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PERIAPICAL MICROSURGERY: A 4-D ANALYSIS OF HEALING PATTERNS

Daniel Crossen

A thesis submitted to the faculty at the University of North Carolina at Chapel Hill in partial fulfillment of the requirements for the degree of Master of Science in the School

of Dentistry (Endodontics).

Chapel Hill 2018

Approved By:

Peter Z Tawil

Thiago Morelli

(2)
(3)

ABSTRACT

Daniel Crossen: Periapical Microsurgery: A 4-D Analysis of Healing Patterns (Under the direction of Peter Tawil)

This study analyzed the volumetric healing pattern of the buccal plate after

periapical microsurgery over time, with focus on the bucco-lingual thickness of bone

and the regression of the surface contour of the cortical plate. Twelve surgical sites

were analyzed in vivo at least one year following periapical. Volumetric healing was analyzed by converting pre-operative and post-operative CBCT images into digital

3-Dimensional models; then registering the models to be able to analyze the changes in

volume over time. Analysis was completed using the software “GeoMagic,” which

allowed for registration of the volumes, calculation of volume change, and a calculation

of the margin of error. Results showed the reduction of bucco-lingual thickness and the

regression of the cortical plate to be within the margin of error in all cases. It is

therefore concluded that periapical microsurgery does not cause thinning of the

(4)

ACKNOWLEDGEMENTS

This research was supported by a grant from the AAE Foundation for

Endodontics. It was also supported by the 2016-2017 Dr Shizuko Yamauchi

Endodontics Graduate Student Award, given by the Yamauchi family and the Dental

Foundation of North Carolina, INC.

Thesis Mentor: Dr. Peter Z. Tawil

Thesis Advisor: Dr. Thiago Morelli

Thesis Advisor: Dr. Donald Tyndall

UNC Dept of Endodontics: Dr. Ashraf Fouad, Donna Perdue, Cindy Hynes, Neldy

Pagan

ITK-SNAP software: http://www.itksnap.org

GeoMagic Software: https://www.3dsystems.com/software

(5)

TABLE OF CONTENTS

List of Tables . . . vii

List of Figures . . . viii

List of Pictures . . . ix

Thesis Introduction . . . 1

References . . . 3

Review of Literature . . . 4

i: Periapical Microsurgery a: History . . . 4

b: Microsurgical Technique . . . 6

c: Indications . . . 8

d: Tissue Considerations . . . 10

e: Traditional Outcome Measurements/Criteria . . . 12

f: Gap of Knowledge . . . 13

ii: CBCT a: Development and Implementation of CBCT in the Dental Office . . . 14

b: CBCT use in the evaluation of healing after periapical microsurgery . . . 16

c: CBCT as used in this study . . . 17

iii: 3-D Software a: ITK-SNAP and Conversion to .STL . . . 18

b: Geomagic . . . 19

(6)

Formatted Sections for the Journal of Endodontics

i: Introduction . . . 26

ii: Materials and Methods . . . 28

iii: Results . . . 31

iv: Discussion . . . 34

v: Conclusion . . . 35

References . . . 37

Thesis Conclusion . . . 41

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LIST OF TABLES

(8)

LIST OF FIGURES

Figure 1 - Boxplot of the volume change of the buccal cortical plate . . . 33

Figure 2 - Graphic representation of the volume change in mm3 compared

to the average error in mm . . . 34

Figure 3 - Graphic representation of the time elapsed between periapical

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LIST OF PICTURES

Picture 1 - Screenshot of a pre-operative .STL file after segmentation using ITK-SNAP . . . 42

Picture 2 - Screenshot of .STL after being imported into “GeoMagic” . . . 43

Picture 3 - Screenshot of a post-op .STL file after segmentation using ITK-SNAP . . . 44

Picture 4 - Screenshot of post-operative .STL after importation into “GeoMagic.” . . . 45

Picture 5 - Screenshot of color map from “GeoMagic” showing changes

in surface contour between pre-operative and post-operative .STL volumes . . . 46

Picture 6 - Cross-sectional image from “GeoMagic” . . . 47

Picture 7 - Selection of area of interest using “GeoMagic” . . . 48

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THESIS INTRODUCTION

Endodontics has been defined as the diagnosis, prevention, and treatment of

apical periodontitis. Non-surgical root canal treatment, often referred to as “getting a

root canal,” is often the first line of treatment for apical periodontitis if the tooth is to be

retained. When infection persists or returns, further treatment is warranted (1). This

further treatment is divided into two categories: non-surgical root canal retreatment, and

apical surgery. Modern surgical techniques and materials are referred to as “periapical

microsurgery” (2). While the ability of the periapex to heal following non-surgical

removal of microbes has been demonstrated since Kakehashi, Stanley, and

Fitzgerald’s seminal article in 1965 (3), the healing of the periapex following apical

surgery has not been as well studied.

Although studies have consistently shown healing to occur following apical

surgery, they have focused simply on the reduction of the apical lesion and

regeneration of the lamina dura (4-7), or, in some of the cone-beam computed

tomography (CBCT) studies, the Hounsfield units of the periapical area (8). Even then,

the sample population sizes have been small enough to render the power of the study

too small to achieve statistical significance in many of their findings. To date no study

has analyzed the volumetric patterns of healing, including their effects on the cortical

plate and bucco-lingual ridge thickness. Until recently, this would have been

(11)

counterparts (9), and without surgical re-entry, there was no way to analyze healing in vivo. However, modern CBCT now allows us to examine hard tissue changes in vivo utilizing a non-invasive approach (10). By measuring the volume and bucco-lingual

thickness of healed bone, clinicians will have the knowledge of whether grafting is

prudent at the time of periapical microsurgery in order to prevent later grafting requiring

surgical re-intervention should implants be necessary at a future date.

The aim of this study was to evaluate the volumetric healing of hard tissue over

time after periapical microsurgery; with specific focus on the bucco-lingual thickness of

bone and the surface contour of the cortical plate. The study converted CBCT images

into 3-D models using the software, “ITK-SNAP” (11), and then overlaid, or registered

the models made prior to surgery with those made 1-5 years after surgery, and

calculated the changes in bone volume using the software “Geomagic.” Analysis was

(12)

REFERENCES

1. Friedman S. Considerations and concepts of case selection in the management of post‐treatment endodontic disease (treatment failure). Endodontic Topics. 2002;1:54-78. 2. Tawil P, Saraiya V, Galicia J, Duggan D. Periapical Microsurgery: The Effect of Root

Dentinal Defects on Short- and Long-term Outcome. JOURNAL OF ENDODONTICS. 2015;41:22-27.

3. KAKEHASHI, S., STANLEY, H., & FITZGERALD, R. (1965). Effects of surgical exposures of dental pulps in germ-free and conventional laboratory rats. Oral Surgery Oral Medicine Oral Pathology Oral Radiology and Endodontology, 20(3), 340-340.

4. Lingaraj JB, Kotrashetti SM, Gupta N. Healing assessment of osseous defects of periapical lesions with use of freeze dried bone allograft. Journal of Maxillofacial and Oral Surgery. 2009;8:362-365.

5. Tanomaru-FIlho M, Jorge ÉG, Guerreiro-Tanomaru JM, Reis JMS, Spin-Neto R, Gonçalves M. Two- and tridimensional analysis of periapical repair after endodontic surgery. Clinical Oral Investigations. 2015;2014;19:17-25.

6. Rud, J., Andreasen, J.O., Mo¨ ller Jensen, J.E., 1972. Radiographic criteria for the assessment of healing after endodontic surgery. Int. J. Oral Surg. 1, 195–214.

7. Molven, O., Halse, A., Grung, B., 1987. Observer strategy and the radiographic

classification of healing after endodontic surgery. Int. J. Oral Maxillofac. Surg. 16, 432– 439.

8. Kaya S, Yavuz I, Uysal I, Akku Z. Measuring bone density in healing periapical lesions by using cone beam computed tomography: A clinical investigation. Journal of

Endodontics. 2012;38:28-31.

9. Ford TRP. The radiographic detection of periapical lesions in dogs. Oral Surgery, Oral Medicine, Oral Pathology. 1984;57:662-667.

10. Peters CI, Peters OA. Cone beam computed tomography and other imaging techniques in the determination of periapical healing. Endodontic Topics. 2012;26:57-75.

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REVIEW OF LITERATURE

i: Periapical Microsurgery

a: History

Periapical microsurgery is integral to the practice of a modern endodontist (1). A

longitudinal cohort study in Florida showed that 13% of the population has received

endodontic treatment of some form, and that 3% of those procedures were surgical in

nature. So while surgical endodontic treatment may seem rare, as less than one half of

one percent of the population has had an apical surgery (2), the total number of

endodontic surgeries per year in the US alone is approximately 300,000, which affects

quite a substantial number of individuals (3). The same survey showed that less than

5% of all surgical endodontic procedures are completed by general dentists, while over

70% of non-surgical endodontic procedures are performed by general dentists. A

survey of practicing endodontists showed that surgical procedures make up 7.2% of all

treatments in the modern endodontic practice (4). As such, surgical procedures are

integral to the practicing endodontist both in establishing a rapport of specialist-level

knowledge and skill, as well as to the financial well-being of a practice.

Surgical endodontic procedures are first mentioned in the literature at the

beginning of the 20th century. As early as 1903, (5) and also in 1906 (6) a technique was described for surgically removing the “roughened” (resorbed) root end and

(14)

surface and filling using burs. This later came to be known as an “apicoectomy,” or

literally the removal of the apex of the root. Schamberg’s detailed description of the

procedure included packing the surgical site with iodoform or carbolated gauze, and

having the patient return for multiple visits until granulation tissue was no longer present

at the site. Only after this was complete did Schamberg advocate obturation (filling) of

the canal. Later, Hartzell advocated complete disinfection and obturation of the canal

prior to surgery (7,8). Hartzell’s techniques were considerably less time-consuming

than prior techniques, and as such were more likely to become widely used among

practitioners at the time. Hartzell claimed a failure rate of less than 7% in cases

completed this way.

At the time, it was already well-known that the apical seal of gutta percha and

eugenol-based sealer was not optimal. As such, within a decade, efforts were made to

replace the apical obturation material with amalgam, in the hopes that the apical seal

could be improved and leakage would decrease. Lucas outlined this retro-preparation

and retro-fill using amalgam in a series of articles from 1916-1919 (9,10,11). Following

resection of the root tip, this was completed by using a small round bur to remove the

apical gutta percha and to create retention for the amalgam, then placing, condensing,

and burnishing the amalgam into the preparation. In the same series, Lucas also

described what later came to be known as the “pack and whack” procedure. For

mandibular anterior teeth, he recommended that the teeth be obturated with copper

amalgam prior to surgery. Then during surgery, there was no need for a

retro-preparation and retro-fill, but only the apicoectomy. During the next few decades, there

(15)

and outlined repeatedly. For example, the use of a bevel was adopted to allow for

better visualization and easier preparation. While Hartzell had reported success rates in

excess of 90%, reviews in the literature showed the long-term success of these

techniques to be closer to 60% (12). Most practitioners recognized this lower success

rate, inferior to that of non-surgical endodontic retreatment. Combined with the

increased invasiveness, recovery time, and esthetic concerns of apical surgery when

compared to surgical retreatment, apicoectomy was not nearly as common as

non-surgical retreatment. This trend continues today (3) even though the success rate of

modern surgical treatment is considerably higher (12,13), especially in certain scenarios

that will be further explained later (14).

b: Microsurgical Technique

In the 1990’s, significant advances were made that considerably changed the

way endodontic surgery was done (15). The advent of the Dental Operating

Microscope allowed for greater magnification and direct light delivery to the surgical site.

This in turn led to the ability to visualize and access the periapical area without the need

for large flaps or large osteotomies (13). Using the dental operating microscope in

combination with transillumination, even the dentinal defects and microcracks present at

the periapex are able to be visualized (16). This increased ability to illuminate and

magnify the surgical site, combined with the ability to visualize the periapical area and

structures therein, have prompted some authors to state that the use of the dental

operating microscope is a must when performing periapical microsurgery, and all

(16)

Ultrasonic handpieces allow for a root end preparation without the use of rotary

handpieces and burs. Traditional rotary instrumentation precludes the instrument from

having bends in the shank, as the entire shank must rotate. Without the necessary

rotation of traditional burs, ultrasonic handpieces are able to be designed in such a

manner so as to fit around the various anatomical impediments, and prepare deep into

the canal without the removal of large amounts of circumferential dentin. In addition,

the manufacturer is able to place a bend near the tip of the ultrasonic instrument, which

allows for the instrument to be used in a smaller osteotomy, and on a flat root-end

surface (18). These techniques, combined with the use of proper direct vision or

micro-mirrors, allow for root-end preparation without the need for a large osteotomy or large

bevel. Smaller bevels decrease the amount of exposed dentinal tubules, which

decreases the chance of leakage into the system (13,19).

Another important aspect of the modern microsurgical technique is the use of a

biocompatible root-end obturation material. In 1990, Dorn and Gartner showed that the

use of IRM or SuperEBA as a root-end filling material resulted in a significant

improvement in 10-year outcomes when compared to amalgam (20). The advent of

Mineral Trioxide Aggregate (MTA) showed extreme promise in histological studies, with

cementum formation on the remaining root surface and even directly on the MTA in the

area of the root-end filling (21,22,23). Today, various materials are used, including

Bioceramics, MTA, SuperEBA, and IRM. Various studies have shown no significant

difference of the long-term clinical outcome between these materials (24,25). However,

histologic studies in animals have shown improved healing after surgery with the use of

(17)

number of inflammatory cells present in the periapex of a tooth treated with MTA is

clinically relevant. While one human outcome study did show improved outcome with

the use of MTA over SuperEBA and IRM (28), the choice of retrofilling material was not

randomized, decreasing the level of evidence supported by the study.

In combination, the widespread use of a dental operating microscope, ultrasonic

root-end preparation, and obturation with newer root-end filling materials has greatly

increased the long-term outlook for surgical root canal treatment (15). While traditional

apicoectomy success rates were seen at 45-60%, the modern technique has shown

long-term success rates in excess of 90% (12,13).

c: Indications

While success rates are influenced by myriad factors, primary non-surgical root

canal therapy generally has a long-term overall success rate of approximately 90% (29).

For the other 10% of cases, a decision must be made as to how to treat the tooth to

best eliminate the existing cause of pathology, as well as to prevent apical periodontitis

from recurring in the future. Generally, there are three options for a tooth with apical

periodontitis that has already undergone endodontic therapy: non-surgical retreatment,

surgical endodontic treatment, or extraction of the tooth in question.

While extraction of the offending tooth is a sure way to eliminate apical

periodontitis, replacing the dentition is a difficult and expensive process, with long-term

survival rates similar to those of endodontic treatment (30). The similar survival rate,

combined with the increased expense of implant replacement therapy, make implant

replacement the least cost-effective of the three options when dealing with apical

(18)

Non-surgical root canal retreatment is the most common method for dealing with

apical periodontitis in teeth with prior endodontic treatment (3). Statistically, the success

rate of non-surgical retreatment is significantly lower than that of primary root canal

treatment (29), and is lower than that of surgical endodontic treatment (25). Yet

non-surgical retreatment continues to be the modality of choice for revision of previously

treated teeth. This is due to myriad factors, and is often based on subjective decisions

rather than knowledge of the literature and comparable success rates of the

procedures. Typically, the provider faced with the decision to treat surgically or

non-surgically has no knowledge of the treatment details of the original root canal treatment.

While radiographically, the obturation may appear adequate, if improper aseptic

technique was used, bacterial contamination may have been present throughout the

entire procedure. Furthermore, the correct cleaning and sealing of fins, accessory

canals, and isthmuses cannot be assured if knowledge of prior treatment is not

available. Finally, patient preference often comes into play. Non-surgical root canal

retreatment is something patients feel comfortable with, as they have already

undergone non-surgical primary root canal treatment. However, periapical microsurgery

is still a surgery, and many patients prefer to avoid surgery, if possible (32).

With the advances to periapical microsurgery over the past three decades, the

success rates of periapical microsurgery are greatly improved compared to the success

rates of traditional apicoectomy (33,34). In fact, periapical microsurgery success rates

now exceed those of non-surgical retreatment (25), especially in cases where the

natural anatomy of the root canal system has been significantly altered during

(19)

periapical microsurgery has a much more predictable outcome. In addition, if a cyst is

suspected, the ability of non-surgical retreatment to resolve the cyst is questionable,

and periapical microsurgery once again has a much more predictable outcome (35).

The use of longer ultrasonic tips allows for deeper root end preparations and fillings,

even up to 9mm, which is generally the length of the entire canal following resection,

rendering the argument of needing non-surgical retreatment initially to cleanse the

canal system a moot point. As such, in these scenarios, and possibly in others, the

prudent clinician may see periapical microsurgery as a preferable alternative to

non-surgical retreatment; both in regards to a predictable outcome, and in long-term cost to

the patient (15,31).

d: Tissue Considerations

A better understanding of the biological processes that guide healing will lead to

a better understanding of the procedure, and ways that it may be further improved. For

both surgical and non-surgical root canal therapy, the goal is healing of the periapical

tissues, including the bone surrounding the root tip. Often, prior to treatment, these

tissues have been severely damaged, with bone replaced by granulation tissue.

Surgical treatment removes the inflamed tissue, but also often removes some of the

healthy bone surrounding the affected area, potentially complicating the natural healing

mechanisms needed to produce a healthy cortical plate and adequate bone volume

(36-39). While studies have shown that healing occurs after surgery, and that the

cortical plate is usually restored, the volumetric healing, especially concerning the

bucco-lingual thickness of bone and the surface contour of the cortical plate, has not

(20)

bucco-lingual thickness of bone to a point where the periodontal support is

compromised for the tooth in question, or even the adjacent teeth. It is also unknown if

a change in the contour of the cortical plate occurs which may compromise future

implant placement if needed in the surgical site or adjacent sites. Such knowledge is

paramount when treatment planning surgical cases; especially cases where the

prognosis may be less than favorable.

Following extraction of teeth, ridge preservation by means of bone grafting and

sometimes barrier placement has become commonplace, showing clear benefits in the

literature (40). Grafting is seen as necessary to maintain adequate bone thickness for

future implant placement (40). Yet in the realm of surgical root canal treatment, bone

grafting is not common at all, and the effects on outcome remain unclear (41, 42).

Some give the argument that bone grafting would raise the cost of treatment, making

the procedure less attractive, as it is often regarded as a cost-saving measure when

compared to implant replacement strategies. Yet the cost difference is not extensive,

and surgical therapy would still cost significantly less for the patient, especially in areas

involving a prosthesis with multiple units (31). If surgical root canal therapy is being

performed as a “last resort” to save the tooth, then the necessity of grafting to facilitate

future implant placement should be a prominent concern in the mind of the prudent

clinician. Lin argues that the periapex is very different from the cervical periodontium,

and grafting may not aid in restoring the periodontal ligament or the cementum (42).

However, both PDL and cementum are present in the periodontium, and grafting has

been shown in the periodontal literature to have a high success rate. Lin also states

(21)

he concedes that there is a paucity of controlled studies to compare the types or sizes

of lesions, or if there are any factors which would precipitate a need for guided tissue

regeneration (42). In 2013, Song et al established that an apico-marginal defect is one

of these situations, and that there is a significant benefit from using guided tissue

regeneration following apical surgery in these cases (43). In these studies, the

outcome measured was resolution of the periapical radiolucency, not maintenance of

bone volume. It is possible that a discrepancy still exists.

e: Traditional Outcome Measurements/Criteria

The methods and criteria for evaluating outcomes of surgical endodontic therapy

evolved with the procedure. In 1972, Jorgen Rud proposed a system of classifying

periapical healing after endodontic surgery that is still widely in use today (44). The

system looks at the change in the periapical radiolucency at the surgical site over time.

In short, elimination of the periapical radiolucency is classified as “complete healing”; a

persistent periapical radiolucency without symptoms, particularly when lamina dura is

visible around the apex, is classified as “incomplete healing” or scar formation;

“uncertain healing” is the classification for a periapical radiolucency that has decreased

in size, yet still persists; and “unsatisfactory healing” is the term given when no

regeneration of bone or lamina dura has occurred, or when symptoms persist.

Another system to evaluate apical periodontitis is the periapical index (PAI),

developed by Dag Orstavik in 1986. Unlike Rud’s system, the periapical index is not

specific to surgical treatment. But the ordinal scale developed by Orstavik has been

shown to have excellent inter-observer reliability, and has been suggested as the

(22)

primarily due to the fact that the subjectivity of diagnosis is reduced by the more

well-defined criteria present in the PAI scale, as well as the ability of evaluators to be blinded

while using the technique (45).

In both of the above systems, healing is assessed using 2-dimensional

radiography. Unfortunately, the surgical site is not 2-dimensional, and traditional

radiography does not give a full understanding of healing at the surgical site. In fact, for

a periapical radiolucency to be visible in 2-dimensional radiography, the cortical plate

must be perforated (46). As such, if there is persistent inflammation around the

periapex, but not extensive enough to perforate the cortical plate, this may persist totally

unknown to the provider. It can also be difficult when using 2-dimensional radiography

to differentiate between overlapping structures, evaluate missed canals that

approximate each other closely, or visualize iatrogenic error in a bucco-lingual

dimension. As such, a new system was proposed to evaluate healing in 3-dimensions

using cone-beam computed tomography (CBCT). In this system, healing of the

resection plane, periapex, and cortical plate is assessed via the different 2-D slices of

the CBCT volume (47).

f: Gap of Knowledge

Using traditional radiography, the 3-dimensional healing pattern of the surgical

site was impossible to visualize in vivo, and thus not completely understood. Even

more recent studies using modern 3-dimensional radiography have only focused on the

elimination of the periapical radiolucency, the regeneration of PDL and lamina dura, and

the reformation of the cortical plate. These signs are an indication of a reduction in

(23)

However, to date no studies have focused on the area around the lesion. Little to

nothing is known about the mechanisms or patterns by which the cortical plate heals. It

is possible that even when the cortical plate regenerates, it regenerates with a

significant narrow defect. It is also possible that while the cortical plate regenerates

within the lesion, there is a loss of bucco-lingual thickness around the lesion.

ii: CBCT

a: Development and Implementation of CBCT in the Dental Office

Until recently, 3-dimensional analysis of healing following surgical endodontic

treatment was impossible without surgical re-entry. While 3-dimensional imaging has

been available in medicine since the invention of computed tomography in 1972, the

technology was too expensive to be economically feasible in dentistry. Ironically, the

earliest machines for computed tomography were designed for evaluation of the head

only (49) although the resolutions of the early scanners were far too low for endodontic

applications. The method of acquiring a CT image went through changes over the

subsequent decades. First, fan-beam computed tomography allowed for more efficient

scanning by allowing multiple detectors to operate simultaneously. This is the method

still currently used for medical CT imaging. The advent of cone-beam computed

tomography (CBCT) in 1998 allowed for 3-dimensional imaging of a limited field at a

greatly reduced cost and radiation dose compared to the previously established

fan-beam computed tomography (50).

To give more details, medical CT imaging is accomplished using a fan-shaped

x-ray beam that makes progressive helical rotations around the subject with the radiation

(24)

are stacked together to simulate a 3-dimensional object. Using the narrow fan-shaped

beam source, each slice is a separate scan, requiring many rotations around the

subject. Cone-beam CT, on the other hand, acquires images using a round collimated

x-ray source, with the x-rays diverging from the source in a cone-shaped fashion

towards the sensor. By so doing, the need for multiple rotations is eliminated, and the

entire process can be completed with a single rotation of 180 or 360 degrees (51).

Thus, the advantages of CBCT over traditional fan-beam CT imaging are a reduction in

radiation dose, a reduction in time required to record the image, and a reduction in cost.

The disadvantages of CBCT are the decreased ability to analyze soft tissue, and the

increase in scatter radiation (52) and, at times, patient motion.

During the 1990’s, the placement of dental implants for tooth replacement

became much more common, and the demand for 3-dimensional dental imaging in the

dental office grew considerably. The reduced cost of CBCT machines allowed for the

implementation of 3-dimensional radiography in the dental office (49). These CBCT

units soon became popular for their applications in the field of endodontics. The ability

of 3-dimensional radiography to aid in the diagnosis and detection of abnormal

anatomy, internal and external resorption, missed canals (53,54,55), perforations,

separated instruments, transported canals, the extent of periapical radiolucency, and

the proximity of anatomical structures (56), has led the American Association of

Endodontists to issue a position statement to clarify that clinicians should consider a

limited-field CBCT “should be considered the imaging modality of choice for diagnosis in

patients who present with contradictory or nonspecific clinical signs and symptoms

(25)

imaging modality of choice for presurgical treatment planning to localize root

apex/apices and to evaluate the proximity to adjacent anatomical structures.” (57)

b: CBCT Use in the Evaluation of Healing after Periapical Microsurgery

Until very recently, there has been a paucity of research involving evaluation of

healing following periapical microsurgery using CBCT. This is likely due to the

established healing indices using 2-dimensional radiography being well established and

in use for decades (44,45). While CBCT has a much higher sensitivity for detecting

periapical radiolucencies compared to periapical radiographs when compared to

histopathological findings as the gold standard (58,59), some providers noted that

CBCT often appears to demonstrate a small periapical radiolucency in teeth that seem

to be otherwise healthy, and even in teeth with vital pulps. More recent research has

shown that while this does occur, these radiolucencies tend to be smaller than 1-2mm in

diameter, and that a radiolucency larger than 2mm in diameter is indeed indicative of

periapical pathology (60). It has been shown that while dental students and residents

may disagree on the presence or absence of periapical radiolucency on CBCT,

experienced clinicians have a much higher inter-observer reliability. While there may

always be error, additional training will help to reduce this error (61).

Recently, a method of evaluating the healing of the periapical radiolucency in

three dimensions was proposed (47). Using multiple indices, this method measures the

healing in two dimensions around the periapex, the surgical entry point, and the cortical

plate. By combining the indices, a general picture of the three-dimensional healing can

be inductively reasoned. The study also showed the inter-observer reliability of CBCT

(26)

post-surgery. However, no volumetric analysis of healing was completed in this or other

studies, nor is there currently any method of evaluating the surgical site healing in a

volumetric fashion.

To date, CBCT research on healing following periapical microsurgery has been

focused on patient-focused outcomes, ignoring the possible effects on related structures

and possible future sequelae. The elimination of periapical radiolucency and

reformation of the cortical plate may correlate well with a reduction in symptoms (48),

but they do not show volumetric changes of the bone and supporting structures. The

use of CBCT for this purpose is the most prudent option currently available. Its use and

reliability are established (47); it has been shown to be as accurate as surgical re-entry

and direct visualization in most situations (62), and it is a non-invasive approach (63)

with relatively low radiation risk (64).

c: CBCT as Used in This Study

In this study, all radiographic volumes were made using cone-beam computed

tomography. This method was chosen for the advantages mentioned earlier; mainly

the decrease in radiation, decrease in time required for image acquisition, and a

reduction in cost. With one exception (Participant #06), all volumes were made using

the Kodak 9000 3D® (Carestream Dental, Stuttgart, Germany). The Kodak 9000 3D®

was chosen for its high resolution in limited field imaging, with a relatively low radiation

dose required to produce the image as compared to other models (64,65). The

average CBCT volume to evaluate apical surgery from the Kodak 9000 is equivalent to

approximately 4 bitewings, or regular dental x-rays (64,66). This is the same amount of

(27)

radiation as a person receives during a 90-minute plane flight (67). When considering

the low radiation from modern CBCT units with limited field in combination with the

added diagnostic ability they provide, it is scientifically reasonable that studies

recommend CBCT over traditional PA evaluation for post-op evaluation. (63,68).

The volumes for participant #06 were made using the Orthophos XG 3D®

(Sirona, Bensheim, Germany). In this case, the pre-operative volume had been made

using the Orthophos XG 3D®, and in order to achieve proper registration, the

post-operative volume needed to be made on the same machine.

Although the effective radiation dose using the Kodak 9000 3D® is relatively low,

equivalent to only 1-5 days of background radiation (64), all efforts were made to protect

vulnerable populations. As such, participants were excluded from the study if they were

pregnant at the follow-up examination, or if they were undergoing radiation therapy.

iii: 3-D Software

a: ITK-SNAP and Conversion to .STL

As stated before, CBCT machines do not create 3-dimensional models of the

subject they have captured. What they create is a series of 2-dimensional images, or

slices. Specifically, in the case of the Kodak 9000 3D®, a series of 470 2-dimensional

images are created. In order for two volumes to be registered, they must first be

converted into 3-dimensional models.

To accomplish this task in this study, the volumes were exported in

uncompressed DICOM format. The DICOM volumes were then processed using the

software “ITK-SNAP” and the areas of interest converted into .STL files, which are true

(28)

was developed specifically for this purpose (69) and has been used for segmentation in

previous publications in the orthodontic literature (70). Segmentation using ITK-SNAP

works by manually selecting a 3-dimensional portion of the volume, setting a grey-level

threshold to eliminate scatter, selecting several points within the selection to guide the

segmentation, and allowing the software to essentially “connect the dots.” By selecting

multiple points, one is assured that the segmentation will not include structures that are

not connected to the main structure being analyzed, such as the opposing arch, or

distant scatter from metal objects. Once the segmentation has been completed, the

object is exported in .STL format, a format commonly used in 3-D modeling and 3-D

printing. (See picture 1, picture 3 in appendix.) While the Kodak 9000 3D® saves

images in 32-bit format, the maximum grayscale ITK-SNAP is able to process is 16-bit.

This was not seen as an issue when creating .STL files, as after segmentation is

complete, the object has essentially 1-bit of depth, meaning the grayscale has been

erased and the object has been completely defined.

b: Geomagic

Once the volumes were converted into .STL format, the software “GeoMagic”

was used to register, or overlay the volumes similarly to subtraction radiography, and

analyze the changes. (See picture 2, picture 4 in appendix.) Once registration was

completed, a color map of the registered images was created to show the changes in

surface contour between pre-operative and post-operative volumes. (See picture 5 in

appendix.) Cross-sectional images were also created to measure the change in

bucco-lingual thickness. (See picture 6 in appendix.) To calculate the volume change in the

(29)

the calculations. (See picture 7 in appendix.) While GeoMagic is marketed directly to

the medical field for applications such as this (71), the software is new enough that to

(30)

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FORMATTED SECTIONS FOR THE JOURNAL OF ENDODONTICS

i. Introduction

Surgical endodontic treatment is an integral part of the modern endodontic

practice (1,2). Over 300,000 surgical endodontic procedures are completed annually in

the United States alone (3). While apical surgery has been practiced for over 100 years

(4,5,6,7), advances in the 1990’s changed the way the procedure was done (8), giving

rise to the term “periapical microsurgery” (9). These changes include use of the dental

operating microscope (8,10,11), the advent of ultrasonic root-end preparation, the

corresponding decrease in the need for bevel preparation (10,12,13), and the use of

biocompatible root-end fillings, rather than amalgam as used traditionally (14,15,16).

Using these new techniques, the success rate of surgical endodontic therapy went from

45-60% with traditional apicoectomy to over 90% with periapical microsurgery (10,17).

It has been established in the literature that at a histological level the periapical

tissues, cortical plate, and gingiva experience a rapid healing following periapical

microsurgery (20,21,22). As a histological evaluation following surgery is not

appropriate, outcomes following periapical microsurgery are most often measured using

the criteria developed by Jens Rud in 1972 (18) or the periapical index proposed by

Orstavik in 1986 (19). These systems utilize 2-dimensional imaging to analyze the

healing of the periapex. As such, they are limited in their ability to diagnose the

(36)

quantify the volumetric changes to hard tissues in and adjacent to the surgical site.

Thus, to date outcome studies have focused on the presence or absence of healing

(9,10,15-19), and the reformation of the cortical plate (23), and not on the volumetric

healing and corresponding site maintenance.

Site maintenance is an important consideration when performing periapical

microsurgery. While guided tissue regeneration has not been shown to improve

outcomes following surgery (24,25) except in certain cases, such as an apico-marginal

defect (26), a lack of adequate site preservation may hinder future implant placement in

the surgical site. It is plausible that it could even affect implant placement in adjacent

sites if osteoclastic activity remodels the cortical plate adjacent to the site while the infill

happens in the osteotomy. While an elimination of the periapical radiolucency on

2-dimensional radiographs corresponds with the reformation of the cortical plate (27), it is

unknown how much the bucco-lingual thickness of the bone at the surgical site is

restored. Even studies using cone-beam computed tomography (CBCT) have focused

on the resolution of the periapical radiolucency (28,29,30) and not on the bucco-lingual

thickness of the bone.

The purpose of this study was to evaluate the 3-dimensional, or volumetric,

healing of the surgical site after at least one year (time being the fourth dimension), with

focus on the bucco-lingual width of the bone and the surface contour of the cortical

plate. One year follow-up has been shown to correlate well with long-term

(37)

ii. Materials and Methods a. Recruitment

Participants were identified from a pool of patients who had been treated at the

University of North Carolina – Chapel Hill between the years 2011-2016 and who had a

CBCT made within three months prior to the date of surgery. Patients were contacted

for a follow-up visit regarding their surgery. Upon completion of the routine follow-up

visit, all patients who met the inclusion/exclusion criteria were offered the opportunity to

participate in the study.

Inclusion criteria were as follows:

1. Patient ASA I or ASA II

2. Patient age 18-65 at time of surgery

3. Periapical microsurgery completed 1-6 years prior to date of recall exam

4. CBCT made within 3 months prior to date of surgery

Exclusion criteria were as follows:

1. Patient ASA III or higher

2. Apico-marginal defect present at time of surgery

3. Tooth in question responds positively to percussion or palpation

4. Tooth in question displays isolated probing defect >5mm

5. Patient pregnant

(38)

In total, 61 patients were identified for follow-up. Of the 61, 11 patients had the

tooth extracted prior to follow-up, 11 patients were unable to be contacted, and 3

refused the follow-up visit. This left 36 patients who were scheduled for the follow-up

exam. Of the 35 patients, 5 did not show up to their follow-up appointment and were

unable to be rescheduled, 2 did not meet the inclusion criteria, and 16 had their original

CBCT lost following a hard-drive failure. This left a total of 13 participants in the study.

Consent was obtained from those who agreed to participate, and a pregnancy

test was administered to any potential participant where pregnancy was a possibility.

All tests were negative.

b. CBCT Exposure

A limited-field CBCT was made of the surgical site. CBCT allows for accurate

examination of hard-tissue in-vivo without the need for surgery (36,37). It has also been

shown to have a high inter-observer agreement (23). With the exception of one

participant, all CBCT volumes were made using the Kodak 9000 3D® (Carestream

Dental, Stuttgart, Germany). The Kodak 9000 has a high resolution in limited field

imaging with a relatively low radiation dose compared with similar models (38,39). One

participant had CBCT made using the Orthophos XG 3D® (Sirona, Bensheim,

Germany). This unit was chosen as the pre-operative CBCT for the patient had been

made on the unit, and as such the post-operative CBCT needed to be made on the

(39)

c. Segmentation and Registration

CBCT does not directly produce a 3-dimensional image. What it creates is a

series of 2-dimensional images, which can be stacked to simulate a 3-dimensional

object (40). This series of images is most often stored in the DICOM format. For

volumetric analysis, the DICOM images must be converted into a true 3-dimensional

object; a process known as segmentation. In this study, segmentation was completed

using the software ITK-SNAP (41), which has been used in the orthodontic literature for

this purpose (42). Following segmentation, the area of interest was stored as a .STL

file, a common file used for 3-D illustration and modeling. (See picture 1, picture 3 in

appendix.)

After segmentation, the pre-operative and post-operative 3-D models were

registered using the software “GeoMagic” (43). (See picture 2, picture 4 in appendix.)

Registration is the process whereby the objects are analyzed, certain reference points

established (in the case of GeoMagic, many reference points,) and the two objects are

overlaid similarly to subtraction radiography so that the changes may be analyzed. The

main difference between registration and subtraction radiography is that with

registration, the changes can be analyzed volumetrically, and not just in two

dimensions.

Using GeoMagic, the registered volumes were analyzed for changes. The

volume change of the buccal bone was quantified using the cortical plate surface as a

(40)

iii. Results

Of the 14 subjects, 2 were excluded following segmentation when it was

determined that the volumes could not be registered due to excessive scatter from

implant restorations and screws used during surgical reconstruction. Thus, 12 subjects

were included for data analysis in this study.

Among the twelve participants, 3 (25%) were male and 9 (75%) female. 2

(16.7%) had received bisphosphonate therapy within the two years prior to surgery. 6

participants were 50 or younger, and 6 were older than 50. Median time post-surgery

was 25 months.

Volumetric analysis showed the median volume change of the buccal cortical

plate to be -24.9mm3 (IQR -8.94 – -67mm3), with an average linear error of 0.7mm

(Table 1, Figure 1). The average linear error is the software’s estimate of how closely

aligned the volumes are following registration. In other words, 24.9mm3 of bone loss occurred in and around the surgical site. Subjects with volume change higher than the

IQR also had greater average error of registration (Figure 2). All linear bucco-lingual

(41)
(42)

Figure 1: Boxplot of the volume change of the buccal cortical plate. Median volume change -24.9mm3 (IQR

5.12mm3

: Boxplot of the volume change of the buccal cortical plate. Median volume (IQR -8.94mm3 – -67mm3), total range of values

(43)

Figure 2: Graphic representation of the volume change in mm

error in mm. The two samples with greatest volume change also had the greatest average error.

iv. Discussion

Although the reported success rate of periapical microsurgery is consistently

90% (10,17), the prudent clinician will concern him/herself with the potential of an

adverse outcome and the reasonable methods known to either avoid that outcome or

prepare for it. While ridge preservation following extraction has shown clear benefi

(44), the potential need for site maintenance following periapical surgery has hitherto

remained unclear (24,45).

representation of the volume change in mm3 compared to the average

The two samples with greatest volume change also had the greatest

Although the reported success rate of periapical microsurgery is consistently

90% (10,17), the prudent clinician will concern him/herself with the potential of an

adverse outcome and the reasonable methods known to either avoid that outcome or

prepare for it. While ridge preservation following extraction has shown clear benefi

(44), the potential need for site maintenance following periapical surgery has hitherto

compared to the average The two samples with greatest volume change also had the greatest

Although the reported success rate of periapical microsurgery is consistently over

90% (10,17), the prudent clinician will concern him/herself with the potential of an

adverse outcome and the reasonable methods known to either avoid that outcome or

prepare for it. While ridge preservation following extraction has shown clear benefits

(44)

The results of this study show that there is little to no regression of the buccal

cortical plate (and resultant thinning of the alveolus) following apical surgery. While

25mm3 of bone loss may seem significant if imagined as a cube approximately 3mm in

length, this is an inaccurate view of the results. Total bone regression was measured

over the surgical site, an area of approximately 12mm x 16mm, or almost 200mm2. Seen in

this light, a loss of 25mm3 of bone is equivalent to less than 0.25mm of cortical plate

regression. This theory is confirmed, as we were unable to measure any linear

bucco-lingual change in thickness, as the changes were within the average error of the

registrations.

One limitation of this study is that the software GeoMagic has not been validated

for this purpose on dry skulls. Validation using dry skulls and known volume change

could establish a better understanding of the average error and the ratio of the affect of

average error on volume change calculations. Another limitation is that during the

surgical procedure, the root tip and some of the cortical bone are removed, which

changes the volume of the hard tissue at the surgical site. This problem could be

remedied by taking the CBCT image immediately following surgery. Other limitations

include a small sample size and a lack of controls. Even with these limitations, the

results were consistent, and confirm the results of studies that were symptom-based

mentioned prior.

v. Conclusion

While the use of GeoMagic has not been previously validated in an endodontic

model, it has been used previously in the orthodontic literature (42). And though the

(45)

microsurgery, and in the absence of grafting materials or membranes, healing occurs

with little to no regression of the buccal cortical plate and resultant thinning of the

alveolar bone. Future research in this area could involve validation of the software

using dry skulls, or a comparison of .STL quality among different CBCT units. Research

could also be furthered by having a larger patient pool and a more stringent set of

inclusion/exclusion criteria to evaluate only patients without metal restorations in the

area to decrease scatter radiation. However, this would be very difficult, as most

endodontically-treated teeth have received a metal-base or zirconia crown, both of

(46)

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2. Lin S, Sabbah, W, Sedgley, C, Whitten B. A Survey for Endodontists in Today's Economy: Exploring the Current State of Endodontics as a Profession and the

Relationship between Endodontists and Their Referral Base. Journal of Endodontics. 2015;41:325-332.

3. Suvey Center, American Dental Association [Internet]. Chicago, IL: ADA, c2005-2006. Survey of Dental Services Rendered and Distribution of Dentists in the United States by Region and State; 2005 [cited 2/24/2016]. Available from:

https://www.ada.org/~/media/ADA/Science%20and%20Research/HPI/Files/05_sdsr2014 0404t121935.pdf?la=en

4. Schamberg ML. The surgical treatment of chronic alveolar abscess. Dent Cosmos. 1906;48:15-24.

5. Moorehead FR. Removal of roughened apex. Dent Cosmos. 1903;45:163.

6. Hartzell TB. Root-tip amputation and external drainage for dental abscesses. Trans Natl Dent Assoc 1908; 207–8.

7. Hartzell TB. Root tip amputation. Dominion Dent J 1911; 23:473–82.

8. Kim S, Kratchman S. Modern Endodontic Surgery Concepts and Practice: A Review.

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Journal of Endodontics. 2015;41:22-27.

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Figure

Table 1 : Table of subjects listed by volume change in increasing order. : Table of subjects listed by volume change in increasing order.
Figure  1:  Boxplot  of  the  volume  change  of  the  buccal  cortical  plate.    Median  volume  change  -24.9mm 3   (IQR
Figure 2: Graphic representation of the volume change in mm
Figure  3:  Graphic  representation  of  the  time  elapsed  between  periapical  microsurgery  and the post-operative CBCT volume.

References

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