Download Evaluation of the Reliability and Accuracy of Using Cone

Clinical Research
Evaluation of the Reliability and Accuracy of Using
Cone-beam Computed Tomography for Diagnosing
Periapical Cysts from Granulomas
Jing Guo, BDS, MS, James H. Simon, DDS,† Parish Sedghizadeh, DDS, Osman N. Soliman, DDS,
Travis Chapman, DDS, and Reyes Enciso, PhD
Abstract
Introduction: The purpose of this study was to evaluate
the reliability and accuracy of cone-beam computed
tomographic (CBCT) imaging against the histopathologic diagnosis for the differential diagnosis of periapical
cysts (cavitated lesions) from (solid) granulomas.
Methods: Thirty-six periapical lesions were imaged
using CBCT scans. Apicoectomy surgeries were conducted for histopathological examination. Evaluator 1 examined each CBCT scan for the presence of 6 radiologic
characteristics of a cyst (ie, location, periphery, shape,
internal structure, effects on surrounding structure,
and perforation of the cortical plate). Not every cyst
showed all radiologic features (eg, not all cysts perforate
the cortical plate). For the purpose of finding the
minimum number of diagnostic criteria present in
a scan to diagnose a lesion as a cyst, we conducted 6
receiver operating characteristic curve analyses
comparing CBCT diagnoses with the histopathologic
diagnosis. Two other independent evaluators examined
the CBCT lesions. Statistical tests were conducted to
examine the accuracy, inter-rater reliability, and intrarater reliability of CBCT images. Results: Findings
showed that a score of $4 positive findings was the
optimal scoring system. The accuracies of differential
diagnoses of 3 evaluators were moderate (area under
the curve = 0.76, 0.70, and 0.69 for evaluators 1, 2,
and 3, respectively). The inter-rater agreement of the
3 evaluators was excellent (a = 0.87). The intrarater
agreement was good to excellent (k = 0.71, 0.76, and
0.77). Conclusions: CBCT images can provide a moderately accurate diagnosis between cysts and granulomas.
(J Endod 2013;39:1485–1490)
Key Words
Biopsy, cone-beam computed tomography, differential
diagnosis, granuloma, periapical cyst
T
he traditional diagnosis of apical cyst is based on histopathological examination
of biopsy tissue, which means that the only way to confirm the diagnosis is surgically
(1, 2). Previously, researchers attempted to make an accurate diagnosis of a cyst
compared with a granuloma using periapical (PA) radiographs (3), water-soluble
contrast media (4), Papanicolaou smears (5), and albumin tests (6). However,
none of these were accurate. Recently, studies on preoperative differential diagnosis
using advanced imaging technology, such as computed tomographic (CT) (7) and
cone-beam computed tomographic imaging (CBCT) (8, 9), have become available
in the literature. Aggarwal et al (7) used computed tomographic scans to differentiate
PA lesions; of 17 lesions evaluated, 12 were accurately diagnosed, wherein the imaging
results concurred with the histopathological diagnosis, indicating that computed tomographic scans could provide relatively accurate diagnosis without invasive surgery. Cotti
et al (9) also reported positive results for CT scans. Shrout et al (8) indicated that granulomas had a narrower range and lower grey values than cysts using CBCT imaging,
which could be used for the differential diagnosis of PA lesions according to the authors.
Researchers have evaluated the accuracy of CBCT imaging to detect apical periodontitis (AP) compared with PA radiographs. Estrela et al (10) evaluated a new PA
index based on CBCT imaging for the identification of AP. More AP was identified using
CBCT imaging (60.9%) than PA radiographs (39.5%) after examining 1,014 images.
The authors concluded that a PA index based on CBCT imaging might offer an accurate
diagnosis of AP. Their study provided convincing evidence of accurate diagnosis of AP
using CBCT images. Tsai et al (11) used simulated PA lesions in human cadavers to
assess the diagnostic accuracy of CBCT and PA radiographs. The authors indicated
that CBCT imaging showed excellent accuracy when simulated lesions were larger
than 1.4 mm, fair to good when between 0.8 and 1.4 mm, and poor when less than
0.8 mm. PA radiographs showed poor accuracy for all lesion sizes. Rodrigues et al
(12) reported a rare case of lymphangioma mimicking AP, indicating that CBCT imaging
could be useful for the diagnosis of well-circumscribed lesions. Rosenberg et al (13)
used CBCT images to differentiate PA cysts from granulomas with inconclusive findings,
indicating a weak agreement between 2 radiologists (k = 0.14) and an overall accuracy
of 0.65 for the first radiologist and 0.51 for the second compared with biopsy results.
Simon et al (14) differentiated PA cysts (cavitated lesions) from granulomas using CBCT
imaging (NewTom 3G; NewTom, Verona, Italy). Seventeen PA lesions were scanned, and
the gray values of each lesion were measured. The lesions were then surgically removed
for biopsy examination. In 13 of 17 lesions, the diagnoses of CBCT images were consistent with pathological reports. The authors indicated that CBCT images may provide
more accurate diagnosis than pathological reports.
From Ostrow School of Dentistry, University of Southern California, Los Angeles, California.
†Deceased.
Address requests for reprints to Dr Reyes Enciso, Ostrow School of Dentistry, University of Southern California, 925 West 34th Street, Room 4268, Los Angeles, CA
90089-0641. E-mail address: [email protected]
0099-2399/$ - see front matter
Copyright ª 2013 American Association of Endodontists.
http://dx.doi.org/10.1016/j.joen.2013.08.019
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The use of CBCT scans for endodontic diagnosis is controversial
because of concerns relating to a higher exposure of radiation to
patients than necessary, long duration of scanning, and expensive
cost compared with conventional dental radiographs (15). Although
CBCT imaging is widely used in orthodontics (16), dental implant treatment planning (17), and the detection of obstructive sleep apnea (18),
the use of gray values in the diagnosis of PA lesions exhibits some disadvantages according to a recent publication (16). Authors of this publication concluded that gray values could be easily affected by the field of
view and spatial resolution selections (16), so in our current study we
used a set of diagnostic criteria based on the radiologic characteristics
of apical cysts instead of using gray values.
The main purpose of the present study was to evaluate a set of diagnostic criteria for differentiating PA cysts from granulomas according to
their CBCT imaging characteristics. The criteria were established based
on the radiologic characteristics of PA cysts (19, 20). The goals of this
study were to evaluate this set of 6 diagnostic criteria and to find out the
optimal number of criteria findings necessary for the differential
diagnosis of PA cysts (cavitated lesions) versus granulomas; to
evaluate the intrarater and inter-rater reliability of 3 independent evaluators using 6 criteria for the differential diagnosis of cysts versus granulomas; and to evaluate the accuracy, specificity, sensitivity, and overall
agreement of CBCT diagnosis and histopathological reports for 3
blinded evaluators.
Materials and Methods
Thirty-six PA lesions diagnosed by clinical symptoms and radiographic findings were selected for the study. The inclusion criteria
of lesions were a minimum average diameter of 5 mm from sagittal
views of CBCT images. The protocol was approved by the Institutional
Review Board of the University of Southern California, Los Angeles, CA
(#UP-12-00506).
Radiology
PA radiolucency was imaged by Kodak 9000 3D (Carestream
Health Inc, Rochester, NY) at the Redmond Imaging Center, University
of Southern California. The technician acquired a fixed field of view
volume of 3.75 5 cm. The pixel size was 76 mm and 15-bit pixels
(32,768 gray values). The scanner was operated at 70–90 kV and
8–10 mA. The Digital Imaging and Communications in Medicine format
images were exported from Kodak 9000 and imported into InVivo
Dental Application 5.1.6 software (Anatomage Inc, San Jose, CA).
Histopathology
Root-end resections were performed per routine clinical protocols. Histopathological specimens were obtained for microscopic
examination, stained by hematoxylin-eosin, and analyzed. All histopathological specimens were examined by a board-certified oral pathologist
(PS) without prior knowledge of clinical symptoms of patients, CBCT
diagnosis, and surgical observation of lesions.
Pathology Microscopic Criteria for the Diagnosis of
Cysts versus Granulomas. For a granuloma diagnosis, there
had to be no histopathologic evidence of cystic organization; no
evidence of squamous lining epithelium as specifically described for
cyst diagnosis to follow; the presence of soft connective tissue morphologically consistent with granulation tissue; and the presence of inflammatory cell infiltrates, foamy histiocytes, or multinucleated giant cells.
For a cyst diagnosis, there had to be histopathologic evidence of fibrous
connective tissue with cystic organization and more than 1 definitive foci
of stratified squamous lining epithelium comprising $50 cohesive cells
attached by visible cell-cell junctions on high-power magnification
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Guo et al.
(60 original) and the presence or absence of inflammatory cell infiltrates within the wall or the lining of the cyst. Epithelial islands or odontogenic rests located or embedded within fibrous connective tissue were
not considered evidence of lining cystic epithelium. Overt evidence of
keratinaceous debris within an epithelial-lined lumen and the presence
of cholesterol clefts and Rushton bodies, erythrocyte extravasation and
hemosiderin deposition, and occasional multinucleated giant cells was
considered supportive of a cyst diagnosis along with the aforementioned
criteria and the acknowledgment that histopathologic findings can overlap between cysts and granulomas, and there is no single pathognomonic feature to discriminate the 2 lesions histopathologically. A
second evaluation of all biopsy slides was taken by the same oral pathologist after 2 weeks to calculate the intrarater reliability.
Diagnostic Criteria
A set of diagnostic criteria (Table 1) for PA cysts was established
based on radiologic characteristics (ie, location, periphery, shape,
internal structure, effects on surrounding structure, and perforation
of the cortical plate) (19, 20). For each lesion, evaluator 1 (JG),
without prior knowledge of the patient or the histopathological
report, examined the Digital Imaging and Communications in
Medicine images and tabulated the data. For each criterion, if
radiologic evidence was found, the lesion would be scored 1 point. A
cumulative score for each lesion was documented. The final score
for each lesion was a number between 0 and 6 according to the
number of positive findings.
Evaluation of Diagnostic Criteria
For each lesion, we computed a cumulative score 0–6 as explained
in the prior section. A score of 1 meant that only 1 of the criteria in
Table 1 was determined to be present in the images. Because of the limitations of CBCT scans and the fact that most cysts do not show all 6 characteristics (eg, not all cysts may perforate the cortical plate), all the
lesions did not show the 6 radiologic findings. For the purpose of
finding the optimal number of diagnostic criteria (scoring system) to
determine if a lesion was a cyst, we conducted 6 receiver operating characteristic (ROC) curve analyses (21). ROC provides measures of accuracy, which is constructed from the sensitivity and specificity of
a diagnostic test. The measure of accuracy was the area under the curve
(AUC), representing the average specificity over all sensitivities (21).
For the first ROC curve, a diagnosis of a cyst corresponded to a score
$1. The diagnosis of a cyst in the sixth analysis corresponded to a score
of 6. Therefore, 6 ROC analyses were conducted based on the histopathological diagnoses from the oral pathologist (cyst = yes/no) and the 6
CBCT diagnoses according to the 6 scoring systems ($1, $2, ., = 6).
The AUC (21) was calculated for each scoring system, ranging in value
from 0.5 (chance) to 1.0 (perfect discrimination or accuracy) (21).
The largest of the 6 AUCs was selected as the best scoring system and
was chosen for the diagnosis of a cyst. Three independent endodontist
evaluators (JG, OS, and TC) blinded to the histopathological reports
examined the images of 36 lesions using the 6 criteria in Table 1. A
TABLE 1. CBCT Diagnostic Criteria for the Differential Diagnosis of a Cyst
Located at the apex of the involved tooth
Well-defined corticated border
Shape is curved or circular
Internal structure of lesion is radiolucent
Displacement and resorption of the roots of adjacent teeth
with a curved outline
Perforation of cortical plate
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Clinical Research
lesion was diagnosed as a cyst if the score was equal or above 4 (the
optimal scoring system).
Intra- and Inter-rater Reliability
To assess the intrarater reliability of the 3 evaluators, all 36 cases
were examined for a second time 6 months later. The intrarater reliability of each evaluator was conducted with Cohen kappa. Cohen
kappa assesses the extent to which a rater agrees in 2 evaluations
of the same set of cases (22). Agreement was noted as excellent if
k $ 0.75, good if 0.60 # k < 0.75, intermediate if 0.4 # k <
0.60, and poor if k < 0.4 (22). Interevaluator agreement between
the 3 evaluators was conducted using Cronbach alpha tests. The Cronbach alpha test is used to assess the internal consistency among
multiple raters (23). Agreement was noted as excellent if a $
0.80, good if 0.60 < a < 0.79, intermediate if 0.40 < a # 0.60,
and poor if a # 0.40 (23). Figure 1 describes the overall protocol
for the study.
CBCT Comparison to Histopathological Reports
Using the best scoring system ($4 criteria), CBCT imaging was
compared with histopathological diagnoses. Sensitivity, specificity,
false-positive rate, false-negative rate, overall agreement, and AUCs
were calculated for each of the 3 independent evaluators. Accuracy
was noted as good if AUC > 0.80, moderate if 0.60 # AUC #
0.80, and poor if AUC < 0.60 (24). SPSS software version 17.0
(SPSS Inc, Chicago, IL) was used in this study with significance
accepted at a value of P < .05.
Results
The intrarater agreement for the oral pathologist was excellent
(k = 0.93). Among the 6 AUCs (Fig. 2A), one for each scoring system,
a score $4 positive findings exhibited the highest AUC (0.76); therefore, it was used in this study for the differential diagnosis of a cyst. A
lesion was diagnosed as a cyst if 4 or more of the 6 criteria evaluated
were considered as ‘‘yes’’ by the evaluator.
Intrarater agreement was good for evaluator 1 (k = 0.71) and
excellent for evaluators 2 (k = 0.76) and 3 (k = 0.77). Results of Cronbach alpha indicated that the interagreement between the 3 evaluators
was excellent, and it was not caused by chance agreement (a = 0.87).
When comparing each evaluator’s ratings with the histopathologic diagnosis (PS), we found a high mean overall agreement (mean overall rate
= 0.77). For evaluator 1, 30 of 36 lesions had the same diagnosis as the
histopathological reports (overall agreement = 0.83, AUC = 0.76,
Fig. 2B). For evaluator 2, 27 of 36 lesions were in agreement (overall
agreement = 0.75, AUC = 0.70, Fig. 2B), whereas 26 of 36 were in
agreement for evaluator 3 (overall agreement = 0.72, AUC = 0.69,
Fig. 2B). Table 2 presents the sensitivity, specificity, overall agreement,
false-positive rate, false-negative rate, and AUC for all 3 evaluators
compared with the histopathological results from the board-certified
oral pathologist (Table 2).
Figure 3A–F shows an example of a lesion with consistent diagnoses
of a PA cyst by 3 evaluators and the histopathological report. Figure 3G–L
shows an example of an inconsistent differential diagnosis between 3
evaluators (a PA granuloma) and the histopathological report (a PA
cyst). Figure 3M–R shows an example of a lesion with consistent diagnoses of a PA granuloma by 3 evaluators and the histopathological report.
Figure 1. The study protocol flowchart.
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Figure 2. (A and B) ROC curves and AUCs. (A) ROC curves and AUCs for 6 scoring systems (evaluator 1) compared with the histopathological diagnoses. (B) ROC
curves and AUCs using the optimal scoring system (evaluators 1, 2, and 3) compared with the histopathological diagnoses. The reference line (solid line) represents chance (50%) accuracy.
Figure 3S–X shows an example of a lesion with inconsistent diagnoses
between CBCT evaluation (2 of 3 evaluators diagnosed it as a PA cyst)
and the histopathological report (a PA granuloma).
Discussion
Surgical biopsy and pathological examination are standard procedures when a distinction between a PA cyst and a granuloma is necessary. Nair (2) concluded that 85% of all PA lesions were PA granulomas.
Lin et al (25, 26) indicated that most reactive PA lesions (granulomas
and radicular cysts) may heal by nonsurgical root canal therapy except
apical true cysts. Apical true cysts (PA cavities completely enclosed in
epithelial lining), particularly larger lesions, may require surgical
intervention because they are self-sustaining and not dependent on
the presence or absence of intracanal infection or inflammation (2,
25). However, there is no direct evidence to show that large cysts or
granulomas can or cannot heal after nonsurgical root canal therapy;
indirect clinical evidence appears to indicate that radicular cysts may
heal or regress after nonsurgical root canal therapy, whereas apical
true cysts require surgery (25). The key factor in establishing that apical
true cysts can or cannot heal after nonsurgical root canal therapy would
be the pretreatment identification of an apical lesion as an apical true
cyst (25). Currently, there is no predictable method of identifying
pretreatment apical lesions as an apical true cyst. Post-treatment biopsy
alone cannot be used to imply that apical true cysts can or cannot heal
after nonsurgical root canal therapy; this determination requires definitive pretreatment identification, which is impossible at this time (25). If
we were able to predict the presence of apical true cysts before nonsur-
gical root canal therapy, we could conduct outcome studies in animals
and humans to test the hypothesis of whether inflammatory cysts can or
cannot regress after nonsurgical root canal therapy (25). Thus, as 1
potential step toward this end, we evaluated in the current preliminary
study whether CBCT imaging could represent a feasible biopsyindependent alternative for differentiating apical cysts from granulomas.
CBCT imaging has been considered to be 1 nonsurgical alternative
used in the differentiation between apical cysts and granulomas (14). Tsai
et al (11) compared CBCT imaging and PA radiographs, and the results
showed that CBCT imaging showed excellent accuracy when simulated
lesions were larger than 1.4 mm, whereas AP radiographs showed
poor accuracy for all lesion sizes. Rodrigues et al (12) used PA radiographs, CBCT scans, and magnetic resonance imaging as methods to evaluate a lymphangioma mimicking AP, concluding that CBCT scans could
diagnose well-circumscribed lesions. However, its use is still controversial. CBCT imaging provides gray values rather than Hounsfield units,
which are easily affected by field of view, spatial resolution selection,
hard beaming, scattering, and the number of basis projections (17).
On the positive side, CBCT imaging has advantages in the field of endodontics because of better representation of soft tissue, lower exposure to radiation, and less cost compared with conventional CT imaging (27).
In this study, a set of 6 diagnostic criteria was evaluated to differentiate PA cysts from granulomas. The 6 criteria were based on the
radiologic characteristics of a PA cyst (location, periphery, shape,
internal structure, and effects on surrounding structure) (20). In
some cases, it is difficult to differentially diagnose a PA cyst from
a granuloma (20). The reason is that a granuloma might present
TABLE 2. Sensitivity, Specificity, False-positive Rate, False-negative Rate, Overall Agreement and AUC for 3 Evaluators Compared with Histopathological Diagnoses
Evaluator
Sensitivity
Specificity
Overall rate
False-positive rate
False-negative rate
AUC
1
2
3
0.60
0.60
0.60
0.92
0.81
0.77
0.83
0.75
0.72
0.08 (2/26)
0.19 (5/26)
0.23 (6/26)
0.40 (4/10)
0.40 (4/10)
0.40 (4/10)
0.76
0.70
0.69
AUC, area under the curve.
Sensitivity = true positive/(true positive + false negative), specificity = true negative/(true negative + false positive); overall rate = (true positive + true negative)/total number, false positive rate = false positive/
(false positive + true negative); false-negative rate = false negative/(false negative + true positive).
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Figure 3. (A–F) A lesion with consistent diagnoses between CBCT evaluation and histopathological diagnosis as a PA cyst. (A) A 3-dimensional reconstruction
image, (B) CBCT sagittal view, (C) CBCT coronal view, (D) CBCT axial view, (E) 40 histopathological photomicrograph, and (F) 100 histopathological photomicrograph. (G–L) A lesion with inconsistent diagnoses between CBCT evaluation (interevaluator agreement of a PA granuloma) and histopathological diagnosis (a
PA cyst). (G) A 3-dimensional reconstruction image, (H) CBCT sagittal view, (I) CBCT coronal view, (J) CBCT axial view, (K) 40 histopathological photomicrograph, and (L) 100 histopathological photomicrograph. (M–R) A lesion with consistent diagnoses between CBCT evaluation and histopathological diagnosis as
a PA granuloma. (M) A 3-dimensional reconstruction image, (N) CBCT sagittal view, (O) CBCT coronal view, (P) CBCT axial view, (Q) 40 histopathological
photomicrograph, and (R) 100 histopathological photomicrograph. (S–X) A lesion with inconsistent diagnoses between CBCT evaluation (2 of 3 evaluators
diagnosed it as a PA cyst) and histopathological biopsy (a PA granuloma). (S) A 3-dimensional reconstruction image, (T) CBCT sagittal view, (U) CBCT coronal
view, (V) CBCT axial view, (W) 40 histopathological photomicrograph, and (X) 100 histopathological photomicrograph.
with the same radiologic characteristics as a cyst. Also, not every cyst
will show all radiologic features (ie, not all cysts may perforate the
cortical plate) (20). Thus, an optimal number of criteria were assessed (highest AUC of 6 diagnostic criteria) in order to differentiate
a cyst from a granuloma with the most accuracy. Using ROC analyses
to assess the accuracy of each scoring system, we found that 4 or
more positive findings (criteria on Table 1) were the optimal choice
for a lesion to be diagnosed as a cyst (AUC = 0.76). All 3 evaluators in
our study showed moderate accuracy when compared with histopathological diagnoses from the board-certified oral pathologist (AUC =
0.76, 0.70, and 0.69).
In the present study, the results indicate that CBCT images could
provide good to excellent accuracy for differential diagnosis between
cysts and granulomas with excellent inter-rater (a = 0.87) and good
to excellent intrarater reliabilities. The mean overall agreement of 3
evaluators was 0.77, which was the same as that in a previous study
by Simon et al (14) using CBCT gray values. In that study, 13 of 17
CBCT diagnoses coincided with the biopsy reports (overall agreement
= 0.77). According to the authors, in the 4 cases of split diagnosis,
the pathological reports were inaccurate to diagnose AP because the
biopsy examination might not represent the entire lesion and epithelium
JOE — Volume 39, Number 12, December 2013
may be present but not identified in the viewed sections. The authors
concluded that CBCT imaging might be more accurate than biopsy
examination.
In a recent study by Rosenberg et al (13), 2 radiologists independently analyzed CBCT images from 45 patients using a set of diagnostic
criteria. The results indicated a weak (poor) agreement between 2 radiologists (k = 0.14), and an overall accuracy (AUC) of 0.65 for the first
radiologist and 0.51 for the second compared with the biopsy results.
The moderate to weak agreement between radiologists might be
because of the large number of possible diagnoses (eg, cysts, likely
cysts, granulomas, likely granulomas, and others), whereas only 2
possible differential diagnoses were taken into account in this article
(cyst/granuloma). In this study, we also attempted to reduce uncertainty
by reducing the number of criteria to 6 and making the diagnosis of
a cyst a quantitative measure (the presence of 4 or more radiologic
criteria). In the previous study, radiologists chose the best diagnosis
for each lesion based on the diagnostic criteria without a clear scoring
system; however, in the present study, evaluators only examined the
lesion based on the 6 predefined criteria and reported a cyst diagnosis
if 4 or more positive findings were present. The authors believe that this
quantitative scoring system reduced uncertainty and increased inter-
CBCT for Diagnosing PA Cysts from Granulomas
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rater and intrarater reliability and accuracy compared with prior
studies.
One of the limitations in our study was the small sample size.
Further studies on a larger number of cases will be required to
confirm the findings of the present study. Moreover, the small
amount of PA cyst lesions (10/36) also may have contributed to
the high rates of false negatives (4/10, 4/10, and 4/10 for the 3 evaluators). Another limitation is the inclusion of only 2 types of PA
lesions. On the positive side, the accuracy of all evaluators was
moderate, and the inter- and intrarater reliability was good to excellent. Finally, the cross-sectional nature of this study and the level of
evidence it represents is insufficient to make any recommendations
or claims regarding the clinical usefulness of CBCT imaging for the
diagnosis of reactive endodontic lesions. Well-controlled human
studies that are longitudinal in nature would be required to show
the clinical relevance and efficacy of CBCT imaging in the current
context, particularly given the radiologic standard of care (ie, as
low as reasonably achievable) for radiation exposure and safety to
patients. Accordingly, the current study is not meant to provide clinical evidence or rationale for subjecting patients to the additional
radiation of CBCT imaging.
In summary, CBCT images provided a moderately accurate differential diagnosis between cysts and granulomas when the apical lesion
presented with a minimum average diameter of 5 mm. CBCT imaging
exhibits potential for further research in endodontics for the differential
diagnosis of cysts versus granulomas.
Acknowledgments
The authors deny any conflicts of interest related to this study.
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