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Clinical Research

Evaluation of New Cone-beam Computed Tomographic


Criteria for Radiographic Healing Evaluation after Apical
Surgery: Assessment of Repeatability and Reproducibility
Thomas von Arx, Prof Dr med dent,* Simone F.M. Janner, Dr med dent,*
anni, Dr med dent,†‡ and Michael M. Bornstein, Prof Dr med dent*
Stefan H€

Abstract
Introduction: Conventional 2-dimensional radiography showed an excellent intraobserver agreement (repeatability). With regard to interob-
uses defined criteria for outcome assessment of apical server agreement (reproducibility), the B index (healing of apical and cortical defects
surgery. However, these radiographic healing criteria combined) and the R index (healing on the resection plane) showed substantial congru-
are not applicable for 3-dimensional radiography. The ence and thus are to be recommended in future studies when using buccolingual CBCT
present study evaluated the repeatability and reproduc- sections for radiographic outcome assessment of apical surgery. (J Endod 2016;-:1–7)
ibility of new cone-beam computed tomographic
(CBCT)-based healing criteria for the judgment of peri- Key Words
apical healing 1 year after apical surgery. Methods: Apical surgery, cone-beam computed tomography, healing indices, radiographic healing
CBCT scans taken 1 year after apical surgery (61 roots outcome, repeatability, reproducibility
of 54 teeth in 54 patients, mean age = 54.4 years)
were evaluated by 3 blinded and calibrated observers
using 4 different indices. Reformatted buccolingual
CBCT sections through the longitudinal axis of the
treated roots were analyzed. Radiographic healing was
assessed at the resection plane (R index), within the
T he evolution of modern apical surgery is based on the enhancement of visualization
(surgical microscope, endoscope), the introduction of microsurgical techniques
and microinstruments, and the use of biocompatible and cement-inducing root-end
apical area (A index), of the cortical plate (C index), filling materials (1–4).
and regarding a combined apical-cortical area (B index). The introduction of cone-beam computed tomographic (CBCT) imaging has been
All readings were performed twice to calculate the intra- another milestone in modern endodontics (5). Although CBCT imaging has gained a
observer agreement (repeatability). Second-time read- wide reputation for diagnostics and treatment planning, CBCT scanning does not yet
ings were used for analyzing the interobserver have the same impact on the assessment of endodontic treatment outcome (6). The latter
agreement (reproducibility). Various statistical tests is mainly because of economic aspects and concerns about radiation dose (7). In apical
(Cohen, kappa, Fisher, and Spearman) were performed surgery, CBCT imaging has been shown to be an important tool for case assessment and
to measure the intra- and interobserver concurrence, treatment planning (8, 9). However, the actual benefit of CBCT imaging for treatment
the variability of score ratios, and the correlation of outcome and its cost-effectiveness (cost-benefit analysis) have not yet been elaborated
indices. Results: For all indices, the rates of identical in conjunction with conventional or surgical endodontics.
first- and second-time scores were always higher than Recently, some clinical articles have documented the use of CBCT imaging for post-
80% (intraobserver Cohen k values ranging from operative evaluation in apical surgery (10–12). These studies either compared
0.793 to 0.963). The B index (94.0%) showed the periapical radiography (PA) and CBCT imaging in the outcome assessment of
highest intraobserver agreement. Regarding interob- ‘‘radiographic healing’’ based on the absence or presence of radiolucencies in
server agreement, the highest rate was found for the follow-up radiographs or measured the size of persistent lesions using CBCT imaging.
B index (72.1%). The Fleiss’ k values for R and B indices Although some authors have suggested a new CBCT periapical index for the evaluation of
exhibited substantial agreement (0.626 and 0.717, endodontic lesions before treatment (13, 14), that index is not applicable and useful for
respectively), whereas the values for A and C indices CBCT assessment of the outcome of apical surgery.
showed moderate agreement (0.561 and 0.573, respec- Traditionally, the PA criteria for healing assessment of apical surgery are based on
tively). The Spearman correlation coefficients for R, A, C, the work by Rud et al (15) and Molven et al (16). However, a recent study has shown
and B indices all exhibited a moderate to very strong cor- that these 2-dimensional criteria may not be valid for the evaluation of 3-dimensional
relation with the highest correlation found between C images (12). A new experimental dog study has suggested scoring criteria for CBCT
and B indices (rs = 0.8069). Conclusions: All indices evaluation of teeth treated with apical surgery (17).

From the Departments of *Oral Surgery and Stomatology and †Preventive, Pediatric, and Restorative Dentistry, School of Dental Medicine, University of Bern and

Private Practice Limited to Endodontics, Bern, Switzerland.
Address requests for reprints to Dr Thomas von Arx, Department of Oral Surgery and Stomatology, School of Dental Medicine, University of Bern, Freiburgstrasse 7,
CH-3010 Bern, Switzerland. E-mail address: thomas.vonarx@zmk.unibe.ch
0099-2399/$ - see front matter
Copyright ª 2016 American Association of Endodontists.
http://dx.doi.org/10.1016/j.joen.2015.11.018

JOE — Volume -, Number -, - 2016 New CBCT Criteria for Radiographic Healing 1
Clinical Research
TABLE 1. Definition of R, A, and C Indices According to Chen et al (17)
Index Definition Score 0 Score 1 Score 2
R Resection plane (cut root No bone deposition (no Partial bone deposition Complete bone deposition
face) formation of PDL space) (partial formation of (complete formation of
PDL space) PDL space of normal
width)
A Apical area (former bone No apparent bone Partial bone formation Complete bone formation
defect) formation
C Cortical plate (access bone Not re-established Re-established, but Re-established and flat
window) concave
PDL, periodontal ligament.

Figure 1. A schematic illustration of the R index (bone deposition along the resection plane).

The objective of the present study was to evaluate these new CBCT- Otoscope; Karl Storz GmbH, Tuttlingen, Germany) was used for intrao-
based criteria in a prospective clinical study for the radiographic perative diagnostics during root-end management (resection, cavity
outcome assessment 1 year after apical surgery. preparation, and filling). All treated roots were filled with MTA (Pro-
Root Dentsply Tulsa Dental, Tulsa, OK).
Patients were recalled 1 year after surgery for healing assessment
Material and Methods including a clinical examination, PA, and CBCT imaging. For the present
The present study was approved by the Ethics Committee of the analysis, only 1 tooth was randomly included (Quickcalcs; GraphPad
State of Bern, Switzerland (approval number KEK-BE 098/11) (18). Pa- Software Inc, La Jolla, CA) in patients who had apical surgery of multiple
tients were enrolled provided that they agreed on having presurgical and teeth.
1-year follow-up PA and CBCT radiographs in conjunction with apical The CBCT images were obtained with 3D Accuitomo 170 (J Morita
surgery. Patient information, recruitment, and treatment were per- Manufacturing Corp, Kyoto, Japan). The normal field of view was
formed according to the Declaration of Helsinki 2013. 4  4 cm or 6  6 cm for preoperative and 4  4 cm for postoperative
All surgeries were performed using local anesthesia in an oper- CBCT imaging. The parameters of the recordings were 3.0 mA and 80 kV
ating room by the same surgeon (19). All surgical steps were performed with an exposure time of 17.5 seconds. CBCT images were evaluated on
using a surgical microscope. A rigid endoscope (Hopkins Tele a Dell 380 workstation (Dell SA, Geneva, Switzerland) and a 19-inch

Figure 2. A schematic illustration of the A index (bone formation within the apical area).

2 von Arx et al. JOE — Volume -, Number -, - 2016


Clinical Research

Figure 3. A schematic illustration of the C index (reformation of the cortical plate).

TABLE 2. Overview of Evaluated Teeth (N = 54) and Roots (N = 61) Furthermore, a separate radiographic analysis was performed by
the same 3 observers using a so-called B index. The latter was created to
N teeth N roots
simplify the periapical radiographic assessment in combining the A and
Maxilla C indices of the initially applied indices. The B index was defined as
Central incisors 9 9
Lateral incisors 8 8
follows:
Canines 1 1 B-score 2: Complete hard tissue (‘‘bony trabecular’’) fill of former
1st premolars 3 3
2nd premolars 8 8 lesion/osteotomy site and formation of an intact cortical plate in its
1st molars 5 6 (5 mesiobuccal, anatomically correct shape
1 distobuccal) B score 1: Any situation not attributable to B scores 0 or 2
Subtotal 34 35 B score 0: Neither hard tissue fill of former lesion/osteotomy site
Mandible
Canines 2 2
nor formation of cortical plate
2nd premolars 2 2
1st molars 16 22 (15 mesial, 7 distal)
Subtotal 20 26 Statistical Analysis
Total 54 61 For the intraobserver agreement, the Cohen kappa values were
calculated for 2 ratings using squared weights (20). For the interob-
Eizo monitor with a resolution of 1280  1024 pixels (Eizo Nanao AD, server agreement between second-time readings of R, A, C, and B
W€adenswil, Switzerland). indices, Fleiss’ kappa values were calculated. The Fisher exact test
For further analysis, reformatted CBCT scans in the buccolingual was used (confidence level of 95%) to check whether the ratios of
plane through the center of the root along its longitudinal axis were eval- agreement between the observers were significantly different from
uated. The relevant section had been preselected by a surgeon who was each other. Spearman correlation coefficients were calculated to
not involved in the radiographic assessment. The evaluation was based analyze correlations between the indices. All tests were performed using
on the R, A, and C indices (Resection plane, Apical area, and Cortical the Internet-based R software package (R 3.0.3; www.r-project.org; The
plate) as suggested by Chen et al (17). The criteria of the scores are R Foundation, Vienna, Austria).
presented in Table 1 and Figures 1–3. Three observers were
calibrated with 1-year follow-up CBCT images of teeth that had been pre- Results
viously treated with apical surgery and that did not belong to the present Fifty-four teeth in the same number of patients fulfilled the criteria
study cohort. No time limit was set for image evaluation, and the ob- for CBCT assessment 1 year after apical surgery. At the time of surgery,
servers were allowed to use the software tools for image editing (size, patients had a mean age of 54.4  10.2 years (range, 24–73 years) and
brightness, and contrast). All images were evaluated twice with a min-
imum interval of 2 weeks to determine the intraobserver agreement
(repeatability). Second-time readings were used for interobserver anal- TABLE 4. Repeatability (intraobserver agreement) of First- and Second-time
ysis (reproducibility) and healing judgment of the treatment. Readings
Observer 1 Observer 2 Observer 3 All observers
TABLE 3. Healing Rates per Index (N = 61) Index (N = 61) (N = 61) (N = 61) (N = 183)
Complete Partial R (esection 80.3% 80.3% 90.2% 83.6%
Index healing (%) healing (%) No healing (%) plane) k = 0.801 k = 0.821 k = 0.920 k = 0.855
A (pical 80.3% 83.6% 85.3% 83.1%
R (esection plane) 54.1*‡ 29.5 16.4† area) k = 0.793 k = 0.839 k = 0.878 k = 0.843
A (pical area) 47.5* 37.7 14.8† C (ortical 90.2% 86.9% 90.2% 89.1%
C (ortical plate) 21.3* 32.8 45.9† plate) k = 0.919 k = 0.897 k = 0.909 k = 0.910
B (one) 34.3‡ 45.9 19.7 B (one) 96.7% 93.4% 91.8% 94.0%
k = 0.963 k = 0.941 k = 0.941 k = 0.947
*Statistically significant overall difference between R, A, and C values; Fisher exact test, P = .0003908.

Statistically significant overall difference between R, A, and C values; Fisher exact test, P = .0001033. Kappa values (20): <0, no agreement; 0–0.2, slight agreement; 0.21–0.40, fair agreement; 0.41–

Statistically significant difference between R and B values; Fisher exact test, P = .045. 0.60, moderate agreement; 0.61–0.80, substantial agreement; 0.81–1, almost perfect agreement.

JOE — Volume -, Number -, - 2016 New CBCT Criteria for Radiographic Healing 3
Clinical Research
TABLE 5. Reproducibility (interobserver agreement) of Second-time Readings (N = 61)
Observers Observers Observers Observers Observers
Index 1 = 2 = 3* 1 = 2 (s3) (%) 2 = 3 (s1) (%) 1 = 3 (s2) (%) 1 s 2 s 3 (%)
R (esection plane) 67.2% 9.8 19.7 3.3 0
k = 0.626
A (pical area) 59.0% 19.7 8.2 13.1 0
k = 0.561
C (ortical plate) 59.0% 13.1 3.3 24.6 0
k = 0.573
B (one) 72.1% 19.7 4.9 3.3 0
k = 0.717
Kappa values (20): <0, no agreement; 0–0.2, slight agreement; 0.21–0.40, fair agreement; 0.41–0.60, moderate agreement; 0.61–0.80, substantial agreement; 0.81–1, almost perfect agreement.
*1 = 2 = 3: all 3 observers had identical scores.

included 25 men (46.3%) and 29 women (53.7%). The total number of Correlation of Study Parameters
evaluated roots was 61 (Table 2). The Spearman correlation coefficients for R, A, C, and B indices all
With regard to healing classification, none of the cases had a study exhibited a moderate to very strong correlation (Table 6). The highest
parameter with 3 different scores; hence, at least 2 observers always correlation was found between C and B indices (rs = 0.8069, very
agreed on the same healing score per case and index. Based on a ma- strong correlation), whereas the lowest correlation was observed be-
jority classification (same rating by at least 2 observers), the resection tween R and C indices (rs = 0.5945, moderate correlation).
plane exhibited the highest rate of complete healing (54.1%), whereas
rates of complete healing of the apical area (47.5%) and the cortical
plate (21.3%) were lower. Complete healing with regard to the B index Discussion
was 34.3% (Table 3). The present prospective clinical study evaluated the repeatability
and reproducibility of new CBCT-based radiographic indices for
assessing the 1-year healing outcome of apical surgery (Figs. 4–7).
Repeatability (Intraobserver Agreement)
The rates of identical first- and second-time scores per study Material
parameter and observer were always higher than 80% (Table 4). Scores Although this study had a prospective design, patients could not be
never differed >1 when comparing first- and second-time ratings. On enrolled consecutively because some of the patients declined to have a
average (all observers), the B index (94.0%) showed the highest CBCT scan taken 1 year after apical surgery. The number of evaluated
intraobserver agreement, which was significantly different from teeth (N = 54) is comparable with the number (N = 52) in the study
the R (P = .003) and A indices (P = .002) but not the C index by Christiansen et al (10) but larger than the number (N = 11) in
(P = .132). the study by Tanomaru-Filho et al (11); both studies also used CBCT
imaging for radiographic outcome evaluation after apical surgery but
Reproducibility (Interobserver Agreement) with different objectives compared with the present study.
For all study parameters, scores across the 3 observers never
differed >1; hence, 2 observers always agreed on the same score for
each case and index. The highest overall agreement (all 3 observers
giving the same score) was found for the B index (72.1%), whereas
the reproducibility regarding healing assessment of the apical area
and the cortical plate (each 59.0%) had the lowest reproducibility
(Table 5). The Fleiss’ kappa values for R and B indices exhibited
substantial agreement (k = 0.626 and k = 0.717, respectively),
whereas the values for A and C indices showed moderate
agreement (k = 0.561 and k = 0.573, respectively). The ratios of agree-
ment between the 3 observers regarding the R, A, and C indices
(P = .598) and the novel B index (P = .694) were not significantly
different.

TABLE 6. Correlation of R, A, C, and B Indices


Comparison of indices Correlation coefficient*
R versus A 0.7287
R versus C 0.5945
R versus B 0.6952
A versus C 0.7569
A versus B 0.7655
C versus B 0.8069
*Spearman correlation coefficient: 1 = perfect correlation, 0.80–0.99 = very strong correlation, Figure 4. The distal root of a first mandibular molar showing complete heal-
0.60–0.79 = strong correlation, 0.40-0.59 = moderate correlation. ing in a 24-year-old woman (all indices were 2).

4 von Arx et al. JOE — Volume -, Number -, - 2016


Clinical Research

Figure 5. The mesial root of a first mandibular molar showing partial healing Figure 7. The lateral maxillary incisor showing no healing in a 56-year-old
on the resection plane in a 57-year-old man (R, A, and B indices = 1, woman (all indices were 0).
C index = 0).

Methodology remains the gold standard and reference for healing assessment after
According to current guidelines, CBCT imaging should not be used apical surgery, surgical harvesting of periapical tissue at the 1-year
for postsurgical and follow-up evaluation in apical surgery, mostly follow-up was judged ‘‘nonethical’’ and discarded.
because of radiation issues (7, 21, 22). However, previous studies The rationale for using CBCT imaging (instead of histology) is
have shown that conventional PA provides a different (ie, most often based on a recent experimental dog study reporting that the results ob-
a better and hence an overestimated) radiographic judgment of tained from CBCT imaging corresponded to the histologic results 6
periapical healing compared with CBCT imaging (10, 12). Hence, the months after apical surgery (17). Similar to Chen et al’s study param-
present study was designed and approved by the institutional review eters (17), the present investigation determined the healing on the re-
board to provide further insight with regard to repeatability and sected root-end surface as well as the healing of the apical area and the
reproducibility of CBCT-based healing criteria. Although histology cortical plate. From a clinical perspective, the healing on the resected
root-end surface is the most critical because bone formation along
the cut root face indicates that the root-end filling is bioinert, bioactive,
and bacteria tight. However, such minute tissue healing is not visible on
PA, and healing on the cut root face may only be inferred from the refor-
mation of a periodontal ligament space.
The rationale for using buccolingual CBCT scans was mainly a
practical one because mesiodistal CBCT scans of roots with an ectopic
position (maxillary incisors, canines, buccal roots of first premolars)
would be located outside the ‘‘bony housing,’’ with the apical area
located external to the surrounding cortices (Fig. 8).

Healing Outcome
The highest percentage of complete healing (54.1%) was
observed for the R index and the lowest (21.3%) for the C index. Cases
with partial healing on the resection plane showed that bone is ‘‘creep-
ing’’ over the cut root face from buccal and lingual aspects, eventually
forming a bony bridge at the resection level (Fig. 5). Re-establishment
of the cortical plate apparently takes longer compared with R and A
indices because it is the furthest away from the concentric growth
pattern of new bone formation and because there is no hard tissue sur-
face (access window) for new bone deposition. Hence, cortical refor-
mation has to await the infill (A index) of the bony crypt up to the level of
the buccal cortex.
Figure 6. The lateral maxillary incisor showing only limited healing in a 60- With regard to the B index, only 34.3% of the evaluated cases were
year-old man (R, A, and B indices = 1, C index = 0). considered completely healed in the present study; in other words,

JOE — Volume -, Number -, - 2016 New CBCT Criteria for Radiographic Healing 5
Clinical Research
the A and C indices among 3 observers and also combines apical and
cortical healing judgment, thus simplifying the rating procedure, it is
suggested to use the B index in future CBCT studies regarding radio-
graphic healing evaluation after apical surgery.

Reproducibility
The present study only accepted a rigorous interobserver agree-
ment (ie, scores had to be identical for all observers). Often studies
including multiple observers with different ratings try to reach a
consensus rating, with the risk that 1 observer has to give in. For inter-
observer agreement, the B index again showed a higher value (72.1%)
than the A and C indices (each 59%). Also, the R index (67.2%) had a
higher interobserver agreement than the A and C indices. When using
buccolingual CBCT images for healing judgment after apical surgery,
the R and B indices are recommended for clinical practice and future
research based on our results.
Unfortunately, the agreement rates obtained in this study cannot be
compared with data from other studies because such data have not been
reported. In Christiansen et al’s study (10), the authors remarked that
there was considerable variation between the observers’ detection of a
remaining defect using CBCT imaging, but the actual interobserver
agreement rate was not provided.

Conclusion
To our knowledge, this is the first clinical study to apply new CBCT-
based criteria for radiographic healing evaluation 1 year after apical
surgery. All study parameters showed excellent intraobserver agree-
ment (repeatability). With regard to interobserver agreement (repro-
ducibility), the B index (healing of apical and cortical defects
combined) and the R index (healing on the resection plane) showed
substantial congruence and thus are to be recommended in future
studies when using buccolingual CBCT sections for radiographic
outcome assessment of apical surgery.

Acknowledgments
The authors thank Anja M€uhlemann, Institute of Mathematical
Statistics and Actuarial Science, University of Bern, Switzerland, for
her assistance regarding the statistical analysis and Bernadette
Rawyler, Medical Illustrator, School of Dental Medicine, University
Figure 8. A schematic illustration showing a situation (right maxillary central of Bern, Switzerland, for the schematic illustrations.
incisor) in which the mesiodistal CBCT plane (red section) through the center The authors deny any conflicts of interest related to this study.
of the tooth would be outside the bony housing in the apical area. However, the
buccolingual CBCT plane (blue section) depicts all relevant structures. References
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