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Ultrasound real-time imaging in the differential

diagnosis of periapical lesions

E. Cotti1, G. Campisi2, R. Ambu3 & C. Dettori1


1
School of Dentistry, Department of Conservative Dentistry and Endodontics, University of Cagliari, 2Department of Radiology,
Hospital `G. Brotzu' Cagliari and 3Department of Pathologic Anatomy, School of Medicine, University of Cagliari, Cagliari, Italy

Abstract and a granuloma was made. The lesions obtained during


endodontic surgery were processed and examined with
Cotti E, Campisi G, Ambu R, Dettori C. Ultrasound real-
a light microscope. The results from the biopsies were
time imaging in the differential diagnosis of periapical lesions. Interna-
compared with the descriptions made with the ultra-
tional Endodontic Journal, 36, 556^563, 2003.
sound images.
Aim To assess whether the use of real-time ultrasound Results The di¡erential diagnoses between periapical
imaging (echography), together with the application of granulomas and cystic lesions, which were based on
`Colour Power Doppler', can help the di¡erential diagno- the echograpic ¢ndings, were con¢rmed by the results
sis of periapical lesions based on their contents. of the histopathologic examination in all the 11 cases:
Methodology Eleven patients diagnosed with peria- four being granulomas and seven being cystic lesions.
pical lesions using conventional clinical and radio- Conclusions Ultrasound real-time imaging is a tech-
graphic ¢ndings and who had been scheduled for nique that may help make a di¡erential diagnosis
endodontic surgery were examined using ultrasound between cysts and granulomas by revealing the nature
imaging and Colour Power Doppler at the site of the of the content of a bony lesion. This technique may have
lesions. Lesions were described in each case byan expert further applications in the study of other lesions of the
echographist, together with an endodontist, according jaws.
to a scheme described previously. Information on the size
Keywords: echography, endodontic diagnosis, peria-
of each lesion, its content and its vascular supply was
pical lesions.
gained and recorded by means of the ultrasound images;
then, a tentative di¡erential diagnosis between a cyst Received 3 May 2002; accepted10 April 2003

(Priebe et al. 1954). The possibility of distinguishing


Introduction
between a true cyst and a granuloma may be of help in
Imaging techniques are essential in endodontics, espe- predicting treatment outcome (Nair 1998). Direct digital
cially for the study of periapical lesions, and it is impor- radiography is not better than conventional radiography
tant that new and more promising techniques are in the detection and measurement of periapical lesions
constantly being evaluated (Òrstavik & Pitt-Ford 1998). (Scarfe et al. 1999). Computerized tomography (CT) has
Conventional radiographic procedures have limita- been suggested as a noninvasive method that could be
tions in that they do not reliably demonstrate the pre- used to make a di¡erential diagnosis between a cyst
sence and size of the lesions in bone (Bender & Seltzer and a granuloma (Trope et al.1989) and to manage exten-
1961, van der Stelt 1985). Also, they do not allow the dif- sive lesions (Cotti et al. 1999), but routine use of CT is
ferential diagnosis between cystic and noncystic lesions associated with high radiation risks (Dula et al. 1996).
Real-time ultrasound imaging (echography) is widely
used in medicine: it is based on the phenomenon of the
Correspondence: Elisabetta Cotti, via Roma149, Cagliari 09124, re£ection of ultrasound (US) waves (echoes) at the inter-
Italy (Tel.: ‡39 070 662710; fax: ‡39 070 659689; e-mail: faces betweentissues that have di¡erent acoustic proper-
cottiend@tin.it). ties.

556 International Endodontic Journal, 36, 556^563, 2003 ß 2003 Blackwell Publishing Ltd
Cotti et al. Echography in endodontics

`Hypoechoic' or `transonic' is a given area with low been diagnosed with a periradicular lesion of endodontic
echo intensity; `anechoic' is an area where there is no origin based on clinical signs and symptoms (Trope
re£ection of echoes (i.e. any area ¢lled with £uids) and et al. 1998) and both intraoral and panoramic radio-
`hyperechoic' is an area that shows high echo intensity. graphic ¢ndings. The patients were scheduled to be trea-
Bone exhibits total re£ection (hyperechoic/echogenic), ted in the Department of Conservative Dentistry and
and this is the reason why US imaging can only be per- Endodontics at the University Clinic in Cagliari, and
formed through bone windows/lesions. Areas that con- the treatment plan included endodontic surgery with
tain di¡erent types of tissues show a `dishomogeneous apicoectomy, retrograde ¢lling and biopsy for each case.
echo' (Auer & VanVelthoven 1990). Patients who agreed to take part in the study were asked
The application of Colour Power Doppler ultrasound to sign an informed consent form before undergoing
to the echography o¡ers an opportunity to evaluate the echographic examination. The area of diagnostic
and determine the presence, direction and velocity of interest in the mouth was selected for the echography.
blood £ow within the ultrasound image of the examined The ultrasonic probe, covered with an insulating latex
tissue. Colour Power Doppler gives a colour-coded repre- glove ¢nger, was positioned on the buccal sulcus of the
sentation of the Doppler signal and its time modi¢cation maxillary bones corresponding to the apical area of the
(Fleischer & Emerson 1993). tooth of interest inside the mouth. Subsequently, it was
The use of real-time ultrasound examination for the placed outside the mouth in the corresponding external
evaluation of bone lesions of endodontic origin has been area. The tissues to be examined were covered with a
assessed recently and reported (Cotti et al. 2002). The layer of echographic gel (Aquagel, HP, Palo Alto, CA,
purpose of this study was to evaluate whether it is possi- USA). The probe was put in contact with the tissue and
ble to make a di¡erential diagnosis between periapical then moved slightly in order to obtain an adequate num-
lesions with di¡erent histopathologic features based on ber of transversal scans (approximately four) to de¢ne
echographic study. the bony defect. Colour Power Doppler was applied to
each examination.
For each lesion, a representative echographic image
Materials and methods
was selected; it was saved in a magneto-optical disk
(Eastman Kodak, Rochester, NY, USA) and analysed by
Echographic examination
an expert echographist together with an endodontist.
Echographic examinations of periapical lesions were A report was described in a chart (Cotti et al. 2002),
completed using an Elegra Siemens apparatus with a and a tentative di¡erential diagnosis between a cystic
regular-size, linear, high-de¢nition, multifrequency lesion and a granuloma was agreed based on the follow-
ultrasound probe (Siemens, Erlangen, Germany) at a fre- ing principles:
quency of 7^9 MHz. The examinations were performed  Cystic lesion: a transonic (hypoechoic) well-contoured
by an expert echographist along with an endodontist. cavity, surrounded by reinforced bone walls, ¢lled
Eleven Caucasian patients, aged between 25 and with £uids and with no evidence of internal vascular-
50 years, were selected for the study. The patients had ization on Colour Power Doppler examination.

Table 1 Classi¢cation of data relative to


PT. AGE SEX TOOTH DIAG. CL ‡ RX DIAG. ECHO DIAG. HISTO
periapical lesions, clinical, radiographic,
ecographic and histopathologic 1 67 M 33 PAL PAC PAC
diagnosis 2 46 F 33 PAL PAC PAC
3 39 M 12 PAL PAC PAC
4 28 F 15 PAL PAC PAC
5 57 M 11 PAL PAC PAC
6 35 M 44 PAL PAC ‡ PAG PAC ‡ PAG
7 52 F 41^31 PAL PAC PAC
8 64 F 21 PAL PAG PAG
9 32 F 26 PAL PAG PAG
10 39 M 21 PAL PAG PAG
11 37 F 21^22 PAL PAG PAG

PT. ˆ Patient; DIAG. CL ‡ RX ˆ diagnosis: clinical and radiographic; DIAG. ECHO ˆ diagnosis:
ecographic; DIAG. HISTO ˆ diagnosis: histopathologic; PAL ˆ periapical lesion; PAC ˆ periapical
cyst; PAG ˆ periapical granuloma.

ß 2003 Blackwell Publishing Ltd International Endodontic Journal, 36, 556^563, 2003 557
Echography in endodontics Cotti et al.

Figure 1 (a) Panoramic radiograph showing a lesion involving the periradicular area of the tooth 33 (arrowed). (b) Echotomogram
(ultrasound image) showing a`transonic lesion' (arrowed) with well-de¢ned and reinforced contours (the dotted line indicates the
major diameter of the lesion). (c) The microphotograph of one of the sections of the lesion shows a cystic cavity lined by epithelium
(arrowed) (H&E 2). (d) Microphotograph of a detail from the previous lesion showing the strati¢ed squamous epithelium
(arrowed) (H&E 40).

558 International Endodontic Journal, 36, 556^563, 2003 ß 2003 Blackwell Publishing Ltd
Cotti et al. Echography in endodontics

Figure 2 (a) Panoramic radiograph showing a lesion (arrowed) in the periapical area corresponding to the teeth 42, 41and 31. (b)
Echotomogram of the same lesion showing a well-contoured transonic lesion (short arrow), containing scattered echogenic
particles (long arrow). (c) The histomorphology of this periapical lesion shows a strati¢ed squamous cyst lining with several goblet
cells (arrow) (H&E 40).

ß 2003 Blackwell Publishing Ltd International Endodontic Journal, 36, 556^563, 2003 559
Echography in endodontics Cotti et al.

 Granuloma: a poorly de¢ned lesion, which could be


Results
frankly corpusculated (hyperechoic/echogenic) or
could show both corpusculated and hypoechoic The results are summarized in Table 1.
areas, exhibiting a rich vascular supply on Colour
Power Doppler examination.
Echographic examination
Images of the periradicular lesions were obtained easily
Surgical endodontics
and identi¢ed in all the cases using both the intraoral
In all the11clinical cases, surgical endodontics was per- and extraoral procedures.
formed according to Arens et al. (1998). The lesions col- The echographic study showed the presence of seven
lected were stored in 10% bu¡ered formalin and sent lesions, ¢ve of which (from 1 to 5) were frankly hypoe-
for histopathologic examination. choic with well-de¢ned contours and which with Colour
Power Doppler did not show evidence of internal vascu-
larization. These cases were diagnosed as periapical
Histopathologic examination
lesions with cystic appearance (Fig. 1a,b).
After ¢xation in 10% bu¡ered formalin, the surgical Of the remaining two lesions, one (lesion 6) exhibited a
specimens were routinely processed for histology round shape, with interruption of the bone pro¢le and
by an automated histoprocessor (Ventana Medical an echostructure that was described as `mixed' because
Systems, AZ, USA), dehydrated through a graded it showed a content that was both hypoechoic (inthe cen-
series of ethanol and in¢ltrated by para¤n. The tre and toward the mesial side of the associated root)
specimens were then embedded by an embedding and hyperechoic (in the surrounding areas).With Colour
centre (Especialidades Medicas, Cunit, Tarragona, Power Doppler, a rich vascularization was observed on
Spain) and semiserially sectioned with a microtome the external area of the lesion. This lesion was diagnosed
(model Top Rotary S-130, Pabish, Milano, Italy). Sections as a periapical granuloma with a £uid-¢lled cavity
were then mounted on glass slides, which were inside. The 7th lesion showed a regular oval shape, with
stored at 36 8C for 1 h and passed through a descend- well-de¢ned contours, reinforced bone walls and no evi-
ing concentration of alcohol in order to have the dence of vascularization at the Colour Power Doppler.
para¤n removed. The sections were subsequently The content within this lesion was mostly hypoechoic,
stained with haematoxylin and eosin, covered with a but, unlike the others of the same kind, it showed small,
coverslip by a synthetic mounting glue (BioMount, scattered echoes as if it was a £uid with dense particles.
Byo-Optica, Milano, Italy) and observed on a light This lesion was diagnosed as a periapical lesion with cys-
transmission microscope (Axioskop, Zeiss, Gottingen, tic appearance and a prominent secretory content
Germany). (Fig. 2a,b).
Immunohistochemistry was carried out for one of The remaining four lesions exhibited a rounded shape
the specimens: slides that had been pretreated with only partially de¢ned. In two of the cases, an interrup-
polylysin were used; the sections were processed to test tion of the bone pro¢le was observed on the right side;
for human polyclonal cytokeratins (Biogenex, San the echostructure of these lesions showed a content that
Ramon, CA, USA) using a dilution of1 : 50.The immunor- was both hypoechoic and hyperechoic. The content of
eactions were enhanced by means of the streptavidin- the other two lesions was frankly echogenic (hypere-
biotin-peroxidase technique with a rabbit antihuman choic). On Colour Power Doppler examination, all these
antibody followed by a counterstaining with Mayer's four lesions showed a vascularization that varied from
haematoxylin. rich to scattered.
The evaluation of the histological sections was com- All of these were classi¢ed as periapical granulomas
pleted in a blind manner. (Fig. 3a,b).

Figure 3 (a) Panoramic radiograph showing a lesion (arrowed) in the periapical area of the tooth12. Tooth12 was diagnosed with
vertical crown-root fracture and was extracted during the surgery. (b) Echotomogram of the same lesion (in the square) that
presents a round lesion (black arrow in the upper and lower contours), with an echogenic and mixed content (white arrow) and
vascular supply (blue spots; the yellow and red spots are the result of a twinkling artefact of the Colour Doppler). (c) The
histopathologic picture of this lesion is characterized by a highly vascular, oedematous connective tissue with abundant mixed
in£ammatory cells in¢ltrate (H&E 25).

560 International Endodontic Journal, 36, 556^563, 2003 ß 2003 Blackwell Publishing Ltd
Cotti et al. Echography in endodontics

ß 2003 Blackwell Publishing Ltd International Endodontic Journal, 36, 556^563, 2003 561
Echography in endodontics Cotti et al.

All six cases in which the ultrasound images showed a


Histopathologic report
well-contoured area with a transonic content and where
The results from the histopathologic examination con- the Colour Power Doppler did not show the presence of
¢rmed the echographic observations: the lesions from 1 vascularization were described as epithelial lined cav-
to 5 were diagnosed as cystic lesions and showed the pre- ities following histopathologic observations. The four
sence of a cavity lined with strati¢ed squamous epithe- cases in which the ultrasound images displayed lesions
lium. Within the lumen of the cavity, necrotic debris in which contours were not regular with an echogenic
and numerous impressions from cholesterin crystals or mixed content and a widespread blood £ow were
were seen (Fig. 1c,d). described as periapical granulomas from a histological
The histopathologic examination of lesion 6 showed a standpoint. Two cases demonstrated the sensitivity of
widespread granulomatous tissue containing an area this diagnostic technique. In lesion 6, the ultrasound
of strati¢ed squamous epithelium that lined a lumen. examination with Colour Power Doppler displayed all
The immunohistochemical staining for cytokeratins possible elements: echogenic content, rich vascular sup-
applied to this case con¢rmed the previous observations ply and a transonic area. The tentative diagnosis of a
on the epithelial lining. mixed cystic and granulomatous lesion was supported
The examination of lesion 7 showed a cavity with a by the histopathologic report that showed an extensive
lumen lined by a squamous epithelium presenting areas granulomatous lesion containing a smallercavity, which
of cylindrical ciliated cells and several goblet cells was completely lined by epithelium. The lesion in case
(Fig. 2c). 7 exhibited a well-contoured shape, and its content
The histopathologic reports on lesions 8^11 consis- appeared to be hypoechoic as if ¢lled with a £uid that
tently described a typical granulomatous appearance: had some small particles inside. During the surgical exci-
connective tissue with widespread areas of PMNs, lym- sion of this lesion, there was a dense, yellowish secretion.
phocytes, monocytes and newly formed blood vessels The histomorphology of this periapical lesion showed a
(Fig. 3c). cavity lined by a secretory epithelium, which was an
unusual occurrence.
Discussion
Conclusions
The results from preliminary investigations sugges-
ted that ultrasound real-time imaging was an easy Based on the results of this and previous work (Cotti et al.
and reproducible examination that could become a 2002), real-time ultrasound imaging can be considered
useful adjunct to conventional radiography in the a new imaging technique that can be used in the
management of extensive periapical lesions, as it endodontic ¢eld for the study of periapical lesions.With
provides speci¢c information on the size of the lesion real-time ultrasound observation, it is also possible to
(Cotti et al. 2002), it has few risks and the images are determine the histopathologic nature of the lesion: cystic
obtained in digital form that are easy to read, store and versus granulomatous by examining its shape and its
reproduce. echo content, and by applying Colour Power Doppler to
From a biological standpoint, in experimental and provide evidence of its vascularization. Future research
clinical studies, no adverse e¡ects of ultrasound waves in the multiple di¡erential diagnoses of bone lesions of
have been shown to occur in the tissues as a conse- the jaws is suggested.
quence of echographic examination (Baker & Dalrymple
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