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CHOLANGIOCELLULAR CARCINOMA:
PATHOLOGICALi ULTRASONOGRAPHIC AND
ANGIOECHOGRAPHIC CORRELATIONS
Rozalinda POPOVA-JOVANOVSKA, Akiko SAITO, Ken TAKASAKI,
Masakazu YAMAMOTO and Naoaki HAYASHI
Department of Gastroenterology (Director: Prof. Naoaki HAYASHI), lnstitute of Gastroenterology,
Tokyo Women's Medical College (Received September, 24, 1993)
Correlations were sought among histopathologic, ultrasonographic (US) and angio-echographic findings in 27 resected cholangiocellular carcinoma (CCC) cases. According to macroscopic appearance, CCC was classified into three types: nodular, periductal and intraductal. This classification was accepted because clinico-pathological features, as well as prognosis, differed among tumor types. A tumor mass was clearly visible in nodular type tumors. Of the 20 nodular cases, 17 were large tumors and 3 were small (less than 3 cm). The large tumors were ill-defined (70%), showed a hypoechoic rim (65%), had an echo pattern which tended to be more echogenic and were associated with bile duct dilatation (59%). Vascular structures within the tumor were of importance as US characteristics of CCC. Portal tract passing through the tumor (23%), disappearing portal tract (29%) and the "Vessel like structures" sign (53%) were recognized only in the large tumors. Small nodular type tumors had a hypoechoic or isoechoic echo pattern with no other significant US findings. Tumor mass could not be identified or was poorly visualized in periductal and intraductal type CCC. A disappearing portal tract sign was noted in four, while bile duct dilatation was seen in all five periductal type cases. Two cases had intraductal type CCC. Tumor mass filling the bile duct was seen in one case. These tumors showed the most marked bile duct dilatation. Examination of microscopic specimens revealed predominantly tumor cells in the periphery of 20 nodular type tumors, which on US were visualized as a hypoechoic rim (55%). Central dense fibrotic tissue areas were associated with increased echogenicity on US, 76% of which were
hyperechoic or isoechoic, while 24% were hypoechoic. Certain US findings were
characteristic of mucinous carcinoma and hemangioma like tumor.In addition, angioechography was performed in 9 of these CCC cases. After C02 injection, three angioechographic patterns were discernible, peripheral enhancement in three cases, whole tumor enhancement in four cases and partial tumor enhancement in two cases. There was a tendency for the angioechographic pattern to change from whole to peripheral enhancement as the tumor increased in size. Pathological examination showed that the areas with tumor cell predominance correlated with positive enhance-ment, whereas areas with dense fibrotic tissue correlated with non or negative enhancement. Pathological, US and angioechographic comparisons contribute to under-stand the significance of the different US and angioechographic appearances of CCC.
Introduction
According tQ "The General Rules for the
Clini-cal and PathologiClini-cal Study of Primary Liver
Cancer" issued by "The Liver Cancer Study
Group Japan" 1992i), cholangiocellular carcinoma (CCC) is regarded as a primary liver cancer when the tumor originates from the epithelium of an intrahepatic bile duct. However, tumors arising from the right and left hepatic duct and hilumcarcinoma are excluded, although most other
classifications include them2). CCC is a relatively
uncommon djsease, constitutjng 9.5 percent of all
malignant hepatic tumors2). It shows a wide
spectrum of appearances on ultrasonography
(US)3}N5}, computed tomography (CT)6)]'), angio-graphy8> and magnetic resonance (MR)9}. Con-sequently, many aspects of diagnostic imaging for CCC remain to be elucidated. To date, few detailedreports have appeared in the literatureiO)Ni3}.
In order to correctly assess the US findings of CCC, a detailed study of the histology of the resected specimen was perforrned. There have been reports concerning 'correlations between the
histopathology and US patterns of hepatic
tumorsi4)Ni6). One such report focused oncorrela-tions in CCCi7>. The present study however
includes pathological examination of the gross appearance of a tumor as well as its histomor-phologyi8}N22). A number of ultrasonographic fea-tures of CCC were correlated with pathologic
findings.
In addition, angioechography is introduced as a
diagnostic modality and its significance for CCC is
reviewed and discussed. Angioechography, used as a supplementary imaging modality to conven-tional US, can enhance tumor diagnosis by
de-tecting tumor vascularity23)'"27). Angioechographic
patterns were correlated with histopathologic
findings obtained at hepatic resection.
This study was designed firstly, to understand the different appearances of CCC on conventional
US and to clarify various structural details within
the tumor. In particular, attention was given to the presence of the portal tract and vascular
structures within the tumor detectable by US, which have not previously been described. The second aim was to provide additional considera-tions for diagnosing CCC by angioechography.
Subjects and Methods
A retrospective review was made of 27 cases of histologically proven CCC resected from Novem-ber 1986 through March 1993. In accordance with an accepted classification systemi>, the term
cholangiocellular carcinoma was applied to
tumors located in an intrahepatic bile duct. Pa-tients with right and left hepatic duct carcinoma, hilar carcinoma and extrahepatic bile duct car-cinoma were excluded from the study. There were 16 males and 11 females, for a ratio of 1.5:1. Age ranged from 38 to 75 years, with a mean of 59. All 27 patients underwent hepatic resection. Precise pathological review was achieved by detailed macroscopic and microscopic inspection of a series of 10 to 15 specimens of the tumor. Consensus was based on the histopathological findings and US patterns of each CCC tumor.Ultrasonic examinations were performed with either a convex or a sector array electronic scan-ner with a 3.5 MHz transducer (SSA 270 Toshiba, Tokyo, Japan, RT-3600 Yokogawa, Tokyo, Japan).
Grouping of the 27 cases was based on the
macroscopic appearance of the tumor. Macrosco-pically, CCC was classified into three types:. nodular, periductal and intraductal according the anatomical location and growth pattern of the
tumor20).
1. Nodulartype;tumoroccursinanintrahepatic
small bile duct and upon infiltrating the liver parenchyma forms a nodular mass. The nodule is not encapsulated and in some instances iscon-tinuous with the wall of the bile duct (Fig. Ia, b).
2. Periductal type; tumor invades along the
course of a bile duct with abundant fibrosis, producing a sclerosed mass, resulting in wall
thickening and a stricture like lesion. Spread into
the surrounding liver parenchyma generally
occurs and the tumor mass may be seen around
the obstruction <Fig. Ic).
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ge･{ ･ eqv'ww/ilSE'' Fig. 1 Surgicalspecimensofcholangiocellularcarcinoma(a) Large nodular type. Tumor mass is seen in the right lobe of the liver. (b) Small nodular type, tumor measured 1,5 cm. (c) Periductal type, tumor mass along the bile duct wall resulting in wall thickening and narrowing. (d) Intraductal type, with a tumor mass filling the bile duct and marked bile duct dilatation.
3. Intraductal type; tumor shows intraductal-growth filling the lumen, and slight involvement
of the surrounding liver parenchyma (Fig. Id).
According to the above classification, detailed examination of the US appearance of a CCC was reviewed for each tumor type. The study included tumor appearance and structural details within
the tumor and surrounding liver parenchyma.
Furthermore, areas of special interest were the portal tract and vascular structures inside the tumor visualized by US and corresponding find-ings detectable with the naked eye on macroscopic speclmens.Correlations between US and microscopic find-ings were considered separately. Histological
ex-amination of microscopic specimens included
identification of various tumor components in
different parts of the tumor as well as the
histo-logical type.
Among the 27 CCC cases, 9 with nodular type
underwent preoperative angioechography exami-nation, and of these 7 were histologically
diag-nosed as having tubular adenocarcinoma, One
tumor was a mucinous carcinoma and another
had some hemangioma like histological features. The diagnostic method employed was a combina-tion of convencombina-tional angiography and ultrasound. Following conventional, superselective hepatic angiography or digital subtraction angiography (DSA) with the catheter placed in the proper hepatic artery, 5-10 ml of C02 gas was given in a bolus injection directly into the hepatic artery. Under continuous US monitoring, C02 gas flow was observed entering the tumor and surrounding liver parenchyma until it had been washed out. Angioechographic examination included estima-tion of the angioechographic pattern, duraestima-tion of contrast enhancement in the tumor andResults
There were 20 nodular, five periductal and two intraductal CCC cases. Corresponding US find-ings for each tumor type are summarized in Table
1. Macroscopic and US appearances of CCC
tumors'are shown in Figures 1 and 2.
Nodular Type
Among the 20 nodular cases, 17 were designated as large nodular type with sizes ranging from 3 to 12 cm in diameter. The margin was ill-defined and irregular in 12 tumors (70%), while a hypoechoic
rim sign was seen in 11 tumors (65%). Echo
patterns differed depending on tumor size, large tumors tending to be more echogenic. Seven nod-ules (41%) had hyperechoic echo patterns, four (23%) were isoechoic and five (29%) were hypo-echoic. A strong echo with an acoustic shadow within the tumor mass was found in four cases. Portal tract and vessel like structures within the tumor appeared as:-Portal tract passing completely through the tinmor (Fig. 3a). This was observed in four cases. No irregularity apart from slight compression was
noted along the portal tract.
-Disappearing portal tract (Fig.' 3b). Portal
tract (second or third ramifying branches) can be seen up to the tumor site or slightly inside the tumor and then cannot be distinguished. Five
nodular type cases had a disappearing portal tract,
in two of which the portal tract could be followed only up to the tumor site while in the other three it could be followed part way inside the tumor and
then could not be seen. ･
-Vessel like structure (Fig. 3c). Hyperechoic linear area without an acoustic shadow. These findings were seen as double hyperechoic parallel linear structures of varying thicknesses, 4 to 10
mm in length. Since･these structures were
thought to most closely resemble vessels the author has referred to them as "vessel like struc-tures". These findings were seen in 9 (53%) of the large nodular type cases but in no other type of
CCC.
Bile duct dilatation was recognized in 10 (59%)
large type nodules.
Three tumors were less than 3 cm in diameter. The margin was ill-defined in two cases (67%). No
hypoechoic rim was seen. Two tumors showed
hypoechoic (67%) and one a isoechoic pattern
(33%). Associated bile duct dilatation was observed in one case (33%).
Table 1 Characteristics of CCC on US
lmagmg
Gross appearance
Nodular Periductal Intraductal
large small
n=17
n=3
n=5
n=2
Nodularmass 17(100%) 3.(100%) 3(60%) o(o%)
III-definedmargin 12(70%) 2(670%) s(looo/.) 2aooo/.)
Hypoechoicrim 11(65%) o o o Echopattern Hyperechoic 7(41%) o o o Isoechoic 4(23%) 1(33%)' 5(100%) 2(looo/o) Hypoechoic 5(29%) 2(670/.) o o StrongechowithAS. 4(230/.) e o o Portaltractwithintumor PTpassingthrough tumor 4(23906o) o o o DisappearingPT 5(29%) o 4(800%) 2(100%) Vessel-likestructure withintumor 9(530%) o 0 o
Bileductdilatation lo(sgo/,) 1(330/o) s(looo/.) 2(looo/o)
AS : acoustic shadow, PT : portal tract.
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,,,i,kSieewli,lk ljegligl,agilw. ua ev es ge tw""Ftitl .}.".ts,iYas,mp, twge .AigtrEFig. 2 Ultrasonographic appearance of different types cholangiocellular carcinoma
(a) Large nodular type: echogram shows an ill-defined hyperechoic tumor with peripheral hypoechoic rim (arrows), (b) Small nodular type: hypoechoic nodule in the posterior segment of the liver (arrow). (c) Periductal type with portal tract narrowing and slight proximal bile duct dilatation. Tumor mass site (arrows) (d) Intraductal type marked bile duct dilatation in the right lobe. Bile ducts end abruptly at the tumor site (arrows).
Periductal Type
Of the 5 periductal type cases, three had poorly
identified isoechoic tumor masses. Two showed no tumor mass around the site of the lesion. The echo pattern of the tumor was generally isoechoic but was recognizable because of a slight irreg-ularity of the liver parenchyma. Tumor presence
was associated with moderate bile duct dilatation,
proximal to the stricture. Associated adjacent dilatation of the bile duct was noted in all five
cases. As to the portal tract, US revealed localized disappearance of the portal tract in four cases. In
one case, this sign was associated with clearly demonstrated narrowing and irregularity of the
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Fig. 3 Vascular structures inside the tumor
``Disappearing portal tract"
the lesion area (arrow). (c) "Vessel-like structures
acoustic shadow (arrows).
ge "masnv(
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･.eeww
.f.,ise"ge "tnge.wwpame " af:'It"(a) Portal tract passing through the turnor (arrow). A large portal tract is surrounded by tumor mass, (b)
, portal tract can be seen up to the tumor site but cannot be distinguished in ", hyperechoic double parallel linear findings without an
adjacent bile duct.
Intraductal Type
Two cases of the tumors were intraductal type CCC. One case showed an intraluminal echogenic mass without an acoustic shadow. Disappearance
of the portal tract and proximal bile duct
dilata-tion were seen. The other case presented marked
bile duct dilatation and points at which the bile ducts ended defined the tumor location, although the tumor mass itself could not be seen. Atrophy of the live parenchyma in the involved segment
was noted in one patient.
Histological-US Correlation
Correlations between histological and US
find-Table 2 Pathologic-US correlations
Pathologic examination Corresponding US findings
Tumor margin
Infiltrative growth
(no capsule formation) n=27 margmIrregular ill-defined 21(78%)
Tumor mass Marginalarea-tumor cellpredorninance n=20 Hypoechoicrim 11(55%) Centralarea-dense fibrotictissue n=21 Echopattern: Hyperechoic Isoechoic Hypoechoic 7(330/.) 9(430/o) 5(240/.) Extensiveareasof.mucln n=1 Hypoechoicpattern 1 Additional findings Abscessformation
withdebris n=1 Strongechowithacousticshadow 1
Hemangiomalike
structure n=1
Inten.sehyperechoic
pattern 1
ings are shown in Table 2.
Lack of capsule formation and infiltrative type growth on US indicated ill-defined tumor bound-aries and an irregular margin. Fourteen of the 20 nodular type tumors and all of the periductal and
intraductal type tumors showed ill-defined
margins (78%), while the remaining six nodular
type tumors showed relatively well-defined
margins. As to tumor components, tumor cells were predominant in the peripheral area of
nod-ular type tumors. On US the same area was
visualized as a hypoechoic rim in 11 (55%), a finding which defined the iarge nodular type
tumors. A hypoechoic rim was seen in seven
hyperechoic tumors and four isoechoic tumors. The large nodular and periductal type tumors
contained central dense fibrotic tissue with islets
of tumor cells and a few small areas of necrosis. These histopathological patterns were related to increased echogenicity on US. A hyperechoic echo pattern was present in seven (33%) out of 21 tumors and nine (43%) tumors had an isoechoic pattern while five tumors showed a hypoechoic
echo pattern. Small tumors, less than 3 cm in size,
revealed islets of tumor cells scattered in the scanty fibrotic stroma and therefore appeared on US as isoechoic or hypoechoic. The case with mucinous carcinoma showed a well-defined hypo-echoic tumor on US. The mucin component
corre-Angioechographic
sponded to the hypoechoic area.
CCC associated with abscess and debris mate-rial appeared on US as a strong echo with an acoustic shadow, and was therefore interpreted as a stone. One case had unusual histopathological findings. Part of the tumor contained dilated vascular spaces lined with tumor cells and resem-bled hemangioma. This area on US was described as hyperechoic and was suggested to be heman:
gioma while the other part of the tumor was
hypoechoic.Angioechographic Examination
Basically, the angioechographic patterns of nod-ular type CCC can be divided into three groups according to enhancement features (Fig. 4). -peripheral enhancement-the peripheral area of the tumor is markedly enhanced, while the central portion reveals non or negative enhance-ment.
-whole tumor enhancement-homogeneous
enhancement of the entire tumor with the grade of
intensity ,varying according to the tumor type.
-partial enhancement-only a portion of the
tumor is enhanced.The appearance of the nine CCC cases
exa-mined by angioechography differed according to tumor size as well as the various tumor com-ponents. Summarized data are presented in Table
pattern of CCC
Peripheral enhancement
n=3
Whole tumor enhancement
n=4
Partial enhancement
n=2
M intensely enhanced area
[l$llil talnt enhancement
BIiiSSg non i negative enhancement
Fig. 4 After C02 injection, three angioechographic patterns of cholangiocellular carcinoma
Table 3 Tumor size-angioechographic pattern correlations
Tumor les'ion Angioechographic appearance Tubular adenocarcinoma
<3cm
3--5 cm>5cm
n=2
n=2
n=3
1×2
3
Partial enhancementWhole tumor enhancement
Peripheral enhancement
Mucinous carcinoma
>5 cm
n=1
1
Faint whole tumor enhancement Hemangioma'like tumor
>5 cm
n=:r1
Partialenhancement3.
There were seven tubular adenocarcinomas two of which were small and differed in angioecho-graphic findings. One showed an enhanced central area within the tumor despite most of the tumor being non-enhanced, while the other revealed
homogeneous intense positive enhancement
throughout the tumor. Two other tubular adeno-carcinomas, from 3 to 5 cm in size, showed whole
tum,or enhancement. Enhancement intensity
varied in degree but was roughly homogeneous. Three cases larger than 5 cm, showed predom-inantly marked enhancement of peripheral areas immediately after C02 injection. The peripheral rim was characteristically thick with intense enhancement. This was in contrast to the sur-rounding liver parenchyma, thus clearly defining the tumor margin which is usually ill-defined.
Inside the tumor, only some spotty enhanced
areas were .seen.
The two remaining cases, in which tumor size exceeded 5 cm had characteristic histomorpho-logic features which reflected the angioechogra-phic appearance. Angioechography of the muci-nous carcinoma revealed entirely heterogeneous faint tumor enhancement and a thin peripheral enhanced rim. Following C02 injection, the hy-perechoic portion of the tumor with a
hemang-ioma like structural component was markedly
enhanced, making the tumor thereby appear
par-tially enhanced.
Wash-out Time
Hemodynamic assessment during an
angio-echographic procedure is a useful additional parameter. Following C02 injection, a CCC im-mediately shows one of the three patterns pre-viously described, i.e. peripheral enhancement,
whole tumor enhancement or partial
enhance-ment with progressive clearing of the C02 con-trast. Three CCC tumor cases had an adequately
measured washLout time. The results were 10
min., 10 min. and 15 min for each tumor,regard-less of tumor size.
Angioechographic-Pathologic Correlations
Results are summarized in Table 4. The corre-lations between angioechographic patterns and the histopathology of resected sPecimens showed that tumor areas with dense fibrotic tissue'
ther entire tumors or parts of the tumor, corre-sponded to the absence of enhancement. These79 -Table 4 tions Pathologic-angioechographic correla-Pathologicexamination Gradesof enhancement
-
+-Densefibrotictissuen=5
Tumorcellpredominancen=6
5 1 5Mucincomponentn=1
Hemangioma-likestructuren=1 1 1 -:non/negative enhancernent, +: H+ : positive enhan￠ement. faint enhancement,a
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b Fig．5 （a）Microscoplc findings Al Dense central fibrotic tlssue， Bl The perψheral area shows predomln− ance of tumor cells，C：Normal liver parenchyma．（b）Angioechogram A：Non enhanced central portion of the tumor， B：Thick intensively enhanced peripheral rim， C：Non enhanced surrounding hver parenchyma， b Fig．6 （a）Microscopic findings Small tubular adenocarclnoma with predominance of tumor cells and scanty fibrotic tissue．（b）Angioechogram Entire intensive homogeneous tumor enhancement（arrow）．a
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Fig. 7
(b) Faint tumor enhancement and thin peripheral hyperechoic rirn (
(a) Mucinous carcinoma with islets of tumor cells and large mucinous lakes.
arrows).
b a '1ts: ttz-ts,ua-ex.:trw'ma: triki,llgs'-agtwdemp "< di, eqxx:xvatwerlj￠di$ Fig. 8 Hemangioma-liketumor(a) Portion of the tumor shows dilated vascular spaces lined with tumor cells, Showing intense enhancement in the area of dilated vascular spaces (arrows).
b
(b) Angioechogram
findings were seen in the central portion of the three peripherally enhanced tumors (Fig. 5) and in two of the partially enhanced tumors. Marked tumor cell infiltration and scanty fibrotic stroma produced a positive enhancement pattern with differing intensities in angioechography. This pattern was seen in the peripheral area of the three large tumors, one 3, 5 cm tumor and a tumor
smaller than 3 cm (Fig. 6). One 5 cm tumor
showed less intense enhancement.In addition, the mucinous carcinoma had large mucinous lakes in which the enhancement
inten-sity was faint, making for a weak correlation (Fig.
7). The CCC tumor with a hemangioma like
structure, revealed very intense enhancement in
the area of dilated vascular spaces (Fig. 8).
'
Discussion
Previously the ultrasonographic apperance of cholangiocellular carcinoma was generally
des-cribed as either nodular or infiltrative, depending
on whether or not the tumor mass was visible3)N5}, the reasons for different appearances not being clear. Cholangiocellular carcinoma was
macro-scopically classified as nodular, periductal or
in-traductal type, according to gross appearance. This classification system proved to be acceptable
because clinical and pathologic features as well as
prognosis differed among tumor types20). Intra-hepatic metastasis and portal vein tumor throm-bus were more frequent in nodular type tumors and in periductal tumors with marked parenchy-mal infiltration. The intraductal type, which histopathologically was papillotubular carcinoma with intraductal growth and in some instances slight parenchymal infiltration, had the best
prognosis2i).
Review of the echo pattern images of the 27
resected CCC cases and correlation with the
resected macroscopic specimens revealed that the US appearance of CCC was related to the gross appearance of the tumor. Tumor mass formation was clearly demonstrated in the nodular typewhile it was only poorly identified or not visible in
the periductal and intraductal types.
Visualiza-tion of the tumor mass was dependent on the site of origin and the direction of the tumor's growth pattern. Taking these findings into consideration, it appears that the nodular, periductal and in-traductal types of CCC may be distinguishable by
us.
The majority of patients showed nodular type
CCC･ which was visualized mainly as an
ill-defined nodular mass by US. Hypoechoic tumors did not show a hypoechoic rim because of the equal intensity of the echo pattern. To clarify whether the hypoechoic rim observed on US is due to the tumor itself, rather than changes in the surrounding liver tissue caused by the presence of the tumor, a careful histologic examination was carried out. CCC shows infiltrative type growth, therefore compression of the surrounding liver parenchyma was not marked, although surround-ing, liver cells appeared slightly compressed in some regions in proximity to the tumor site. Consequently, it seems that the hypoechoic rim is related mainly to the predominance of tumor cells in the peripheral part of the tumor and less to changes in the surrounding liver parenchyma. Echogenicity was demonstrated to be dependent on tumor diameter. As the tumor increases in size,
it becomes more echogenic4). These tumors
showed slightly hyperechoic homogeneous echo
patterns, due to an increase in fibrotic tissue and
some small necrotic areas. Extensive areas of necrosis were not frequently observed. The inten-sity of the echo pattern was important in differ-ential diagnosis, particularly with metastatic tumors which have a more echogenic tumor mass than CCC. Small nodular tumors (less than 3 cm) appeared as a hypoechoic or isoechoic ill-defined nodule with no other significant US findings Differentiation from other small lesions is diffi-cult, particularly if the tumor has a hypoechoic echo pattern. Associated bile duct dilatation may be of importance in such cases.
To our knowledge, vascular detection by US has not previously been discussed in regards to CCC
tumors. Therefore, in this study, particular
of a portal tract and a "vessel like structure" described as a hyperechoic linear finding within the tumor. "Portal tract passing through the turpor" occurs when the portal tract is large and
fibrotic tissue from periportal pedicle's is thick,
making tumor invasion difficult, and tumor tissue grows so as to surround the portal tract. The "disappearing portal tract" sign is suggestive of
interstitial invasion along the portal tract, as well
as the bile duct and portal vein tumor thrombus.
The "vessel like structure" was a unique US
finding of nodular type tumors. The correspond-ing gross specimen examination revealed the pre-sence of minor tributaries. Therefore, it was concluded that there was a correlation between these findings. The vessel like structure might represent a trapped portal tract inside the tumor. The associated signs of portal tract presence and "vessel like structures" within the tumor were of importance as US characteristics contributing to the diagrtosis of CCC. On the other hand, since vascular involvement has very important prog-nostic considerations these findings could also be useful for predicting probable invasion of the portal tract around the tumor site. However, USdetection of interstitial invasion along the portal tract was quite limited.
Failure to image the tumor mass in periductal type tumors is attributable to tumor infiltration into the surrounding liver parenchyma in the absence of marked compression. A diagnosis of CCC is indicated by findings of the portal tract disappearing at the site of the lesion and also by
proximal bile duct dilatation.
Intraductal type tumors are confined to the bile duct and on occasion the tumor mass can be seen
to fill the bile duct. There is an association with
prominent bile duct dilatation. Atrophy of the involved segment or lobe of the liver, due to bile duct or portal tract obstruction, may also be
present.
Intrahepatic lithiasis can be associated with CCC28)J29) but in our series it was found only in nodular type tumors. The presence of abscess and debris may produce a strong echo pattern leading
- 83
to mlsmterpretatlon.
Bile duct dilatation is a striking feature of CCC3)･5). According to the classification system used in this study, there are different degrees of bile duct dilatation. Bile duct dilatation in the nodular type depended upon the size and position of the tumor. The periductal type showed varying
degrees of diiatation proximal to the lesion, while
the intraductal type had the most marked bile duct dilatation. Dilatation was not related to the
presence of stones in the bile duct.
Angioechography is used as an adjunct to en-hance the ability of conventional ultrasound. According to our experience and a review of the
iiterature, hepatocellular carcinoma, focal nodular
hyperplasia, hemangioma and metastasis have
characteristic angioechographic features. To our knowledge, there have been no previous report onCCC angioechographic patterns. Small tumors
differ in their angioechographic patterns, and differentiation from other small liver tumors, particularly HCC, is difficult. However, having experienced only two cases we do not have ade-quate data to make a definitive description. As tumors increase in size, their angioechographic patterns･ change from whole to peripheral enhan-cement, and the central portion of the tumor contains more.dense fibrotic tissue and fewer tumor cells. Thus, the angioechographic appear-ance of the tumor is one of peripheral enhappear-ance- enhance-ment and a non-enhanced central portion. It is particularly important to differentiate between metastatic tumor24) and CCC. With large tumors, the peripheral enhancement of CCC is thicker and tends to be more intense than that of metastatic tumors.
Conclusion
Correlations between US and pathologic find-ings of the resected specimens revealed that US findings differed for nodular, periductal and in-traductal CCC tumors. In nodular type tumors, the tumor mass is clearly visible and attention should be paid to the presence of portal tract and "vessel like structure" signs. US findings of
disappearing portal tract sign and bile duct dilata-tion are the most distinctive features of periductal
and intraductal type tumors. Angioechography is a useful diagnostic procedure for defining the nodular type of CCC. Observations obtained from conventional US and angioechography and corre-lations with pathological findings provide addi-tional evidence supporting a diagnosis of CCC.
Acknowledgment
I wish to express my sincere gratitude to Professor Dr. Hiroshi Obata for providing me with necessary facilities
and constant encouragement during the tenure of my
research work. I would also like to thank the rest of the
Department of Gastroenterology for providing a friendly and stimulating atmosphere to work in.
References
1) Liver Cancer Study Group Japan: The General
Rules for the Clinical and Pathological Study of Primary
Liver Cancer. pp 40-41, Kanehara Shupann, Tokyo (1992)
2) Craig JR, Peters RL, Edmondson HA: Tumors of
the Liver and Intrahepatic Bile Duct. pp 197-212,
Armed Forces Institute of Pathology, Washington (1988)
3) Okada S, Okazaki N, Haniya K et al:
graphy in the early diagnosis of cholangiocarcinoma. Nippon-Rinsho UpnJ CIin Med) 49(8): 1789-1793, 1991 4) Wibulpolprasert B, Dhiensiri T: Peripheral
angiocarcinoma: sonographic evaiuation. J CIin
sound 20: 303-314, 1992
5) Ohta H, Nakano S, Watahiki H et al: Clinical study of cholangiocellular carcinoma. Nippon Shokakibyo Gakkai Zasshi Upn J Gastroenterol) 80(9): 1747-1753,
1983
6) Itai Y, Araki T, Furui S: Computed tomography of primary intrahepatic biliary malignancy. Radiology 147: 485-490, 1983
7) Moriyama N, Muramatsu Y, Takayasu K et al: CT
and MRI diagnosis of intrahepatic bile duct cancer.
Nippon Rinsho Upn J CIin Med) 49(8): 1799-1804, 1991
8) Yoshikawa J, Matsui O, Takashima T: Angiography in the early diagnosis of cholangiocarcinoma. Nippon Rinsho UpnJ CIin Med) 49(8): 1794-1798,1991
9) Dooms GC, Kerian RK, Hricak H et al: carcinoma: Imaging by MR. Radiology 159: 89-94, l986 10) Tomimatsu M, Obata H: Diagnosis of
lular carcinoma. Primary Liver Cancer in Japan (Tobe T et al eds) pp 393-401, Springer-Verlag, Tokyo (1992)
11) Okuda K, Kubo Y, Okazaki N et al: Clinical aspects of intrahepatic bile duct carcinoma including hilar
carcinoma. A study of 57 autopsy-proven cases. Cancer
39: 232-246, 1977
12) Kawarada Y, Mizumoto R: Diagnosis and treatment of cholangiocellular carcinoma of the liver.
gastroenterol 37: 176-181, 1990
13) Mizumoto R, Kawarada Y: Diagnosis and treatment
of cholangiocarcinorna artd cystic adenocarcinoma of the liver. Neoplasms of the Liver (Okuda K & Ishak KG eds) pp 381-396, Springer-Verlag, Tokyo (1987)
14) Hillmann BJ, Smith EH, Gammelgaard J et al:
Ultrasonqgraphic-patholQgic correlation of malignant
hepatic masses. Gastrointest Radiol 4: 361-365, 1979
15) Saito A: Clinico-pathological study of well-differentiated
hepatocellular carcinoma. J Tokyo Wom Med Coll 61(5):
423-429, 1991
16) Tanaka S, Kitamura T, Imaoka S et al:
lular carcinoma: sonographic and histologic correlation.
AJR 140: 701-707, l983
17) Ogasawara T, Lim I, Satoh I et al: Ultrasonography of peripheral cholangiocellular carcinoma-comparison with pathoiogic findings in 7 cases. Rinsho-Hoshasen
Upn J CIin Radiol) 32(1): 79-84, 1987
18) Weinbren K, Mutum SS: Pathological aspects of angiocarcinoma. Pathology 139: 217-238, 1983
l9) Nakajima T, Kondo Y, Miyazaki M et al: A
pathologic study of 102 cases of intrahepatic
carcinoam. Hum Pathol 19(10): 1288-1234, 1988
20) Yamamoto M, Takasaki K, Tsugita M et al: The
clinico-pathological features and surgical treatment for
cholangiocellular carcinoam. Jpn J Gastrointest Surg
26(2): 306, 1993
21) Yamamoto M, Takasaki K, Tsugita M et al:
ductal papillary cholangiocarcinoma. Report of 6 cases.J Biliary Tract & Pancreas 14: 45-50, 1993
22) Sugihara S, Kojiro M: Pathology of cinoma. Neoplasms of the Liver (Okuda K & Ishak KG
eds) pp 143-158, Springer-Verlag, Tokyo (1987)
23) Matsuda Y, Yabuuchi I: Hepatic tumors US contrast enhancement with C02 microbubbles. Radiology 161: 701-705, 1986
24) Saito A, Takasaki K, Nakagawa M et al: Use of
angioechography in the diagnosis of liver tumors. Tan-Sui (Liver-Gall-Spleen) 15(6): 1129-1132, 1987
25) Saito A, takasaki K, Ootani T et al: Diagnostic evaluation of angio-echo method for hepatic tumors. Proceedings of the 51st Meeting of JSUM: pp 277-278,
1987
26) Kudo M, Tomita S, Tochio H et al: Small lular carcinoma: diagnosis with US angiography with
intraarterial C02 microbubbles. Radiology 182:
155-160, 1992
27) Kudo M, Tomita S, Tochio H et al: Hepatic focal
nodular hyperplasia specific findings at dynamic
trast-enhanced US with carbon dioxide microbubbles. Radiology 179: 377-382, 1991
28) Chen MF, Jan YY, Wang CS et al: Intrahepatic
stones associated with cholangiocarcinoma. Am J
troenterol 84(4): 391-395, 1989
29) Koga A, Ichimiya H, Yamaguchi K et al:
thiasis associated with cholangiocarcinoma. Cancer 55:
胆管細胞癌における病理組織所見と超音波検査所見およびアンジオエコー所見の対比 東京女子医科大学消化器病センター サイトウ アキ コ
