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Brett E. Gilbert, DDS

Brett E. Gilbert, DDS

Combining clinical excellence and compassion What can you tell us about your background? I was born and raised in Baltimore, Maryland. I attended college, dental school, and my postgraduate endodontic residency at the University...

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Randy Garland, DDS

Randy Garland, DDS

Exceeding expectations What can you tell us about your background?
I grew up in southern Orange County and earned a bachelor’s degree in biology at San Diego State University in 1983. There I met my future wife, Kim, at the...

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Scott A. Norton, DMD, MSD

Scott A. Norton, DMD, MSD

Focus on family, patients, friends, growth, and community What can you tell us about your background? For as long as I can remember, I wanted to make people smile. I always loved getting the class laughing in grade school. Looking back, I am sure...

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Clinical Articles

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Management of a tooth with a large internal resorption defect

Management of a tooth with a large internal resorption defect

Dr. Robert Slosberg facilitates accurate mapping and obturation of the resportive defect with CBCT imaging Abstract
A patient presented with advanced internal root resorption of tooth No. 9. The prominent location of this tooth...

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Pulpal diagnosis of teeth presenting with condensing osteitis prior to endodontic treatment — a retrospective study

Pulpal diagnosis of teeth presenting with condensing osteitis prior to endodontic treatment — a retrospective study

Drs. Brian Shaughnessy, Margaret Jones, Ricardo Caicedo, Joseph Morelli, Stephen Clark, and Ms. Jennifer Osborne review the occurrence of teeth presenting with condensing osteitis and their associated pulpal diagnosis over a 2-year period. Introduction Read More...

GuttaCore® system: a step forward in the evolution of endodontics

GuttaCore® system: a step forward in the evolution of endodontics

Dr. Andrei Zoryan dispels some of the common myths surrounding carrier-based obturation Carrier-based gutta percha Carrier-based obturation (such as Thermafil®, GT® obturator, ProTaper® obturator [Dentsply Tulsa Dental Specialties]) is one...

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Practice Management

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Effortless, fun, and profitable endodontics

Effortless, fun, and profitable endodontics

In part 2 of his series, Dr. Ace Goerig suggests ways to reduce stress in the practice Almost all endodontists could be completely out of debt and on the way to financial freedom within 5 to 7 years if they only knew the secret. But the secret is...

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Life after root canal — it’s not just about having enough money

Life after root canal — it’s not just about having enough money

Dr. Robert Fleisher ruminates on how to prepare for retirement There are so many articles about everything that you become pretty much overwhelmed and can never expect to read them all. So you pick and choose. You like to learn about the latest and...

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Superior customer service

Superior customer service

Dr. Roger Levin presents the 10 top ways to help create a perfect dental team With the changes brought on by the economy, top companies are bringing in the best resources they can find to evaluate where their organizations stand. They want to know...

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Fig.36

Drs. O. Zmener, R. Martinez Lalis, C. Chaves, G.A. Kokubu, D.R. Grana, and C.H. Pameijer present a study to develop and refine procedures for testing the response of the periapical tissues of rats to root canal preparation and obturation



The primary objective of nonsurgical endodontics is to thoroughly clean and shape the root canal space. This is followed by obturation with biocompatible materials to the cemento-dentinal junction, a point located at approximately 0.5-1.0 mm or more from the anatomical apex (Green, 1960). Filling the root canal to this narrowest point creates the best environment for the periapical tissues to heal (Ricucci and Langeland, 1998). Establishing the working length (WL) short or beyond the minor diameter may result in improper instrumentation and obturation of the canal (Farzaneh et al, 2004; Schaeffer et al, 2005).

Testing periapical tissue reactions to endodontic filling materials in humans, although theoretically ideal, presents ethical difficulties. On the other hand, histopathologic information of endodontic treatment failures that require tooth extraction or apical surgery, as well as studies on cadavers (Green et al, 1977), do not meet the requirements of objective prospective testing (Pascon et al, 1991). Therefore, usage tests should be performed in animals to gain valuable information on the tissue response to endodontic materials (Pascon et al, 1991).

Rat molars have historically been used for testing pulp response to experimental procedures (Maurice and Schour, 1955; Paynter and Wood, 1955; Kozlov and Massler, 1960), and have also been proposed as a suitable experimental model for root canal treatment (RCT) (Muruzabal and Erausquin, 1966; Muruzabal et al, 1966; Erausquin et al, 1966; Erausquin and Muruzabal, 1967a; Erausquin and Muruzabal, 1967b; Tepel et al, 1994).

Previous findings (Muruzabal and Erausquin, 1966; Yu and Stashenko, 1987; Akamine et al, 1994; Al Swaimi et al, 2009) have demonstrated that the rat has many similarities to other animal species and humans with respect to the anatomy of periodontal tissues and the periapical inflammatory response. For instance, periapical healing of root canals of rats that had preoperative apical periodontitis and were treated with intracanal medicaments or root canal sealers, have been reported (Tepel et al, 1994). The rat constitutes an inexpensive research model and is easy to handle in a controlled laboratory environment. However, rat molar root anatomy is structurally different from humans. Gomez and Cabrini (2004) reported important anatomic variations in the apical third of the roots after the second month of birth, which become more pronounced as the animal ages. Among these variations is the progressive apposition of large amounts of root cementum at the apical third, and to some extent within the lumen of the canal, as well as an absence of a true apical constriction.

Both deviations complicate the use of this experimental model since it makes the exact location of the real apical foramen difficult (Erausquin and Muruzabal, 1967a; Erausquin and Muruzabal, 1967b; Gomez and Cabrini 2004). As a consequence, it is difficult to accomplish an accurate preparation and obturation of the root canal, frequently leading to inadvertently placing the obturation material short or beyond the apical foramen, and leading to a progressive disuse of the technique.

A careful analysis, leading to identification of the problems and changes in the technique, may lead to improvements using this animal model system. In recent experiments by Martinez Lalis et al (2010a) and Martinez Lalis et al (2010b), some operative improvements were overcome by obtaining a more precise WL. Based on these findings, the aim of this study was to refine the earlier technique described by Erausquin and Muruzabal (1967a) by ensuring that the root canals are adequately prepared and filled to the desired WL. If this goal could be accomplished, experimental endodontic research in rat molars can once more be endorsed.

Materials and methods
The protocol for this research program was approved in 2007 by the Research Ethics Committee of the Argentine DentalScreen_shot_2012-01-06_at_2.28.32_PM Association.

For the experiments, 20 male Wistar rats weighing ±250 g were used. Animal husbandry and handling met the requirements of the ISO 10993-1 (1992) and ISO 10993-2 (1992), as well as the International Regulatory Requirements for the care and use of laboratory animals (Bayne, 1998).

To reduce the number of variables, only rats of the same age with intact healthy teeth were selected, while all operative procedures were done under aseptic conditions.

The animals were anesthetized by intraperitoneal administration of 14 mg/kg body weight of ketamine chloride and 10 mg/kg body weight acepromazine. Positioned on an operating board in a dorsal position and held in place by the maxillary incisors with a customized clamp, the tongue was displaced, keeping the mouth wide open (Figure 1).
Every effort was exercised to keep the molars in a dry state and isolated from contamination with saliva while the crown of the molar was cleaned and disinfected with an antiseptic solution. As per protocol and to standardize the operative procedures, the right mandibular first molar was used for the test material, while the left molar was untreated and used as a negative control.
In this study, the distal root canal of the molars was used. The mesial root canals were not treated nor used for evaluation. Data from earlier experiments (Martinez Lalis et al, 2010a; Martinez Lalis et al, 2010b) showed that the mean length of the distal root of a mandibular first molar in Wistar rats weighing ±250 g was 3.7 mm (range of 3.5-4.0 mm) from the occlusal surface to the tip of the root.

Root canal preparation
Access to the distal canal was gained through the distal half of the occlusal surface using a #1 round carbide bur in an electric handpiece operating at low-speed under constant cooling with sterile saline. After the pulp chamber was exposed, bleeding was arrested with sterile cotton pellets and saline.

Screen_shot_2012-01-06_at_2.28.38_PMOnce the distal canal was visualized, it was instrumented with size #08-10 K-files. Gross pulp tissue was removed, taking care not to overextend the action of the files more than 2.0 mm beyond the floor of the pulp chamber. During these procedures, the canal was profusely irrigated with saline using a #30 gauge needle.

Radiographic determination of the WL is very difficult as, even with a wide-open mouth, the available space is limited and does not permit placement of a small-size periapical film. To solve this problem, the WL was determined with an electronic apex locator (EAL; Apex Finder 7005; Analytic Technology) (Martinez Lalis et al, 2010b). The animals were randomly assigned to two groups of 10 rats each.

Group 1 (n=10)
In this group, the objective was to determine periapical tissue reaction to materials safely placed 0.5-1.0 mm short to the anatomical apex. The lip-clip electrode was applied to one side, and a size #15 or #20 K-file (depending on the individual root) was attached to the probe of the EAL. The file was then advanced apically until the mark that suggests that the tip of the file had reached the anatomical apex of the root. The file was then slowly retracted to the mark that indicates the location of the cemento-dentinal junction (the minor diameter of the canal). If the measurement remained constant for 5 seconds, the data was registered as the safe WL (SWL).

Group 2 (n=10)
In this group, the objective was to determine periapical tissue reaction to overfilled materials. As in group 1, the file was advanced apically into the canal until the tip of the file reached the anatomical apex of the root. If the measurement remained constant for 5 seconds, the data was registered, and the file was then advanced again through the apical foramen until a point located ±1 mm beyond the apex. Data was then registered as the over-extended working length (OWL).

A silicone stopper was positioned at an occlusal reference point. When the measurement remained constant for 5 seconds, the reading was considered the accurate measure for the SWL or OWL. To ensure the reliability of the measurement, this procedure was repeated twice. Once the desired WL was established, the canal was instrumented with progressively larger sized files under constant irrigation with 2.5% NaOCl solution followed by rinsing with sterile saline and thorough aspiration after every change of instrument. The canals were finally dried with fine sterile paper points.

Root canal obturation
The root canals were filled with the material to be tested (not specified here) to the previously determined WL following standard endodontic procedures. The test material was prepared and handled under aseptic conditions and strictly according to the manufacturer’s instructions. After obturation, the access openings were filled with a glass ionomer restorative material (Ionomax; Subiton SA, BA, Argentina).

Screen_shot_2012-01-06_at_2.29.52_PM

After 10 and 60 days, the animals were euthanized with an anesthetic overdose. At the time of euthanasia, the health of the animal and the condition of the coronal restoration were evaluated.

Histological procedures
After euthanasia, the mandibles were dissected and immediately fixed in 10% buffered formalin (pH = 7.4). After 96 hours of fixation, the soft tissues were removed, and a digital radiograph was made using the RadioVisioGraphy (RVG) system (CDR DICOM; Schick Technologies) in order to evaluate the apical limit of the canal obturation (Figure 2).
The mandibles were then decalcified in 10% EDTA, embedded in paraffin, and sectioned in a bucco-lingual direction oriented parallel to the longitudinal axis of the root until the distal canal was visible. Serial sections 7 µm thick were cut and stained with hematoxilyn and eosin (H&E).

Care was taken that the sections of the apical portion of the canal includes material/tissue interface and the surrounding periodontal and bone tissues. To estimate the tissue response in the areas adjacent to the test materials, three sections belonging to the central areas of each specimen were analyzed and photographed at different magnifications with a digital Canon Powershot A510 camera (Canon, Tokyo, Japan), coupled to a stereomicroscope.

Histopathological evaluation criteria
Assessment was made at each observation period with respect to the type of periapical reaction to the tested materials, changes in vessels, the type of cells present, root resorption, and whether an inflammatory reaction was still present over time or if the periapical tissues had returned to  normal. Comparisons were made with the untreated root canals.

Results
At the end of the observation periods, the animals were in good health, and none of them lost their restorative coronal fillings.
Nine animals from the 60-day period showed coronal restorations that had considerable wear on their surfaces. Digital radiographs of the dissected mandibles revealed that, in general, all specimens showed root canals that were prepared and filled to the predetermined lengths.

In group 1, teeth in which the root filling was limited to the SWL initially showed an inflamed pulp stump containing many inflammatory cells (Figures 3A and 3B) whose severity tend to diminish with time while apical closure was not seen in any case, even after 60 days.

In group 2, the periapical tissue reaction in teeth overfilled to the predetermined OWL revealed different degrees of inflammation. In the short-term period, the areas in contact with the overfilled material showed the presence of a granulomatous tissue with the presence of polymorphonuclear leukocytes, lymphocytes, plasmocytes, macrophages, and occasional eosinophils. After 60 days, a fibrogranulomatous tissue containing less proportion of inflammatory cells and newly formed vessels were seen to be surrounded by a thick consistent fibrous connective encapsulation free of inflammatory cells. Some areas of root resorption were additionally seen in the majority of the overfilled teeth (Figure 3C). Comparisons with the negative controls revealed that the untreated teeth had normal pulps as well as healthy periodontal and bone tissues (Figure 3D).

Discussion
Biocompatibility of a root canal filling material has been recognized as one of the most important properties of an endodontic material.

In this study, we analyzed the periapical tissue response to endodontic materials, using the mandibular first molar of the rat as an experimental model. The observations cited above are selected examples that illustrate the results of the experimental procedures.

It should be emphasized that during our research program of experimental endodontics in rats, different filling materials were tested. However, the procedures and the results described here were not meant to analyze a reaction of the periapical tissue to any particular filling material. They merely illustrate the different outcomes that may occur under different experimental conditions and the usefulness of the mandibular first molar of the rat as an animal model for experimental endodontics.

A further objective was to explain how the technique was refined by procedures that produce results that are more reliable and reproducible. For this purpose, ±250 g weight animals were used. Younger animals have incompletely developed apexes, while animals exceeding ±350 g weight have excessive deposition of root cementum at the apex (Gomez and Cabrini, 2004). Using older animals makes it difficult to establish contact between the test material and periapical tissues due to the considerable thickness of cementum. The main difference from earlier investigations (Muruzabal and Erausquin, 1966; Muruzabal et al, 1966; Erausquin et al, 1966; Erausquin and Muruzabal, 1967a; Erausquin and Muruzabal, 1967b) consisted of using the distal, rather than the mesial root canal, as it is easier to access and instrument, thus addressing previously reported difficulties (Erausquin and Muruzabal, 1967a; Erausquin et al, 1966; Martinez Lalis et al, 2010a; Martinez Lalis et al, 2010b).

For irrigation, a 2.5% NaOCl solution was used. NaOCl is widely recognized as one of the most effective irrigating solutions either when used alone or in combination with other chemical solutions (Svec and Harrison, 1977; Baumgartner and Mader, 1987; Siqueira et al, 1997; Siqueira et al, 2000; Carvalho et al, 2008), and it is reported to have no negative effects on the periapical tissues in rats when used in concentrations of 2.5% or 5.0% (Tepel et al, 1994).

Available methods to determine the WL include the use of radiographs, EALs, and tactile sense. While radiographs are still considered necessary to determine the WL in humans (Bernáth and Szabó, 2003), they present many problems in rats, and accurate non-distorted operative radiographs of endodontic procedures are difficult to obtain (Martinez Lalis et al, 2010a; Martinez Lalis et al, 2010b). This was the major reason why, in earlier experiments (Erausquin and Muruzabal, 1967a; Erausquin and Muruzabal, 1967b), root canals were inappropriately prepared and filled as the WL was established by tactile sense only. Consequently, the determination of the limit of instrumentation and obturation of the canals constituted a serious drawback. The use of an EAL has, to the large extent, overcome these problems.

In a preliminary experiment (Martinez Lalis et al, 2010a), the Apex Finder 7005, a self-calibrating instrument, was used strictly according to the manufacturers’ instructions. The main objective was to evaluate the reliability and usefulness of the device to determine the location of a true WL in the rat molar and to determine if it was able to provide reliable information when a file extended beyond the anatomical apex or in cases of root perforation. The results demonstrated that, as in humans (Nahamias et al, 1983; Hembrough et al, 1993), an EAL device provided a valuable and accurate record of the different clinical situations and/or incidents that may have happened during RCT in the rat molar. Warnings were easily noted when the file was located short or beyond the anatomical apex or when it caused an accidental lateral root perforation (Zmener et al, 1999). The latter two are the most frequent incidents that occur during RCT in rats (Muruzabal and Erausquin, 1966; Muruzabal et al, 1966; Erausquin et al, 1966; Erausquin and Muruzabal, 1967b; Erausquin and Muruzabal, 1968; Martinez Lalis et al, 2010a; Martinez Lalis et al, 2010b). As per protocol, only the Apex Finder 7005 was used in our experiments. Therefore, the suitability of other commercially available EALs used for experimental endodontic treatment in rat molars needs to be investigated. These experiments are now in progress.

Conclusion
The suitability of the mandibular first molar in rats in endodontic research has been re-evaluated. The anatomy of the mandibular distal root in Wistar rats weighing ±250 g allows for easy access and canal instrumentation and obturation using current standard procedures.

An EAL for intraoperative procedures was very useful and aided the operator in adequately determining the desired WL. Furthermore, it helped the operator perform better-controlled canal preparation and accurate placement of the obturating material.
The use of an EAL also facilitated the operative procedures, regardless of the amount of root cementum or other variables that complicate working on rat molars (Gomez and Cabrini, 2004).

The technique described here is relatively simple and reproducible, allows evaluation of periapical tissue reaction to instrumentation and intracanal endodontic filling materials, and can be performed in any properly equipped laboratory setting at a low cost.

Acknowledgements
This research program was financially supported by a grant from the Argentine Dental Association, Buenos Aires, República Argentina.

Bios
Osvaldo Zmener, DDS, Dr. Odont, is Head Professor for the Postgraduate Program for Specialized Endodontics at the Faculty of Medical Sciences, School of Dentistry, University of El Salvador, Buenos Aires, Argentina.

Ricardo Martinez Lalis, DDS, Dr. Odont, is Head Professor for the Postgraduate Program for Specialized Endodontics at the Faculty of Medical Sciences, School of Dentistry, University of El Salvador, Buenos Aires, Argentina.

Carolina Chaves, DDS, is Associate Clinical Professor for the Postgraduate Program for Specialized Endodontics at the Faculty of Medical Sciences, School of Dentistry, University of El Salvador, Buenos Aires, Argentina.

Gabriel A. Kokubu, DDS, Dr. Odont, is Head Professor, Department of Oral Pathology, Faculty of Medical Sciences, School of Dentistry, University of El Salvador, Buenos Aires, Argentina.

Daniel R. Grana, DVM, is Assistant Professor, Department of Oral Pathology, Faculty of Medical Sciences, School of Dentistry, University of El Salvador, Buenos Aires, Argentina.

Cornelis H. Pameijer, DMD, MScD, DSc, PhD, is Professor Emeritus, University of Connecticut School of Dental Medicine.

References
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Bernáth M, Szabó J (2003) Tissue reaction initiated by different sealers. Int Endod J 36(4):256-261.

Carvalho AS, Camargo CHR, Valera MC, et al (2008) Smear layer removal by auxiliary chemical substances in biomechanical preparation: a scanning electron microscope study. J Endod 34(11):1396-1400.

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Zmener O, Grimberg F, Banegas G, et al (1999) Detection and measurement of endodontic root perforations using a newly designed apex-locating handpiece. Endod Dent Traumatol 15(4):181-185.

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