Mithaq F.doc
J Bagh College Dentistry Vol. 25(Special Issue 1), June 2013 The value of ultrasound
Oral Diagnosis 59
The value of ultrasound and color doppler
ultrasonography in the evaluation of periapical lesions in
comparison to histopathological and/or surgical findings
Mithaq A. Zebun, B.D.S. (1)
Ahlam A. Fattah, B.D.S., M.Sc. (2)
ABSTRACT
Background: Imaging techniques play a very important role in the specialty of endodontic. The ultrasonographic
technique is non-expensive procedure, safe, and reproducible. The aim of the study was to determine the sensitivity,
specificity, and accuracy of ultrasound and color Doppler ultrasonography in evaluation of periapical lesions (cyst,
granuloma, mixed lesion “cyst within graulomas mass”, and abscess.
Subject, Material and method: The sample consists of prospective study for 64 Iraqi participants who attended
Karbalaa Specialized Center for Dentistry (males & females).
Those patients were diagnosed clinically and radiographically as having periapical lesions of dental origin. They were
examined by real time ultrasound and color Doppler ultrasonography with echographic predilection about the type
of the lesion based on three parameters measured by ultrasound including: content, outline, and the vascularity. The
echographic diagnosis was compared to the final histopathological and /or surgical findings obtained from the
periapical surgeries.
Results: The sensitivity, specificity and accuracy of ultrasound diagnosis were respectively as follow: for periapical
cyst, they were 92.3%, 96.1%, and 95.3%. While for periapical granulomam, they were 87.0%, 92.7%, and 90.6%. For
mixed lesions, they were 66.7%, 98.4%, and 96.9% and lastly for periapical abscess, they were 92.0%, 97.4%, and 95.3%.
The ultrasound diagnosis in our study had an overall agreement of 89% between ultrasound diagnosis and final
diagnosis based on histopathological and/ or surgical findings.
Conclusion: Ultrasound is a non- invasive, low cost, and complementary method for examination and diagnosis of
periapical lesions and there is correlation of ultrasonographic findings with histopathological and /or surgical findings
for final diagnosis.
Key words: periapical lesions, ultrasound, color Doppler. (J Bagh Coll Dentistry 2013; 25(Special Issue 1):59-66).
INTRODUCTION
Periapical lesions resulting from necrotic
dental pulp are among the most frequently
occurring pathologies found in the alveolar bone,
exposure of the dental pulp to bacteria and their
by-products, acting as antigens, may elicit non
specific inflammatory responses as well as
specific immunological reactions in the
periradicular tissues, and cause the formation of
periapical lesion (1,2). Radiology is the first, but
not the only, method used to identify intra- and
extra-osseous jaw lesions (3,4). Clinical
examination and radiographs alone cannot
differentiate between cystic and non cystic
lesions. Being able to distinguish between the
two may be of importance in predicting treatment
failure (5), and it is very important to accurately
diagnose the periapical lesions and exclude any
rare chance of neoplastic occurrence (6).
Computerized tomography (CT) can be used to
make a differential diagnosis between cystic and
non cystic lesions (7, 8).
Unfortunately, routine use of CT is associated
with high dosage of radiation, even though dose
reduction methods have been established (9).
(1) Master Student, Department of Oral Diagnosis, College of
Dentistry, University of Baghdad.
(2) Assistant Professor, Department of Oral Diagnosis, College
of Dentistry, University of Baghdad.
Magnetic resonance imaging (MRI) is useful
in the diagnosis, but it is not practical in the
dental field. Ultrasound has no ionizing
radiation, no known harmful effects at the
energies and doses used, in addition the
technique is widely available and inexpensive
(10).
MATERIALS AND METHODS
The study sample consists of 64 Iraqi patients
(males and females) with periapical lesions
referred for treatment to Kerbalaa Specialized
Centre between September 2011 and April 2012.
Their age ranged between (15-60) years old. The
ultrasound examination was performed by using
a Philips of HI 11 XE ultrasound system with 7.5
MHz linear array probe in (Al-Hussein general
hospital). The parameters measured by
ultrasound were as shown in figures (1, 2, 3, and
4):
1- Texture of the lesion: the interpretation of
grey values on an image is based on a
qualititative comparison of the echo intensity
with that of normal tissue. Hypoechoic or
transonic is an area with low echo intensity;
anechoic is an area where no reflection occurs (i.
e. any area filled with fluid), and hyperechoic is
an area which has high echo intensity (11).
J Bagh College Dentistry Vol. 25(Special Issue 1), June 2013 The value of ultrasound
Oral Diagnosis 60
2- Vascularity: by the color power Doppler,
the vascularization within the lesion can be seen.
A differential diagnosis between cystic lesion
and granuloma may be done based on the
following principles: cystic lesion is a transonic,
well defined cavity filled with fluid and with no
evidence of internal vascularization at the color
power Doppler, while the granuloma is a distinct
lesion shows hyperechoic texture and internal
vascularization with out well defined contour.
3- The margin of the lesion: if it is regular or
irregular.
Figure 1: Ultrasound of periapical cyst show
hypoechoic texture, well defined margin and
reinforced bone
Figure 2: Uultrasound of periapical
granuloma show hyperechoic texture and
vascularization (blue and red spots)
Figure 3: Ultrasound of mixed periapical
cyst/granuloma show hypoechoic and
avascular center with hyperechoic and
vascular periphery
Figure 4: Ultrasound of periapical abscess
show irregular margin and hypoechoic
texture
Statistical data analysis
OR (odds ratio) to measure the strength of
association between 2 categorical variables, such
as the presence of certain US criteria and having
a specific final diagnosis, the odds ratio (OR)
was used. For example OR for the association
between having a hypoechoic texture and having
a final diagnosis of periapical cyst, equals the
ratio of the odds of having the specific US
criteria versus lacking it among cyst cases to the
similar odds among non-cyst cases.
Having periapical
cyst
+ -
BC
AD
D
C
B
A
OR ==
Presence of specific US
criteria
+ A B
- C D
Sensitivity is the conditional probability that a
diseased person has a positive result.
Specificity is the conditional probability that
a disease-free person has a negative test result.
Positive Predictive Value (PPV) is the
conditional probability that a person with a
positive test result is truly diseased.
Negative predictive value (NPV) is the
conditional probability that a person with a
negative test result is truly free of the disease.
Accuracy (percent agreement) is the
proportion of true results among all test results
(positive and negative) (12)
RESULTS
As shown in table (1):
The US diagnosis had an overall accuracy
(agreement) of 89% with the final diagnosis. The
US diagnosis was most accurate in periapical
abscess (highest agreement) and least accurate
for mixed lesion (lowest agreement).
J Bagh College Dentistry Vol. 25(Special Issue 1), June 2013 The value of ultrasound
Oral Diagnosis 61
As shown in table (2):
Three US criteria, namely: hypoechoic texture,
avascular pattern, and well defined margin were
tested for their strength of association in
predicting a final diagnosis of periapical cyst
(PAC). The presence of a well defined margin on
US was the strongest criteria among the three
tested. It increased the risk of having PAC by
294 times. Coming second in importance was
hypoechoic texture, which increased the risk of
positive diagnosis of PAC by 69.8 times.
Avascular pattern ranked third in importance. It
increased the risk of having PAC by 24.1%. All
the three tested US characteristics had a
statistically significant association with diagnosis
of PAC
As shown in table (3)
The US criteria, namely: hyperechoic texture,
vascular pattern, and the absence of well defined
margin were tested for their strength of
association in predicting a final diagnosis of
periapical granuloma (PAG). The vascular
pattern on color Doppler US was the strongest
criteria among the three tested. A positive
vascular pattern increased the risk of having
PAG by 266.7 times. Coming second in
importance was hyperechoic texture, which
increased the risk of positive diagnosis of PAG
by 84.4 times. The absence of well defined
margin on US was the least important among the
three. The vascular pattern and hyperechoic
texture on US had a statistically significant
association with diagnosis of PAG, while the
irregularity of the lesion margin did not have
statistical association with the diagnosis of PAG.
As shown in table (4):
Four US criteria, namely: hypoechoic texture,
anechoic texture, avascular pattern, and the
absence of well defined margin were tested for
their strength of association in predicting a final
diagnosis of PAA. The avascular pattern was the
strongest criteria among the four tested, this
increased the risk of having PAA by 80.6 times.
Coming second in importance was the anechoic
texture which increased the risk of having PAA
by 62.7 times. The absence of well defined
margin ranked third in importance that it
increased the risk of having PAA by 29.0, while
the hypoechoic texture did not have statistical
association with the diagnosis of PAA.
As shown in table (5)
Three US criteria, namely: mixed texture
(hypoechoic center and hyperechoic periphery),
mixed vascularity (avascular center and vascular
periphery) and the absence of well defined
margin were tested for their strength of
association in predicting a final diagnosis of
mixed lesion. The mixed texture and mixed
vasculariy increased the risk of having mixed
lesion by 120 times, while the absence of well
defined margin did not have statistical
association with the diagnosis of periapical
mixed lesion.
As shown in table (6):
For periapical cyst (PAC):
Two US criteria had a perfect sensitivity
(100%).These criteria are hypoechoic texture and
avascular pattern which are most useful when
being negative since it can exclude possible
presence of PAC with 100% confidence
(negative predictive value).
The most specific US criterion was a well
defined margin 96.1%.
A well defined margin was also the criterion
associated with highest accuracy (95.3%).
An US diagnosis of PAC had an overall accuracy
of 95.3%, sensitivity of 92.3%, and a specificity
of 96.1%.
As shown in table (7):
For periapical granuloma (PAG):
The most sensitive US criteria was the absence
of well defined margin 91.3% which is most
useful when being negative since it can exclude
the possibility of being PAG with 96.8%
confidence(negative pretest probability).
The most specific US criterion was the vascular
pattern 97.6.
The vascular pattern was also the criterion
associated with highest accuracy (93.8%).
An US diagnosis of PAG had an overall accuracy
of 90.6%, sensitivity of 87% and specificity of
92.7%.
As shown in table (8):
For periapical abscess (PAA):
1. Two US criteria had a perfect sensitivity
(100%).These criteria are the absence of well
defined margin and the avascular pattern which
are most useful when being negative since it can
exclude possible presence of PAA with 100%
confidence (negative predictive value).
2. The most specific US criterion was the
anechoic texture (100%).
3. The anechoic texture was the criterion
associated with highest accuracy (78.1%).
4. An US diagnosis of PAA had an overall
accuracy of 95.3%, sensitivity of 92% and
specificity of 97.4%.
As shown in table (9):
For periapical mixed lesions:
The most sensitive US criteria was the absence
of well defined margin 100% which is most
useful when being negative since it can exclude
the possibility of being mixed PAL with 100%
confidence (negative pretest probability).
J Bagh College Dentistry Vol. 25(Special Issue 1), June 2013 The value of ultrasound
Oral Diagnosis 62
Two US criteria were the most specific. These
criteria were the mixed texture and mixed
vascularity, each criterion had specificity of
98.4%.
The mixed texture and mixed vascularity were
the criteria associated with highest accuracy
(96.9%).
An US diagnosis of mixed PAL had an overall
accuracy of 96.9%, sensitivity of 66.7% and
specificity of 98.4%.
DISCUSSION
Ultrasound is easy, reproducible, and the
equipment is relatively cheap compared to the
other advanced imaging modalities. The images
obtained are easy to read once the observer is
trained. By obtaining a real time image, a
working diagnosis can be made without delay
and it also prevents unnecessary exposure of the
patient to ionizing radiation (8, 13). From a
biological standpoint , in experimental and
clinical studies, no adverse effect of US waves
have been shown to occur in the tissues as a
consequence of echographic examination, and
even if the effect of repeated echographic
examination is less certain, the risks entailed by
radiography are much greater (14,15,16).The
possibility of identifying lesion content before
any surgical procedure can be obtained by using
US examination, using the higher frequency (7.5
MHz) in the technique to increase the signals
penetration of the lesion (17). The current study
used sample size (n=64) and a clear methodology
relating the US diagnostic criteria to final
diagnosis obtained by histopathology and / or
surgical assessment. Allowing for an accurate
reporting of validity parameters of each US
criteria, making the US as an excellent guide for
the surgeon. In the present study four
pathological types of PAL were identified. The
most commonly identified lesion was PAA in
two fifth of the sample (39.1%) followed by
PAG in more than one third (35.9%). Ranked
third in frequency was PAC reported in one fifth
(20.3%) of the sample. A rare finding was a
mixture of periapical cyst and granuloma in only
4.7% of the sample. The US diagnosis in our
study had an overall agreement of 89% with the
final diagnosis based on histopathological and /or
surgical evaluation. The agreement was higher
for PAA (95.8%) compared to PAC and PAG
(85.7% and 87.0% respectively). Dib et al in
1996 in their study on a sample of 72 patients
with intraosseous lesions of the jaws reported an
overall agreement of US ranging between 92.3%
for lesions with solid content, 73.9% for lesions
with liquid content, 92.8% for lesions with mixed
content, and 7.7% for lesions with dense liquid
content. Other pioneer studies based on very
small sample size reached to a conclusion that
US in combination with color Doppler were
sensitive and very useful in differentiating
between PAC and PAG and correlated well with
the histological findings of the PALs; however
no validity parameters were reported because of
the small sample size (16,18,19).
The conclusions that can be drawn from this
study are:
1. This study supported the fact that real time
imaging ultrasound as a new imaging
technique that can be used in endodontic field
for the study of periapical lesions.
2. US is a good diagnostic tool for
differentiation of PALs (cyst, granuloma,
abscess, and cystic cavity within granuloma)
based on ultrasonic selected criteria
including; echo content, vascularity, and
lesion margin.
3. US was highly sensitive in the diagnosis of
PAC (92.3%), followed by PAA (92.0%),
then PAG (87.0%), while the sensitivity of
US diagnosis of mixed PAL was relatively
moderate (66.7%).
4. US was highly specific in the diagnosis of
mixed PAL (98.4%), followed by PAA
(97.4%), then PAC (96.1%), and lastly the
specificity of US diagnosis of PAG was
92.7%.
5. The US diagnosis in our study had an overall
agreement of 89% with the final diagnosis
based on histopathological and /or surgical
evaluation. The agreement was higher for
PAA (95.8%) compared to PAC (85.7%) and
PAG (87.0%), and it was less for mixed
cyst/granuloma periapical lesions (66.7%).
6. The strength of association (OR) was greater
in PAA (437.0) followed by in PAC (294.0)
then in mixed PAL (120) and lastly in PAG
(84.4).
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Table 1: Agreement between US and final diagnosis
Final diagnosis
Periapical
granuloma
Periapical
cyst
Periapical
abscess
Mixed periapical Cyst
Granuloma Total
N
N % N % N % N % N %
U/S diagnosis
Periapical granuloma 20 87.0 0 0.0 2 8.7 1 4.3 23 100.0
Periapical cyst 2 14.3 12 85.7 0 0.0 0 0.0 14 100.0
Periapical abscess 0 0.0 1 4.2 23 95.8 0 0.0 24 100.0
Mixed periapical Cyst
Granuloma 1 33.3 0 0.0 0 0.0 2 66.7 3 100.0
Percent agreement = 89%
Table 2: Strength of association between US criteria and positive final diagnosis of PAC
Total Positive final diagnosis of periapical cyst
N N % OR P 95% CI of OR
U/S diagnosis of periapical cyst
Negative 50 1 2 Ref
Positive 14 12 85.7 294.0 <0.001 (24.6 to 3518.2)
Hypoechoic texture on U/S
Negative 37 0 0 Ref
Positive 27 13 48.1 69.8 <0.001 (8.4 to 578.8)
Avascular pattern
Negative 24 0 0 Ref
Positive 40 13 32.5 24.1 0.003 (2.9 to 196.3)
Irregular lesion margin on U/S
Irregular 50 1 2 Ref
Regular 14 12 85.7 294.0 <0.001 (24.6 to 3518.2)
J Bagh College Dentistry Vol. 25(Special Issue 1), June 2013 The value of ultrasound
Oral Diagnosis 64
Table 3: Strength of association between US criteria and positive final diagnosis of PAG
Total
Positive final diagnosis of periapical
granuloma
N N % OR P 95% CI of OR
U/S diagnosis of periapical
granuloma
Negative 41 3 7.3 Ref
Positive 23 20 87 84.4 <0.001 (15.6 to 457.4)
Hyperechoic texture on U/S
Negative 41 3 7.3 Ref
Positive 23 20 87 84.4 <0.001 (15.6 to 457.4)
Vascular pattern
Negative 43 3 7 Ref
Positive 21 20 95.2 266.7 <0.001 (26 to 2729.8)
Irregular lesion margin on U/S
Regular 14 2 14.3 Ref
Irregular 50 21 42 4.3 0.072[NS] (0.9 to 21.5)
Table 4: Strength of association between US criteria and positive final diagnosis of PAA
Total Positive final diagnosis of periapical abscess
N N % OR P 95% CI of OR
U/S diagnosis of periapical abscess
Negative 40 2 5 Ref
Positive 24 23 95.8 437.0 <0.001 (37.5 to 5093.1)
Hypoechoic texture on U/S
Negative 37 13 35.1 Ref
Positive 27 12 44.4 1.5 0.452[NS] (0.5 to 4.1)
Anechoic texture on U/S
Negative 53 14 26.4 Ref
Positive 11 11 100 62.7 <0.001 (7.5 to 524.4)
Avascular pattern
Negative 24 0 0 Ref
Positive 40 25 62.5 80.6 <0.001 (9.9 to 654.1)
Irregular lesion margin on U/S
Regular 14 0 0 Ref
Irregular 50 25 50 29.0 0.002 (3.6 to 235.9)
Table 5: Strength of association between US criteria and positive final diagnosis of mixed PAL
Total
Positive final diagnosis of periapical
cyst/granuloma
N N % OR P 95% CI of OR
U/S diagnosis of mixed periapical
cyst/granuloma
Negative 61 1 1.6 Ref
Positive 3 2 66.7 120.0 0.003 (5.4 to 2688.8)
Hypoechoic center / hyperechoic
periphery texture on U/S
Negative 61 1 1.6 Ref
Positive 3 2 66.7 120.0 0.003 (5.4 to 2688.8)
Avascular center / vascular periphery
Negative 61 1 1.6 Ref
Positive 3 2 66.7 120.0 0.003 (5.4 to 2688.8)
Irregular lesion margin on U/S
Regular 14 0 0 Ref
Irregular 50 3 6 2.1 0.511[NS] (0.2 to 20.6)
J Bagh College Dentistry Vol. 25(Special Issue 1), June 2013 The value of ultrasound
Oral Diagnosis 65
Table 6: Validity of US criteria for PAC
PPV at pretest probability =
NPV at pretest probability
=
10% Sensitivity Specificity Accuracy 50% 90%
U/S diagnosis of
periapicalcyst
Negative 923 96.1 953 95.9 99.5 99.1
Positive
Hypoechoic texture on U/S
Negative 100 72.5 711 78.4 97.0 100.0
Positive
Avascular pattern
Negative 100 47.1 57.8 65.4 94.4 100.0
Positive
Irregular lesion margin on U/
S
Irregular 92.3 96.1 95.3 95.9 99.5 99.1
Regular
Table 7: Validity of US criteria for PAG
PPV at pretest probability=
NPV at pretest
probability =
10%
Sensitivity Specificity Accuracy 50% 90%
U/S diagnosis of periapical
granuloma
Negative 87 92.7 90.6 92.3 99.1
98.5
Positive
Hyperectoic texture on U/S
Negative 87 92.7 90.6 92.3 99.1 98.5
Positive
Vascular pattern
Negative 87 97.6 93.8 97.3 99.7 98.5
Positive
lrregular lesion margin on U/S
Irregular 91.3 29.3 51.6 56 4 92.1 96.8
Irregular
Table 8: Validity of US criteria for PAA
PPV at pretest probability=
NPV at pretest
probability = 10%
Sensitivity Specificity Accuracy 50% 90%
U/S diagnosis of periapical abscess
Negative 92 97.4 95.3 97.3 99.7 99.1
Positive
Hypoechoic texture on U/S
Negative 48 61.5 56.3 55.5 91.8 91.4
Positive
Anechoic texture on U/S
Negative 44 100 78.1 100.0 100.0 94.1
Positive
Avascular pattern
Negative 100 61.5 76.6 72.2 95.9 100.0
Positive
Irregular lesion margin on U/S
Regular 100 35.9 60.9 60.9 93.4 100.0
Irregular
J Bagh College Dentistry Vol. 25(Special Issue 1), June 2013 The value of ultrasound
Oral Diagnosis 66
Table 9: Validity of US criteria for mixed PAL
PPV at
pretest
probability=
NPV at
pretest
probability=
10%
Sensitivity Specificity Accuracy 50%
90%
U/S diagnosis of mixedpenapical cyst granuloma
Negative 66.7 9S.4 96.9 97.7 99.7 96.4
Positive
Hypoechoic center hyperechoic periphery texture on
U/S
Negative 667 98.4 96.9 97.7 99.7 96.4
Positive
Avascular center vascular penphery
Negative 66.7 93.4 96.9 97.7 99.7 96.1
Positive
Irregular lesion margin on U/S
Regular 100 23 26.6 56.5 92.1 100.0
Irregular