I Apexification Healing Patterns Comparing MTA & Bioceramic Putty

Apexification Healing Patterns Comparing MTA & Bioceramic Putty

Thesis

Presented in Partial Fulfillment of the Requirements for the Degree Master of

Science in the Graduate School of The Ohio State University

Adam H. Richardson, DDS

Graduate Program in Dentistry

The Ohio State University

2020

Thesis Committee

Ashok Kumar, BDS, MS, Advisor

Kumar Subramanian, DDS, MS

Ehsan Azadani, DDS, MS

Dennis McTigue, DDS, MS

Jin Peng, MD, MS, PhD

Copyrighted by

Adam H. Richardson, DDS

2020

Abstract

Purpose: The purpose was to compare radiographic healing patterns and clinical outcomes in teeth treated with apexification using Bioceramic Putty (EndoSequence

Bioceramic BC RRM-Fast Set Putty) and Mineral Trioxide Aggregate (ProRoot MTA) by clinical exam and CBCT after at least a year post-treatment.

Methods: Subjects were identified with a retrospective search of Epic Clarity Databse

(Epic Systems, Verona WI, USA) for ADA code for apexification. The inclusion criteria were as follows: (1) Patients age 6-18 with immature permanent incisor root with apexification treatment completed at least one year prior on maxillary anterior teeth or mandibular anterior teeth using either MTA or BC-RRM as a root-end closure material.

(2) At least one year of follow up exam including CBCT imaging. (3) Apexogenesis was not indicated. (4) A history of radiographs (traditional periapical imaging or CBCT) taken prior to treatment of apexification. (5) Adequate cooperation for in-office treatment. Patients returned for recall no less than one year after treatment to complete a clinical exam and a CBCT. Clinical factors evaluated include: tenderness to percussion, tenderness to palpation, percussive tone, color, mobility, and presence/absence of swelling or sinus tract. Four calibrated examiners evaluated radiographic factors. The radiographic factors included: PDL, Lamina Dura, periapical radiolucency (3D), apical anatomy, stage of root development at time of treatment, apexification plug position, and calcific apical bridge.

Results: 15 patients with 16 teeth met the inclusion criteria. Five teeth demonstrated a periapical lesion, 2 teeth from the MTA group and 3 teeth from the BC-RRM group. The

clinical success rates were 85.7% and 100% for MTA and BC-RRM respectively. The radiographic success rates were 57.1% and 66.7% for MTA and BC-RRM respectively.

Conclusions: There was no significant difference in outcomes of apexification when

MTA and BC-RRM putty were used as root-end filing materials. Both materials demonstrated successful outcomes in the short term with restoration of function and esthetics. Furthermore, tooth retention with no symptoms also improves psychological well-being

Dedication

This document is dedicated to my mother and father for their constant support to keep

moving forward, and to my research advisors for their guidance and expertise.

iii

Acknowledgements

I would like to thank my thesis committee for their support and guidance throughout my

project, as well as during my education. I would also like to thank my co-residents for

their consistent documentation.

Vita

May 2010………………………………………………………….Claremore High School

May 2014………………………...... ……………….BS Zoology, University of Oklahoma

May 2018………………………………….……………….DDS, University of Oklahoma

2018 to present…………………………………Resident, Division of Pediatric Dentistry

The Ohio State University and Nationwide Children’s Hospital

Fields of Study

Major Field: Dentistry

Table of Contents

Abstract………………………………………………………………………….…………i Dedication…………………………………………………………………………...……iii Acknowledgments……………………………………………………………………..…iv Vita……………………………………………………………………………...…………v List of Tables……………………………………………………………….……………vii List of Figures………………………………...…………………………………………viii Introduction………………………………………………….……………….……………1 Materials and Methods………………………………………………………………….....6 Results……………………………………………………………………………………13 Discussion…………………………………………………………………………..……19 Conclusion…………………………………………………………….…………………25 Bibliography………………………………………………………………………..……26

List of Tables

Table 1 Gender and Race Demographic Data.………………………………….………..12 Table 2 Associations Between Material Used for Apexification and Clinical Outcomes.16 Table 3 Associations Between Material Used for Apexification and Radiographic Outcome………………………………………………………………….………17

vii

List of Figures

Figure 1 Moorree’s Classification of Root Development.……………………....…….…11 Figure 2 Age Distribution………………………………………………….….....………13 Figure 3 Distribution of Teeth Based on Moorree’s Tooth Development Scale..….……14 Figure 4 Distribution of Periodontal Injury……………………………………..…….…15 Figure 5 Distribution of Pulpal Injury…………………………………………..……….15

viii

Introduction

Dental trauma in the pediatric population leads to a multitude of functional and esthetic problems with possible psychological impact during the lifetime of the individual. Following a traumatic event, healing patterns are highly variable depending on the severity of the trauma, age of the child and host response. One such outcome with traumatized teeth in children is involvement of the pulp with necrotic degeneration of the neurovascular bundle, necessitating endodontic therapy. The treatment options are predicated on the stage of root development. If endodontic therapy is necessary in a tooth with immature root development, apexogenesis or apexification is indicated.

Apexogenesis is the development and formation of a root end; frequently used to describe vital pulp therapy performed to encourage the continuation of this process1,2,3 ;while apexification is a method to induce a calcified barrier to form at the apical end of the root.

Apexification is a procedure indicated for non-vital immature teeth that require root canal treatment. Apexification is usually done in teeth that exhibit moderate maturation of the root with an open apex or if regenerative endodontics is unsuccessful or contraindicated1. Historically, calcium hydroxide (CaOH) was one of the most widely used materials for apexification4,5,6,7. This material has a long history of success; however, evident drawbacks in the material have caused its usage to fall out of favor in recent years. To induce the formation of a calcific barrier with calcium hydroxide, multiple visits are required and the material must also be changed periodically6.

Additionally, the formation of the apical barrier can take several months, leading to issues with patient compliance. Though not well substantiated, there is also evidence suggesting increased possibility of tooth fracture when CaOH is used. In support of this

finding the tooth may be weakened by prolonged exposure to CaOH decreasing intrinsic properties of exposed dentin. Furthermore, tooth stability may be compromised during subsequent access of the tooth to change CaOH, and between CaOH, as only a temporary coronal restoration is present4,5. Many studies demonstrate mineral trioxide aggregate

(MTA) is a suitable material for apexification6,8,9,10,11,12. Damale et al. found the formation of an apical barrier occurs faster, on average, when using MTA vs. CaOH as a root-end closing material4. In support of this evidence, another study confirmed these findings by demonstrating apical bridge formation in 3 months with MTA in comparison to 7 months for CaOH7. The process of changing the CaOH requires the operator to re- access the tooth, thus increasing the risk of contamination each time the tooth is exposed and sealed 6,7. Furthermore, weakening of the tooth structure can occur with each subsequent access6,11. For these reasons, new materials are currently being utilized and researched for apexification.

Bioceramic materials are often the material of choice for endodontics.

Bioceramics are bioinert, bioactive, and biodegradable, soluble or resorbable. Bioinert materials are non-interactive with biologic systems and bioactive materials are durable in tissues and can undergo beneficial interactions with surrounding tissues. Examples of bioceramic materials in endodontics are MTA, bioceramic root repair material putty, and

Biodentine23.

MTA is biocompatible, induces formation of hard tissue, and has properties similar to CaOH such as a high pH and antibacterial action13. In a head to head comparison of the two materials, similar success rates were observed when analysis of clinical and radiographic success was completed4,5,7. One advantage that MTA has over

calcium hydroxide is the shortened length of treatment and reduced need for multiple applications of the material. This reduces the burden on the patient and decreases the risk of contamination during the re-access of the affected tooth11. Nevertheless, MTA has notable drawbacks including difficult handling characteristics and a long setting time.

11,14,15. Multiple studies also demonstrate the discoloration potential of the clinical crown when MTA is used as an apexification material16,17. Kohli et al. demonstrated significantly increased incidence of discoloration when using grey and white MTA compared to other bio ceramic materials on the market, and proposed the inclusion of heavy metals in MTA for its discoloration26.

Biodentine is another example of a bioceramic that has been used successfully for apexification. Biodentine is composed of Tricalcium silicate, calcium carbonate, zirconium oxide, and a water-based liquid-containing calcium chloride as the setting accelerator. This average set time is 10-12 minutes and the material has a pH of 11.7 after one day34. Vidal et al demonstrated successful apical closure using Biodentine in a 9 year old patient who suffered a traumatic injury to a maxillary central. At 18 months the patient retained his traumatized tooth, was asymptomatic, and evaluation of CBCT demonstrated PDL health, absence of any periapical pathology, and a calcific bridge apical to the Biodentine plug36. Sharma et al have also demonstrated the success of

Biodentine as an apexification material in a case series37.

Recently, a material called Bio Ceramic Root Repair Material Fast Set (BC-RRM)

Putty has been used successfully in many endodontic procedures. BC-RRM is composed of Tricalcium silicate, zirconium oxide, dicalcium silicate, calcium sulfate, and tantalum pentoxide15,23,24. This material has been shown anecdotally to have superior handling

properties compared to MTA14. Sarris et al. speculate clinical success in root end closure procedures to be positively linked to optimal placement of the apical plug12.

Extrapolating this finding leads to the hypothesis that clinical success is enhanced with improved handling properties of apical plug material. BC-RRM and MTA have been shown to have similar success rates14, 28. Safi et al. found no difference in success rates when comparing MTA and EndoSequence root repair material (RRM), a material similar to BC-RRM, demonstrating success rates of 94.7% and 92% respectively25. In a retrospective study, Shinbori et Al. identified 113 teeth in 94 individuals that had endodontic microsurgery using EndoSequence BC root repair putty as a root-end filling material, a material nearly identical to BC-RRM. Their findings demonstrated an overall success rate of 92%28. BC-RRM has additionally shown comparable sealing ability when compared to MTA; utilizing a novel bacterial leakage model, Antunes et al. found no difference in sealing ability between MTA and BC-RRM14. However, further research is necessary to determine the sealing ability of bioceramics in endodontics, as there exists some conflicting evidence in the literature. Letmalapong et al. found leakage in 93% of

BC-RRM samples after 28 days18. Another material advantage is decreased potential for crown discoloration26.

Nevertheless, there is a gap in knowledge regarding the success of BC-RRM for apexification procedures in human models when evaluated at least one year after completion of treatment. This study aims to compare radiographic healing patterns and clinical outcomes in teeth treated with apexification using Bioceramic Root Repair

Material Fast Set (BC-RRM) putty and Mineral Trioxide Aggregate by clinical exam and

3-dimensional CBCT after at least one year post-treatment. The data were analyzed to

identify prognostic predictors of success. The null hypothesis was that there was no significant difference in the healing patterns of apexification for MTA or BC-RRM putty.

Materials and Methods

Study Design and Ethics:

A retrospective analysis study was conducted to evaluate the healing patterns of teeth treated with apexification using MTA or Bioceramic Root Repair Material Fast Set

(BC-RRM) putty. The study protocol was approved by the ethics committee of the

Institutional Review Board of Nationwide Children’s Hospital (IRB-00000404). Patients’ charts were identified using a search in the hospitals EMR system (Epic) for all patients treated with apexification at Nationwide Children’s Hospital Dental Clinic (NCH).

Subjects were enrolled in the study after a follow up examination was complete at least one year after the procedure.

Subject Enrollment and Inclusion/Exclusion Criteria

The sample comprised of patients presenting to the Nationwide Children’s Dental

Clinic for treatment of traumatized permanent incisors. A Retrospective search of the

Epic system using the ADA code “3353 Apexification/Recalcification – Final visit” identified 66 charts. These 66 patients were contacted via phone up to three times to schedule a follow up visit if they had not been seen at least one year after apexification.

In order to increase the sample size, samples were also identified in a similar manner from Central Ohio Root Canals, a private endodontic practice.

Patients’ charts were reviewed and evaluated for inclusion in the study. The inclusion criteria were as follows: (1) Patients age 6-18 with immature permanent incisor root with apexification treatment completed at least one year prior on maxillary anterior teeth or mandibular anterior teeth using either MTA or BC-RRM as a root-end closure

material. (2) At least one year of follow up exam including CBCT imaging. (3) A history of radiographs (traditional periapical imaging or CBCT) taken prior to treatment of apexification. (4) Adequate cooperation for in-office treatment.

The exclusion criteria were defined as follows: (1) inadequate cooperation for procedure. (2) No follow up after one year. (3) Apexification on a posterior tooth. (4)

Apexogenesis was indicated.

Of the 66, subjects, 15 subjects demonstrated the appropriate inclusion criteria, 14 subjects from NCH and 1 subject from Central Ohio Endodontics.

Surgical Procedure and Material

The patients who met the study criteria had treatment completed by a pediatric dental resident and an endodontist. One patient’s treatment was rendered soley by the endodontist. The same endodontist oversaw all the procedures and performed the placement of the MTA or BC-RRM. All treatment was completed in a similar manner as outlined below. After determination that patients required an apexification procedure, subjects were seen for a pulpectomy. The patients were anesthetized with either 2% lidocaine (1:100,000 epi) and/or 4% articaine (1:100,000 epi) and a rubber dam was placed. The tooth was accessed and remaining pulp tissue removed with hand instrumentation. The tooth was irrigated with 5-6% sodium hypochlorite and dried with paper points. A working length was then determined. The treated tooth was then filled with calcium hydroxide (ApexCal) and sealed with a cotton pellet and triage (glass ionomer). Patients were then asked to follow up for completion of apexification.

At the second visit patients were evaluated for pain and persistent infection with a clinical and radiographic exam prior to apexification. The clinical exam evaluated percussion and palpation sensitivity, tooth mobility, and presence or absence of a sinus tract. If the patient was asymptomatic and radiographic examination revealed no increase in periapical lesion size, then the apexification procedure was initiated. The tooth was re- accessed by a pediatric dental resident and irrigated with 5-6% sodium hypochlorite. The tooth was then dried with paper points. An endodontist then proceeded with the apexification procedure using an endodontic microscope (most commonly: 12x & 17x).

The use of BC-RRM putty or MTA was randomly determined by the endodontist. Either

MTA or BC-RRM putty was placed at the apex at a minimum of 3mm thickness. A periapical radiograph was then utilized to determine adequate placement of the apexification plug. The remaining canal was then filled to the cementoenamel junction with a Calamus backfill technique or filled with BC-RRM putty. The pediatric dental resident then completed the procedure by placing vitrebond over obturation material and a final packable composite. In 14 cases sodium perborate was then placed prior to final restoration in coronal access due to discoloration. Patients who received a bleaching agent were asked to return in two weeks to remove bleach and place final restoration.

Follow-up Procedure

Patients returned at least one year following the completion of apexification for a clinical and radiographic exam. The clinical exam assessed the following: tenderness to percussion, tenderness to palpation, tooth mobility, pain with biting, presence or absence of sinus tract, occlusal trauma, fracture since initial, discoloration.

After the clinical exam, a limited field CBCT was taken of the affected tooth. The

CBCTs were obtained with a Planmeca ProMax® 3D Mid (Planmeca, Illinois, US). The operating parameters were set at 10mA and 90kV, and the exposure time was 15 s. Voxel size was 150 µm. From the CBCT image series, the following factors were assessed:

1. Apical Calcific Bridge – Measured as present or absent. Note: if partial bridge

was appreciated, item measured as absent.

2. Periodontal ligament (PDL) – measured as normal or abnormal. Abnormal PDL

included any areas with widened PDL or absence of PDL.

3. Lamina Dura (LD) – measured as present or absent.

4. Periapical lesion – measured as present or absent

5. Apical plug adaptation – measured as “well adapted” or “not well adapted.” This

measurement was recorded at 3 levels by analyzing coronal slices of the CBCT

series: 1mm from apex, 2 mm from apex, and 3mm from apex.

o This measurement was gathered by utilizing the multiplanar tool in

Romexis® to align the long axis of the tooth to the Y-axis in the software,

which has pre-measured increments of 1mm on axis display.

o These measurements were selected to identify the adaptation of the apical

plug to the dentinal walls and to identify any voids in the material. These

depths were based on the findings by Valois et al. who demonstrated 4mm

of apical plug material was significantly more effective than 1mm, 2mm,

and 3mm in preventing apical leakage38.

A panel of experts consisting of four separate examiners gathered the above data from the CBCT. The panel included three board-certified pediatric dentists and one endodontist. Examiners were blinded to the material used, date of treatment, and patient name for each imaging series. The CBCT series were randomized prior to viewing. Each examiner had access to the entire CBCT series including the anterior posterior slices, sagittal slices, and coronal slices. Imaging was viewed and manipulated on the CBCT software Romexis®. Imaging was viewed on one monitor by the four examiners simultaneously with consistent lighting. All examiners were calibrated using two cases to reduce inter-examiner discrepancies. Nevertheless, discrepancies in ratings were resolved through discussion between examiners and consensus was reached for each case.

Additional information gathered at a later time by the primary investigators from the CBCT includes: (1) Apex diameter measurement - recorded in millimeters in the buccal-lingual and the mesial-distal dimension. (2) Apical plug position – recorded in millimeters short of or past apex. Recorded as “0” if flush with apex. This data was objectively measured using the ruler utility in Romexis®.

Additionally, to increase inter-examiner consistency, examiners were shown a single pre-operative periapical radiograph of each tooth in the study and were asked to assign a Moorree’s score (1-6) to each tooth. The Moorree’s score is used to determine the stage of tooth development (fig. 1)1,2,. Discrepancies in ratings were resolved through discussion between examiners and consensus was reached for each case.

Figure 1 Moorree’s Classification of Root Development

For cases where a lesion was noted as “present,” the pre-operative PA radiograph and an anterior-posterior slice from the corresponding CBCT series was shown to each examiner to be ranked as one of the follow: lesion decreased in size, lesion same size, lesion increased in size.

Demographic and clinical assessments recorded in the trauma flow sheets prior to apexification within the Epic system were collected. The following parameters were recorded for each patient fitting the inclusion criteria:

1. Gender

2. Language

3. Race

4. Ethnicity

5. Primary dental insurance

6. Age

7. Date of injury

8. Tooth injured

9. Periodontal injury

10. Pulpal injury 11

11. Displacement (mm) if intrusion, luxation, or extrusion injury

12. Date of apexification

13. Apexification material

14. Date of follow up exam

Results

Table 1 lists the demographic information of the sample population including patient sex and race. The mean patient age at time of apexification was 12. The mean time to follow up was 3 years. Figure 2 illustrates the distribution of age within the population, while figure 3 illustrates the distribution of tooth development utilizing

Moorree’s classification of root development.

Table 1 Gender and Race Demographic Data

Age Distribution

7 6 5 4 3 2 1 0

Figure 2 Age Distribution

Moorree's Tooth Development Distribution

0 Three Four Five

Figure 3 Distribution of Teeth Based on Moorree’s Tooth Development Scale

A total of 66 patients were identified as having apexification completed at either

NCH or Central Ohio Root Canals. Fifty-one patients were lost to follow up, leaving 15 patients with 16 teeth included in the study population.

Figures 3 and 4 include the distribution of periodontal injuries and pulpal injury, respectively, sustained during the initial trauma. Categories included in periodontal injury include: concussion, subluxation, lateral luxation, intrusion, extrusion, and avulsion. Two teeth included in the sample were avulsed and 1 was intruded representing more severe injuries. One tooth did not have injury type recorded in the chart. Categories included in pulpal injury included no coronal fracture, Class II fracture, and Class III fracture.

Periodontal Injury Avulsion Concussion Intrusion 13% 13% 6% Extrusion 6%

Lateral Luxation 12% Subluxation 50%

Figure 4 Distribution of Periodontal Injury

Class II Pulpal Injury Fracture 7%

No Fracture 33% Class I Fracture 60%

Figure 5 Distribution of Pulpal Injury

Table 2 lists the percentages of teeth in each group that reported the following findings: tenderness to palpation, tenderness to percussion, mobility, pain with biting, presence or absence of sinus tract, occlusal trauma, fracture noted after initial trauma, and discoloration. The following groups were analyzed using Pearson’s Chi-Squared test 15

(Table 2) and no statistical significance was found between groups. Associated with palpation, sinus tract, fracture noted after initial trauma and discoloration and the following p-values were derived from a Chi Square statistical analysis: 0.44, 0.41, 0.44, and 0.11.

Table 2 Association Between Material Used for Apexification and Clinical Outcomes

Table 3 illustrates the teeth in each group with the following findings: presence or absence of apical calcific bridge, plug adaptation (1mm), plug adaptation (2mm), plug adaptation (3mm), normal or abnormal periodontal ligament, normal or abnormal lamina dura, presence or absence of periapical lesion, and plug position. These were also analyzed using Pearson’s Chi-Square test. All groups demonstrated no statistical difference between the two materials. 3 out of 7 teeth treated with MTA and 3 out of 9

teeth treated with BC-RRM had abnormal PDL. 2 out of 7 teeth treated with MTA and 3 out of 9 teeth treated with BC-RRM had a periapical lesion present.

Table 3 Associations Between Material Used for Apexification and Radiographic

Outcome

Five teeth demonstrated a periapical lesion, 2 teeth from the MTA group and 3 teeth from the BC-RRM. Out of the 5 teeth with periapical lesions 4 teeth demonstrated no change in lesion size, while 1 tooth exhibited increase in lesion size. This tooth was from the MTA group. The overall clinical success rate was 85.7 and 100% for MTA and

BC-RRM respectively. The overall radiographic success rate was 57.1% and 66.7% respectively.

Discussion

The primary purpose of this study was to evaluate healing patterns of teeth treated with apexification using MTA and Bio Ceramic Root Repair Material Fast Set (BC-

RRM) Putty. Apexification is a procedure with a high clinical success rate when MTA is used. Many studies mark the success rate of apexification between 85% -94%4,5,6,9,12.

Similar success rates have been verified when a bioceramic root end filling material is used. To reinforce this finding, Safi et al. found a success rate of 92% when evaluated radiographically34. Adding to this finding, Zhou et al. demonstrated success rates of 93% when iRoot BP plus was used for apexification, a material chemically similar to BC-

RRM putty 35. The current study demonstrated success rates by the following criteria: [1] absence of symptoms; [2] healing or no change in apical pathology; [ 3] healing of sinus tract (if present preoperatively); [4] normal periodontal ligament; [5] normal lamina dura.

The success rates from this study were based on the strict criteria established by

Strindberg. The success rate based on the criteria listed demonstrated a success rate of

57% and 66% for MTA and BC-RRM putty respectively. These success rates should be interpreted carefully. Three teeth in the MTA group and 3 in the BC-RRM group demonstrated abnormal PDL. As only one tooth out of the 6 was clinically unsuccessful, the presence of abnormal PDL could be attributed to an apical scar. It should also be noted that change in lesion progression was measured by comparing a pre operative PA radiograph to the post-operative CBCT. Such comparison was difficult, as CBCT is more sensitive in the detection of anatomic structures, particularly changes in bone. This was a drawback of the study.

The success of bioceramics and MTA for apexification can be drawn from their chemical and physical properties. MTA is a calcium silicate-based, biocompatible, bioactive material. It has a high pH, which yields antibacterial properties, is both cementoconductive and cementoinductive, and has the ability to expand10,11,14. The average setting time of MTA is 165 minutes. This material also demonstrates an initial pH of 10.5 and this gradually rises to 12.5 resulting from constant calcium ion release; this likely yields the material’s antibacterial action34. MTA induces the formation of a hydroxyapatite layer between the MTA and the dentinal walls. This formation is likely responsible for the superior sealing abilities seen with MTA11.

Similar to MTA, BC-RRM is another calcium-silicate based material. The manufacturer lists the components of BC-RRM as Tricalcium silicate, zirconium oxide, tantalum pentoxide, dicalcium silicate, and calcium sulfate. This material is also bioactive, stimulating hard tissue formation and even a bond between the dentin and the apexification material14,28,33. The average set time of BC-RRM is around 3-4 hours, but only 20 min with the fast set mix 34. An advantage to this material is its ease of use. BC-

RRM comes premixed with a consistency similar to an intermediate restorative material, making placement less technique sensitive than MTA. The current study analyzed the position of the apical plug at three levels from the apex: 1mm, 2mm and 3mm. With a p- value of 1, 1 and 0.49, respectively, there was no significant difference in adaptation between MTA and BC-RRM. This finding aids in illustrating the usefulness of both materials as a root-end filling material, as very few measurements of “not well adapted” were reported, but does not confirm reported increases in handling properties of BC-

RRM.

Other studies have analyzed the marginal adaptation of bioceramics in endodontics18,32. In one study conducted by Dennis Tran et al. marginal adaptation of

ProRoot MTA, Neo MTA Plus, BC-RRM fast set putty, and BC-RRM fast set putty was compared in extracted roots. Each root was prepared to resemble an open apex and a 6 mm plug was placed. Each sample was then sectioned 3mm from the apex and viewed using a scanning electron microscope. No significant difference was found between the 4 groups in the quality of marginal adaptation at the level of the anatomical apex. However, when gap distance was measured between the material-dentin interface BC-RRM fast set putty with BC Sealer demonstrated a statistically significantly smaller gap size compared to the other materials tested32.

One major drawback of the current study was sample size. A total of 66 patients were identified as having apexification completed at NCH and Central Ohio Root Canals.

Of these subjects, 16 met the inclusion criteria and were thus enrolled in the study. A significant proportion of these patients had their procedure completed prior to 2017. Care should be taken to emphasize importance of follow up examinations to patients and families in the future.

An additional drawback was variation in operators for procedures other than apexification. The population was largely sampled from a postgraduate pediatric training program; different residents often completed different portions of the procedure, such as the initial pulpectomy. Because the access, pulpectomy, and subsequent access seal were portions of the procedure completed by the resident and not the endodontist, suboptimal technique could have let to the high incidence of discoloration found in the present study.

This finding disagrees with other studies indicating a low discoloration rate of BC-RRM

16,17,27. In a color change comparison Alsubait et al. detected progressive discoloration with ProRoot MTA when placed coronally in human extracted teeth. The study also demonstrated color stability (no change in color) when BC-RRM fast set putty was used.

The authors propose the discoloration of ProRoot MTA is due to dissociation of the added radiopacifying agent bismuth oxide. When exposed to like this compound breaks down into metallic bismuth causing discoloration16. The current study found no difference in discoloration between MTA and BC-RRM (table 2). It is likely that suboptimal technique rather than material was the cause of discoloration. Attention to complete removal of pulpal tissue, thorough irrigation and better access seal is recommended to decrease discoloration.

Another drawback was the utilization of pre-operative periapical radiographs to compare CBCT imaging in determining change in lesion size and assess healing. 5 out of

16 teeth had a periapical lesion when viewed on CBCT. Of these 5 teeth, only 1 tooth had an increase in lesion size, while 4 teeth had no change. CBCT is becoming the standard of care when analyzing healing patterns of teeth, as the tooth can be viewed in three dimensions. This allows minute changes in the periodontal ligament and lamina dura to be apparent to the viewer when those findings may be masked in a traditional two-dimensional radiograph25. In teeth diagnosed with pulpal necrosis, Abella et al. found a statistically larger number of periapical radiolucencies when compared to PA radiographs, illustrating the increased precision of the CBCT20,25. This finding also illustrates the presence of false negatives in PA radiographs, which could ultimately change treatment planning.

As no baseline CBCT was taken for these patients, there was difficulty drawing conclusions from these comparisons. However, healing of these teeth was analyzed not only radiographically, but also clinically. In the current study, 85% and 100% of teeth were clinically successful when treated with MTA and BC-RRM putty respectively.

Radiographically, the current study found success rates of 57% and 66% with MTA and

BC-RRM putty respectively. Safi et al reported a difference of 25% in healing when looking at the same tooth using CBCT verse a traditional PA25. This may account for some discrepancy in healing outcomes clinically versus radiographically.

Overall, MTA and BC-RRM demonstrated similar healing patterns when utilized as a root-end filling material. In the MTA group, 4 out of 7 teeth demonstrated apical calcific bridge formation, while 4 out of 9 teeth in the BC-RRM group demonstrated bridge formation. In the current study, both materials produced similar clinical and radiographic success rates. Despite having a radiographic success rate of 66%, all subjects in the BC-RRM group reported no symptoms, while 85% of the MTA group was symptom free. The clinic success is extremely important for function, but the contribution to esthetics should not be overlooked. Allowing these patients to retain maxillary anterior teeth secondary to trauma has a great effect on the psychological well-being of the child.

Despite the drawbacks previously outlined, the current study helps set the foundation for future prospective studies on this topic. The strengths of the present study are blinded examiners to type of root end-filling material, time of follow up, and the utilization of an expert panel to review the CBCTs; the expert panel consisted of three board certified pediatric dentists and one endodontist. An additional strength was that all

apexification procedures were performed by a single operator utilizing an endodontic microscope, thus reducing any treatment-related variables that may affect outcomes.

Identification of parameters essential for prospective trials was also gained during this study. Pre-operative and immediate post-operative CBCT imagining would be beneficial for diagnostic precision and for healing comparison. Capturing CBCT images eliminates the chance for superimposition of anatomical structures and is more useful than PA radiographs at assessing cancellous bone20,25,35,39. To support these findings, Patel et al extracted distal roots of 6 molars from cadaver mandibles and prepared synthetic periapical lesions, then re-implanted the distal roots. Images were then taken of the mandibles with traditional PA radiography and CBCT with various size periapical lesions. The authors found correctly identified periapical lesions in 24.8% and 100% of cases using traditional PAs and CBCT respectively39.

Conclusion

In this retrospective healing analysis, there was no significant difference in outcomes of apexification when MTA and BC-RRM putty were used as root-end filling materials. The overall success rate was 57% and 66% for MTA and BC-RRM. Both materials demonstrated successful outcomes in the short term with restoration of function and esthetics. Furthermore, tooth retention with no symptoms also improves psychological well-being

Bibliography

[1] S. Shabahang, Treatment options: apexogenesis and apexification, Pediatr Dent 35(2) (2013) 125-8.

[2] N. Shah, A. Logani, U. Bhaskar, V. Aggarwal, Efficacy of revascularization to induce apexification/apexogensis in infected, nonvital, immature teeth: a pilot clinical study, J Endod 34(8) (2008) 919-25; Discussion 1157.

[3] Huang GT. A paradigm shift in endodontic management of immature teeth: conservation of stem cells for regeneration. J Dent. 2008;36(6):379‐386.

[4] S.G. Damle, H. Bhattal, D. Damle, A. Dhindsa, A. Loomba, S. Singla, Clinical and radiographic assessment of mineral trioxide aggregate and calcium hydroxide as apexification agents in traumatized young permanent anterior teeth: A comparative study, Dent Res J (Isfahan) 13(3) (2016) 284-91.

[5] S.G. Damle, H. Bhattal, A. Loomba, Apexification of anterior teeth: a comparative evaluation of mineral trioxide aggregate and calcium hydroxide paste, J Clin Pediatr Dent 36(3) (2012) 263-8.

[6] D.T. Holden, S.A. Schwartz, T.C. Kirkpatrick, W.G. Schindler, Clinical outcomes of artificial root-end barriers with mineral trioxide aggregate in teeth with immature apices, J Endod 34(7) (2008) 812-7.

[7] D.P. Pradhan, H.S. Chawla, K. Gauba, A. Goyal, Comparative evaluation of endodontic management of teeth with unformed apices with mineral trioxide aggregate and calcium hydroxide, J Dent Child (Chic) 73(2) (2006) 79-85.

[8] S. Küçükkaya Eren, P. Parashos, Adaptation of mineral trioxide aggregate to dentine walls compared with other root-end filling materials: A systematic review, Aust Endod J 45(1) (2019) 111-121.

[9] R. Pace, V. Giuliani, M. Nieri, L. Di Nasso, G. Pagavino, Mineral trioxide aggregate as apical plug in teeth with necrotic pulp and immature apices: a 10-year case series, J Endod 40(8) (2014) 1250-4.

[10] M. Parirokh, M. Torabinejad, Mineral trioxide aggregate: a comprehensive literature review--Part I: chemical, physical, and antibacterial properties, J Endod 36(1) (2010) 16-27.

[11] M. Parirokh, M. Torabinejad, Mineral trioxide aggregate: a comprehensive literature review--Part III: Clinical applications, drawbacks, and mechanism of action, J Endod 36(3) (2010) 400-13. 26

[12] S. Sarris, J.F. Tahmassebi, M.S. Duggal, I.A. Cross, A clinical evaluation of mineral trioxide aggregate for root-end closure of non-vital immature permanent incisors in children-a pilot study, Dent Traumatol 24(1) (2008) 79-85.

[13] M. Rafter, Apexification: a review, Dent Traumatol 21(1) (2005) 1-8.

[14] H.S. Antunes, L.F. Gominho, C.V. Andrade-Junior, N. Dessaune-Neto, F.R. Alves, I.N. Rôças, J.F. Siqueira, Sealing ability of two root-end filling materials in a bacterial nutrient leakage model, Int Endod J 49(10) (2016) 960-5.

[15] M.L. Porter, A. Bertó, C.M. Primus, I. Watanabe, Physical and chemical properties of new-generation endodontic materials, J Endod 36(3) (2010) 524-8.

[16] S. Alsubait, S. Al-Haidar, N. Al-Sharyan, A Comparison of the Discoloration Potential for EndoSequence Bioceramic Root Repair Material Fast Set Putty and ProRoot MTA in Human Teeth: An In Vitro Study, J Esthet Restor Dent 29(1) (2017) 59-67.

[17] J. Bosenbecker, F.J. Barbon, N. de Souza Ferreira, R.D. Morgental, N. Boscato, Tooth discoloration caused by endodontic treatment: A cross-sectional study, J Esthet Restor Dent (2020).

[18] P. Lertmalapong, J. Jantarat, R.L. Srisatjaluk, C. Komoltri, Bacterial leakage and marginal adaptation of various bioceramics as apical plug in open apex model, J Investig Clin Dent 10(1) (2019) e12371.

[19] C. Papadopoulou, M. Georgopoulou, I. Karoussis, K. Kyriakidou, T. Papadopoulos, In vitro Evaluation of Biocompatibility and Cytotoxicity of Total Fill Bioceramic Root Repair material putty for endodontic use, British Journal of Medical and Health Research, 2020.

[20] F. Abella, S. Patel, F. Durán-Sindreu, M. Mercadé, R. Bueno, M. Roig, An evaluation of the periapical status of teeth with necrotic pulps using periapical radiography and cone-beam computed tomography, Int Endod J 47(4) (2014) 387-96.

[21] C.L. Chen, T.H. Huang, S.J. Ding, M.Y. Shie, C.T. Kao, Comparison of calcium and silicate cement and mineral trioxide aggregate biologic effects and bone markers expression in MG63 cells, J Endod 35(5) (2009) 682-5.

[22] E.A. Chybowski, G.N. Glickman, Y. Patel, A. Fleury, E. Solomon, J. He, Clinical Outcome of Non-Surgical Root Canal Treatment Using a Single-cone Technique with Endosequence Bioceramic Sealer: A Retrospective Analysis, J Endod 44(6) (2018) 941- 945.

[23] G. Debelian, DMD, PhD, M. Trope, DMD, The use of premixed bioceramic materials in endodontics, Society Italiana di Endodonzia, Endodonzia, 2016, pp. 70-80.

[24] C.S. Hirschberg, N.S. Patel, L.M. Patel, D.E. Kadouri, G.R. Hartwell, Comparison of sealing ability of MTA and EndoSequence Bioceramic Root Repair Material: a bacterial leakage study, Quintessence Int 44(5) (2013) e157-62.

[25] C. Safi, M.R. Kohli, S.I. Kratchman, F.C. Setzer, B. Karabucak, Outcome of Endodontic Microsurgery Using Mineral Trioxide Aggregate or Root Repair Material as Root-end Filling Material: A Randomized Controlled Trial with Cone-beam Computed Tomographic Evaluation, J Endod 45(7) (2019) 831-839.

[26] M.R. Kohli, M. Yamaguchi, F.C. Setzer, B. Karabucak, Spectrophotometric Analysis of Coronal Tooth Discoloration Induced by Various Bioceramic Cements and Other Endodontic Materials, J Endod 41(11) (2015) 1862-6.

[27] G. Krastl, N. Allgayer, P. Lenherr, A. Filippi, P. Taneja, R. Weiger, Tooth discoloration induced by endodontic materials: a literature review, Dent Traumatol 29(1) (2013) 2-7.

[28] N. Shinbori, A.M. Grama, Y. Patel, K. Woodmansey, J. He, Clinical outcome of endodontic microsurgery that uses EndoSequence BC root repair material as the root-end filling material, J Endod 41(5) (2015) 607-12.

[29] V. Srinivasan, P. Waterhouse, J. Whitworth, Mineral trioxide aggregate in paediatric dentistry, Int J Paediatr Dent 19(1) (2009) 34-47.

[30] M. Torabinejad, M. Parirokh, Mineral trioxide aggregate: a comprehensive literature review--part II: leakage and biocompatibility investigations, J Endod 36(2) (2010) 190-202.

[31] M. Torabinejad, M. Parirokh, P.M.H. Dummer, Mineral trioxide aggregate and other bioactive endodontic cements: an updated overview - part II: other clinical applications and complications, Int Endod J 51(3) (2018) 284-317.

[32] D. Tran, J. He, G.N. Glickman, K.F. Woodmansey, Comparative Analysis of Calcium Silicate-based Root Filling Materials Using an Open Apex Model, J Endod 42(4) (2016) 654-8.

[33] A. Washio, T. Morotomi, S. Yoshii, C. Kitamura, Bioactive Glass-Based Endodontic Sealer as a Promising Root Canal Filling Material without Semisolid Core Materials, Materials (Basel) 12(23) (2019).

[34] Z. Wang, Bioceramic materials in endodontics, Endodontic Topics 32 (2015) 3-30.

[35] W. Zhou, Q. Zheng, X. Tan, D. Song, L. Zhang, D. Huang, Comparison of Mineral Trioxide Aggregate and iRoot BP Plus Root Repair Material as Root-end Filling Materials in Endodontic Microsurgery: A Prospective Randomized Controlled Study, J Endod 43(1) (2017) 1-6.

[36] K. Vidal, G. Martin, O. Lozano, M. Salas, J. Trigueros, G. Aguilar, Apical Closure in Apexification: A Review and Case Report of Apexification Treatment of an Immature Permanent Tooth with Biodentine, J Endod 42(5) (2016) 730-4.

[37] S. Sharma, V. Sharma, D. Passi, D. Srivastava, S. Grover, S.R. Dutta, Large Periapical or Cystic Lesions in Association with Roots Having Open Apices Managed Nonsurgically Using 1-step Apexification Based on Platelet-rich Fibrin Matrix and Biodentine Apical Barrier: A Case Series, J Endod 44(1) (2018) 179-185.

[38] C.R. Valois, E.D. Costa, Influence of the thickness of mineral trioxide aggregate on sealing ability of root-end fillings in vitro, Oral Surg Oral Med Oral Pathol Oral Radiol Endod 97(1) (2004) 108-11.

[39] S. Patel, A. Dawood, F. Mannocci, R. Wilson, T. Pitt Ford, Detection of periapical bone defects in human jaws using cone beam computed tomography and intraoral radiography, Int Endod J 42(6) (2009) 507-15.