Postoperative radiograph of case 3. (L) One-year follow-up radiograph of case 3 showing persistent periapical radioluency around the mesiobuccal root.
material–like consistency and therefore is easier to handle (17). Although the popularity of ES-BCRR has grown significantly, the evidence supporting its clinical use as a root-end filling material is still lacking. This retrospective study shows promising results of ES-BCRR used in endodontic microsurgery. The high success rate observed in this study is comparable to that reported when MTA is used as the retrofilling material (1, 2), suggesting ES-BCRR is a viable alternative to MTA as a root-end filling material. Making an accurate preoperative diagnosis and appropriate case selection can influence surgical success. Patient-related and tooth-related factors need to be taken into consideration as important determinants when planning apical surgery against other treatment 4
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alternatives. Von Arx et al (18) published a thorough meta-analysis to assess potential prognostic factors for healing outcome in apical surgery. The outcome was found to be better in those cases without preoperative pain or signs, cases with good density of root canal filling, and cases with absence or size <5 mm of periapical lesion. Potential patient and treatment factors examined in this study included age, sex, tooth position, arch, size of periapical radiolucency, and retreatment previous to surgery. None of these factors were shown to be significant prognostic factors for treatment outcome. Regarding the patient-related factors, our findings are in agreement with the majority of previous studies (18, 19, 22) and suggest that healing after apical surgery does not seem to differ significantly JOE — Volume -, Number -, - 2015
Clinical Research between male and female patients or between younger and older patients. Outcome studies have looked at the success rate of teeth on the basis of tooth position and arch type. A prospective study by Song et al (25) found that tooth position (anterior) and arch type (maxilla) were found to be positive predictors. The maxillary anterior teeth tended to have a higher success rate than the other tooth groups, which they attributed to the relatively easy access and less complicated root anatomy. In the present study, molars had the lowest rate of success (86.5%) compared with premolars and anteriors (96.1%), but no significant difference was found possibly because of the uneven distribution of the number of teeth in different groups. This finding is consistent with 2 other previous reports (26, 27). Our present study showed no difference for healing rates for no lesions or lesions # or > 5 mm, which disagrees with the findings in the meta-analysis by Von Arx et al (18); however, it is in agreement with a number of other studies (3, 28). Larger lesions may be less likely and take longer to heal because of the lower number of progenitor cells present for bone regeneration. The lack of significance found in our present study may be attributed to a relatively small sample size and uneven sample distribution. A sinus tract was present in 17 cases (15%), and only 2 of those cases failed (88.2% success). The presence of a preoperative sinus tract did not significantly influence the success rate. These results agree with another study (3) that found cases with a preoperative sinus tract also had a high success rate of 94.1%. Two studies (19, 29) found that patients who have preoperative signs or symptoms have a significantly lower healing rate. However, patients included in our study who presented with pain at the initial examination were not significantly different in healing rates compared with patients without pain. This may be related to the different patient population and sample size in the different studies. Studies have shown that the success rate for apical surgery improves when orthograde root canal retreatment is combined with apical surgery (30). However, orthograde retreatment is not always a costeffective or realistic option for patients. In the present study, 101 teeth did not have retreatment before apical surgery, and these teeth had a success rate of 93%. Whether nonsurgical retreatment was performed before surgery did not appear to have an influence on the surgical success. In this retrospective study, the diagnosis, treatment planning, and surgical procedures were all performed by the same single operator. Although this may only reflect the clinical judgment and skills of a single endodontist and may not be truly representative, it does represent the scenario of the real-world private practice setting. The results provide important preliminary data that can be used to design future prospective cohort or randomized controlled trials. One limitation of the present study is the radiographic evaluation of treatment outcome. Although preoperative cone-beam computed tomography (CBCT) was performed to assist with surgical treatment planning, it was not routinely used to assess outcome. CBCT has become widely available and is able to detect periapical lesions with higher sensitivity; therefore, success rate determined by conventional radiographs may be overestimated compared with when it is evaluated with CBCT (31). However, the increased cost and radiation exposure need to be justified before CBCT can become a standard tool used for treatment follow-up. In conclusion, the use of ES-BCRR as a root-end filling material resulted in a high healing rate of 92.0% in endodontic microsurgery at a minimum 1-year recall examination. This evidence suggests that ES-BCRR is a suitable root-end filling material to be used in endodontic surgery. Future studies with a larger sample size are needed to confirm JOE — Volume -, Number -, - 2015
the findings and to identify potential prognostic factors that may impact the treatment outcome.
Acknowledgments The authors deny any conflicts of interest related to this study.
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