대 한 방 사 선 의 학 회 지 1992 ; 28 (2) : 229~235 Journal of Korean Radiological Society , March , 1992

Clonorchiasis and its Complications:

Cholangiogram Revisited

Jae Hoon Lim, M.D. , Young Tae Ko, M.D. , Dong Ho Lee, M.D. , Kwan Sup Lee, M.D. , Soo Jhi Suh, M.D.* , Seong Koo Woo, M.D.*

Department o[ Radiology, Kyung Hee University Hospital

- Abstract-

Clonorchiasis is known to be closely related with the development of recurrent pyogenic cholangitis and car-

cinoma of the bile ducts. ln order to ascertain the cholangiographic signs for recurrent pyogenic cholangitis or car-

cinoma of the bile ducts arising in patients with clonorchiasis , we reviewed cholangiograms in 42 patients with proven

clonorchiasis. The population consisted of 29 patients with clonorchiasis alone , six patients with clonorchiasis and

recurrent pyogenic cholangitis , and seven patients with clonorchiasis and carcinoma of the bile ducts.

Cholangiographic abnormalities in 29 patients with clonorchiasis alone were intrahepatic m비tiple. ovaI. or elliptic

filling d efects measuring 2-10 mm in size. representing adult l1ukes (n; 24). The pe디pheral bile ducts were obstructed

(n; 18). and the margins were ragged (n; 20) and hazy (n; 12). The intrahepatic bile ducts were dilated diffusely

(n; 27) . and the dilated peripheral small tributaries gave the impression of “ too many ducts appearance" (n; 22).

On the other hand. the extrahepatic bile ducts were less involved; filling defects were less cornmon (n; 7) 와ld dilatation

was mild (n; 17). In six patients with clonorchiasis and recurrent pyogenic cholangitis ‘ there were filling defects

of stones. and the extrahepatic ducts and larger intrahepatic ducts were predominantly dilated. In seven patients

with clonorchiasis and cholangiocarcinoma. all the biliary tree proximal to the tumor was markedly and diffusely

dilated. In the latter two groups. filling defects of f1 ukes and associated findings were less prominen t. but there was

disproportionately severe dilatation of too many intra hepatic ducts

In patients with recurrent pyogenic cholangitis or cholangiocarcinoma ‘ clonorchiasis should be considered as

a underlying cause when cholangiogram shows “ disproportionately" severe dilatation oftoo many intrahepatic ducts.

lndex Words: Bile ducts. radiography ‘ 765. 122

Bile ducts. calcul i. 765. 81

Bile ducts. neoplasms , 765 . 321

Cholangitis , 765 . 202

INTRODUCTION

Clonorchiasis , infestation of liver f1 uke , Clonorchis

sinensis , is one of the most common parasitic disease

in Korea , caused by ingestion of raw l1esh of

freshwater fish (1 -6) . The infestation is usually silent

but. heavy infestation produces obstructive jaundice ,

*양明大뺑交 醫과大쩔 放射線科學敎室

resulting in late sequela of intrahe patic bile duct

dilatation and fibrosis (1-3 , 7) . In these patients , in-

cidence of recurrent pyogenic cholangitis (1. 7-10)

and cholangiocarcinoma (1 , 11-13) is considerably

high.

There have been several reports concerning

cholangiographic features of clonorchiasis in Korean

(4-6) and English literature (3 , 14, 15) . Howe ve r , to

*Department of RadioJogy. Keimy ung University MedicaJ Co lJege

이 논문은 1991년 8월 1 2일 접수하여 1991년 10월 11일에 채택되었음 Received August 12. Accepted October 11. 199 1.

229

Journal of Korean Radiological Society 1992 ; 28 (2) : 229~235

the best of our knowledge , there has been no descrip-

tion concerning the cholangiographic findings in pa-

tients who had clonorchiasis and recurrent pyogenic

cholangitis or cholangiocarcinoma. Here we describe

the cholangiographic findings in 42 patie nts with

clonorchiasis , including what is the first description

in six cases associated with recurrent pyogenic

c holangitis and seven cases associated with

cholangiocarcinoma.

MATERIALS AND METHODS

Cholangiographic examinations of 42 patients

with clonorchiasis were reviewed . This was not a con-

secutive series since many patients with clonor-

chiasis did not undergo cholangiography , especially

in mild infestation. Twenty-seven cases were from the

file of Kyung Hee University Hospital during a

lO-year-period. About the same number of patients

with clonorchiasis underwent cholangiography , but

cholangiograms were lost or inadequate for review ,

or hospital records were insufficien t. 50 these cases

were not included in our study. During the same

period , approximately 600 patients were diagnosed

as having clonorchiasis on the basis of stool examina-

tion for ova of C. sinensis. The remaining 15 cases

were from Dong 5an Hospital during a recent 3-year-

period. The latte r hospital is located in the middle of

more endemic area. Twenty four cholangiograms

were endoscopic retrograde cholangiograms, ten were

percutaneous transhepatic cholangiograms and the

remaining eight were T-tube cholangiograms. En-

doscopic retrograde cholangiography and per-

cutaneous transhepatic cholangiographic studies

were performed because of obstructive jaundice or

persistent elevation of serum alkaline phosphatase

level. T-tube chola ngiography was performed after

surgery of bile duct stone , cancer , or severe infesta-

tion of C. sinensis.

The population consists of three groups: (1) 29 pa-

tients with clonorchiasis alone: (2) six patients with

clonorchiasis and recurrent pyogenic cholangitis: (3)

seven patients with clonorchiasis a nd cholangiocar-

cinoma of the bile ducts: one in the right intrahepatic

duct , five at the bifurcation a nd the other one at the

common hepatic duct. The diagnosis was made on

the basis of positive stool examination for ova in 22

patients (1, 16) , positive ova in stool and/or evacua-

tion of adult flukes from the bile ducts during biliary

surgery or catheter drainage in 20 patients . In two

patients , wedge biopsy of the liver revealed

adenomatous hyperplasia of the bile ducts as we \l as

periductal fibrosis , and in one patent adult f1ukes

were found in the bile ducts (Fig. 1). Thirty eight pa-

tients were men and four patients were women. The

average age was 50 years (age range , 29-72 years).

Cholangiograms were analyzed for the presence

of filling defects of flukes in the bile ducts , the degree

and pattern of dilatation of the bile ducts , and the con-

tour of biliary tree.

Fig. 1. Photomicrograph ofliver biopsy specimen show-ing an adult fluke of C. sinensis (open arrows) within the dilated small intrahepatic bile duc t. The wall of the bile duct shows fibrous thickening (between short arrows), adenomatous hyperplasia of periductal glands (curved arrow) and in f1ammatory cell infiltration (H&E , X40).

RESULTS

The cholangiographic findings are summarized in

Table 1. In one patients , the cholangiogram was nor-

mal. Abnormalities varied from minimal changes

such as a few filling defects within normal bile ducts

to extensive filling defects within markedly dilated

intra- and extrahepatic bile ducts .

Group 1. Clonorchiasis alone

F il1ing defects due to flukes and related findings

Ofthe 29 cases with clonorchiasis alone , multiple

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Cholangiographic Findings

Table 1. Chola ngiographic Findings in 42 Cases of Clonorchiasis

Jae Hoon Lim , et al : Clonorchiasis and its Complications

Clonorchiasis Alone Clonorchiasis with Clonorchiasis with

Recurrent Pyogenic Cholangiocarcinoma (n = 7)

(n = 29) Cholangitis (n = 6)

Findings due to nuke per s e

Ova l or elliptic filling defects

In trah epatic bile ducts

Extrahepatic bile ducts

Ga llbladder

Peripheral duct obstruction

Ragged margin of bile ducts

%

7

?

18

20

Bile duct change

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‘ Number of cases among the 20 cases in which the gallbladder was visualized

oval or elliptic fill ing defects (Fig. 2). ranging from 2

mm to 10 mm , were visualized predominantIy within

intrahepatic bile ducts in 24 cases (83%) , ex-

trahepatic bile ducts in seven cases (24%) and the

gallbladder in two cases . In severe infestation , the bile

ducts were packed with the defects (Fig. 2) but in mild

Fig , 2_ A 35-year-old man with a history of raw fish in-gestion complained of ja undice. A stool examination for ova was positive a nd eggs per day was 1,600 ,000. En-doscOpic retrogade chola ngiogram discloses severe dilatation of intrahepatic bile ducts and innumerable ‘ oval or e lliptic lìlling defects of adult nukes (white arrows) in the peripheral bi le ducts , resulting in obstruction. Bile ducts are hazy , especially in the left h epatic lobe , and margin is ragged. Note relatively s ligh tIy dila ted (13 mm) extrahe patic ducts (black arrow)

infestation , there were several defects scattered

within the dilated bile ducts (Fig. 3). In 18 cases

(62%) , the peripheral bile ducts , namely tertiary ,

Fig. 3. A 51 .year-old man with a history of jaundice. Stool test for ova was positive and egg per day was 800 ,000. Cholangiogram of the left hepatic lobe discloses few , oval filling defects offlukes (arrows) within the tips of diffusely dilated peripheral smaller bile ducts. Note fusiform dilatation of the far periphera l ducts , the periphery being wider than the central ducts and bile ducts are e longated and tortuous . Peripheral ends of some of the ducts are blunt due to obstruction by nukes or aggregates of nukes (open a rrows). At a glance . the intra hepatic bile ducts a re “ too many". There is a minima l stenosis (curved black arrow). The extrahepatic bile ducts are slightly dilated. Arrowhead points the pan-creatic duct

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Journal of Korean Radiological Society 1992 ; 28 (2) : 229~235

quaternary. or more peripheral tributaries. were

obstructed and filling of contrast medium was in-

terrupted (Fig. 2. 3). The tips of these ducts were

blun t. The contour of the bile ducts were irregular

and ragged in 20 cases (69%) due to filling defects.

Bile duct changes

The small intrahepatic bile ducts. tertiary. quater-

nary. or more peripheral ducts. were dilated diffuse-

ly and uniformly (Fig. 2 . 3) in 27 cases (93%). In 22

cases (76%) ‘ the biliary tree was dilated and well

opacified up to the periphery of the liver (Fig. 3). giv-

ing the impression that there were “ too many in-

trahepatic bile ducts' ’. Some cases showed fusiform

dilatation of the peripheral duct. the diameter of the

peripheral ducts being larger than that of the more

central ducts (Fig. 3). The ducts were elongated and

tortuous in these cases. Minimal stenosis of the in-

trahepatic bile ducts (Fig. 3) was present in five pa-

tients (17 %). The margin of the bile ducts is hazy (Fig.

2) in 12 patients (41 %). The extrahepatic ducts were

not dilated (less than 10 mm) in 12 cases (41 %). and

were slightly dilated (less than 15 mm) in 17 cases

(59%).

Findings of the gallbladder

The gallbladder was visualized in 19 cases. There

were two cases showing oval or elliptic filling defects.

The gallbladder was distended moderately or

markedly in 9 cases (44%)

Group 2: Clonorchiasis with recurrent pyogenic

cholangitis.

Cholangiograms in six patients with clonorchiasis

associated with recurrent pyogenic cholangitis show-

ed basically similar findings but modified con-

siderably. There were filling defects of f1ukes. ragged

and hazy margin of the bile ducts. dilatation of the

intrahepatic bile ducts. and “ too many ducts ap-

pearance ‘' . bu t those findings of fI uke per se are less

frequent and less prominent (Fig. 4) . Besides. there

were defects of stone or stones ‘ in contrast to the

Fig. 4. Endoscopic retrograde cholangiogram of a 66-year-old man had a long history of ingestion of raw fish. Stool test disclosed ova of C. sÏnensis. “ Too many intrahepatic bile ducts" are slightly dilated whereas the extrahepatic ducts are markedly dilated. There is an oval filling defect of a stone (arrow). The intrahepatic bile ducts are opacified up to the periphery of the liver but there is no demonstrable filling defect. At surgery. stones in the intrahepatic duct. extrahepatic bile duct and gallbladder were removed

cases with clonorchiasis alone. Cholangiograms in

this group showed predominantly dilated ex-

trahepatic ducts in four cases.

Groups 3: Clonorchiasis with cholangiocarcinoma.

Cholangiograms in all seven patients with clonor-

chiasis and cholangiocarcinoma showed severe

dilatation of the intrahepatic bile ducts proximal to

the tumor. much more severely than in patients with

clonorchiasis alone or clonorchiasis and bile duct

stone (Fig. 5). Bile duct cancer was visualized as a

focal or diffuse narrowing or complete obstruction

Other findings were basically simUar to but less pro-

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Fig.5. A 57-year-old man presented with pruritus and progressive jaundice. Sonogram and CT disclosed diffuse severe dilatation ofthe intrahepatic bile ducts and a mass at the con f1 uence of the right and left hepatic ducts. Drainage catheter was inserted and flukes were evacuated through the catheter. Cholangiogram shows severe diffuse dilatation of the intrahepatic bile ducts. Very smal\ tributaries of “ too many' ’ bile ducts are dilated up to the far peripheral portion ofthe Iiver. dilated much more severely than might be expected in clonor-chiasis alone. Note complete obstruction by cancer (ar-row) at the confluence of the right and left hepatic ducts.

Jae Hoon Li m. et al : Clonorchiasis and its Complications

ding (Figs. 2. 3). The involved bile ducts were ragg-

ed owing to f1 ukes and aggregates of f1 ukes abutting

the wall of the bile ducts as well as cholangitis (Fig.

2). There were only few cases of minimal bile duct

stenosis (Fig. 3).

The change of the bile ducts consisted of diffuse

dilatation of smaller intrahepatic bile ducts (Figs. 2.

3 . 4) and no or minimal dilatation of extrahepatic bile

ducts (3 -6. 14 ‘ 15). The right and left hepatic ducts

and extrahepatic ducts were usually normal. or mild-

ly dilated in some patients with severe infestation.

There was no dist외 biliary obstruction except in cases

with concomittant cholangiocarcinoma. As the en-

tire intrahepatic bile duct are diffusely dilated .

cholangiogram revealed .‘ too many ducts ap-

pearance" at a glance when the biliary tree is ade-

quately visualized (Fig. 2. 3 ‘ 4.5). This is not caused

by actual increase in number of bile ducts. but by

visualization of the dilated smaller tributaries such

as tertiary. quaternary and more peripheral

tributaries. Some of the peripheral tributaries show

ed fusiform dilatation (Fig. 3). The severity ofthe bile

duct dilatation was not necessarily proportional to the

minent than those patients with clonorchiasis alone. number of f1 ukes. Sometimes bile duct margin is hazy

(Fig. 2) due probably to increased mucous secretion

DISCUSSION in the bile duct. p∞r mixing and insufficient amount of contrast media not enough for the dilated

Adult worms of C. sinensis reside in the human peripheral ducts (1 4).

intrahepatic bile ducts and produce m echanical The intrahepatic bile duct dilatation re f1ects basic

obstruction of the bile ducts. cholangitis and periduc- disease process. AduIt f1 ukes reside in the m edium

tal fibrosis (1, 2. 7). It is well known that characteristic and small intrahepatic bile ducts (Fig. 1) and produce

oval or elIiptic filling defects on cholangiogram repre- cholangitis (1, 2. 7) . Dilatation of the smal\er bile

sent liver f1ukes (3-6. 14. 15) . They vary from 2-3 mm ducts is most likely caused by obstruction by f1 ukes.

to 5-10 mm in size. Adult f1 ukes are flat. willow as demonstrated on cholangiograms (3-6. 14. 15). The

leaf1ike. measuring 8-15 mm long. 1.5-4.0 mm wide f1uke or aggregates of f1 ukes could easily occlude the

and about 1 mm thick. As f1 ukes reside in the small small peripheral ducts (Fig. 1). but larger ducts such

intrahepatic bile ducts. these defects were as rightand left hepatic ductsand extrahepatic ducts

predominently within the intrahepatic ducts (Figs. are wide enough to be patent. even if f1 ukes are lodg-

2.3). occasionally scattered in the extrahepatic ducts ed within them (9. 13). Mucosal hyperplasia. mucus

and the gallbladder (3) . These defects are distinguish- in the ducts caused by cholangitis. periductal in f1am-

ed from stone by their elliptical or oval shape. mation. fibrosis and stricture may play additional

smallness and uniformity in size (14). Sometimes roles in the occlusion of ducts and resuItant proximal

f1 uke or aggregates of f1ukes blocked and interrupted small intrahepatic duct dilatation (l. 3. 7)

contrast filling of the small peripheral intrahepatic Cholangiograms in patients complicated with

bile ducts (1 5). giving the impression of abrupt en- recurrent pyogenic cholangitis or cholangiocar-

- 233-

Journal of Korean Radiological Society 1992 ; 28 (2) : 229~235

cinoma showed basically similar appearances to

clonorchiasis alone , but were considerably modified

(Fig. 4). In six cases with clonorchiasis and recurrent

pyoge nic cholangitis , the extrahepatic ducts were

predominantly dilated. a typical cholangiographic fin-

ding in recurrent pyogenic cholangitis without clonor-

chiasis (16-19). In patients with clonorchiasis alone ,

the extrahepatic ducts were normal or mildly dilated

(3-6 , 14 , 15). The findings caU3ed by f1 ukes such as

filling d efects, peripher외 obstruction , and raggedness

of bile ducts were apparent but much less prominen t.

This may be due to extinction of f1 ukes in recurrent

pyogenic cholangitis. The f1ukes are killed by

bacterial infection (1 . 7).

In eight cases of clonorchiasis c omplicated with

cholangiocarcinoma , t h e proximal biliary tree to the

tumor , especially t h e peripheral ducts was marked-

Iy dilated (Fig. 5 ), much more s e verly than might b e

expected in cases of c1onorchiasis alone . Choi et al

(20), in a CT review of c1onorchiasis , described that

CT of the patients with clonorchiasis associated with

the extrahepatic biliary maligna n cies had markedly

dilated intrahepatic bile ducts , while the patients with

c lonorchiasis a lone had diffuse ‘ minimal or mild

dilatation. This may be attributed to the fact that

biliary malignancy is a high pressure obstruction

whereas c1onorchiasis is an incomplete , low pressure

obstruction.

In conclusion , when c holangiogram shows “ too

m a ny intrahepatic bile ducts sign ' ’ and “ dispropor-

tionately" dilate d peripheral intrahepatic bile ducts

in patients with recurrent pyogenic cholangitis or bile

duct carcinoma. clonorchiasis s hould be borne in

mind as a cause of the disease.

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내시경학회지 1991 ; 1 : 29 -32

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Yokagawa M. Clonorch iasis studied by per-

cutaneous cholangiography. and a therapeutic trial

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pearance in clonorchiasis. Br J Radiol 1984:57

681-684

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18 林在勳， 尹榮均， 金짧觸， 閔榮 뺀觸管結石효의 內視鏡

的 遊行{生 廳管造影術. 大韓放射線醫學會誌 1982 ; 18 :

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19 ‘ 洪慶뻐 林在敵 高永泰， 李東鎬. 再發性化腦廳管쏘의 內

視鏡的 遊行性 8흉管造影術. 大韓放射線醫學會誌 1990 ;

26 : 117- 120

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CT findings of clonorchiasis. AJR 1989: 152:281 -284

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< 국문 요약 >

Jae Hoon Lim, et al : Clonorchiasis and its Compl ications

8千吸蟲효과 合f井'ilE: 擔管造影像의 再照明

慶熙大學校 뽑科大學 放射線科學敎室， 양明大學校 醫科大學 放射線科學敎室

林在勳 • 高永泰 • 李東鎬 • 李寬燮 • 徐修之* • 禹뿔組*

1lf吸蟲효이 오래 지속되면 合↑井효으로 再發性化職體管꽃이나 腦管카침이 생길 수 있다. 걱정:者들은 府l댔蟲효과 再發性化腦

體짤꽃이나 觸管햄이 {井發한 경우와 단순히 府吸蟲효만 있는 경우의 腦管造풍끼象을 比較 觀察 하였다. 大便檢훌나 手術時

廳管에서 1lf吸蟲의 .!l ß이나 成蟲을 확인한 42 思者의 總管造풍!*"r을 後向的으로 觀察 하였는데 이 중 29例는 밤1냈蟲효만 있

는 경우였고， 6W~는 府吸蟲효과 再發'1生f 뼈農廳管찢。1. 나머지 7例는 딴吸蟲효과 廳管찮이 {井發된 경우였다. n千吸蟲효만 있

는 29예에서는 成體에 의한 充滿缺根 (n=24) ， 末稍略管의 閒塞(n= 1 8) ， 不規則 하거나(n=20) 희미한 體管(n= 1 2) ， 미만성 R꾸

內 觸管據張 (n=27) , 그리고 “R內 多管 효候" ( n=22 )가 보였다. 再發性 化體體管*이나 廳管찮 뽕、者(n = 1 3) 에서는 觸管 結

石이나 觸管癡에 의한 所見外에， 府吸蟲 成蟲 自體에 의한 變化는 적으나 거의 모두 딴內觸管이 “유난히” 또는 “이상스

레 ” 심하게 據張되고(n= 13) 多管효候(n=12 )가 보였다.

再융휩훈 ↑때훌R홉管갖이나 廳웹훨 뽕、者의 廳管造몽끼象에 府內體管이 “유난히” 심하게 據張 되고 “多管뾰候”가 보이면 두

가지 f짙뽕、의 원인으로서 8꾸I!及蟲효을 꼭 생각해야 한다.

- 235-

29th Congress European Society of Pediatric Radiology (ESPR) venue: Hotel Hilton Budapest, Hungary. contact: Dr. Bela Lombay (pres. ), Borsod County Hosp .’

Ped. Rad. , P.O. Box 188, 3501 Miskolc , Hungary . (Tel: 36-46-2121 1; Fax: 36-46-23694) 1992/04/27 -01

8th Int. Symposium Radionuclides in Nephro-Urology venue: Chester, United Kingdom contact: Mr. P.H. 0 ’ Reilly. Dep t. of Urology.

Stepping Hill Hospital, SK2 7JE Cheshire , United Kingdom. (Tel: 061-419 5484; Fax: 06-419 5699) 1992/05/06-08

92nd Meeting American Roentgen Ray Society venue: Marriot World Center Orlando , Florida, USA. contact: American Roentgen Ray , Society ,

1891 Preston White Drive , VA 22091 Reston , USA. (Tel: 703-6488992; Fax: 1992/05/10-15

Radiology & Oncology 92 venue: Int. Convention Centre , Birmingham , United Kingdom. contact: British Institute 0 [, Radiology ,

36 Portland Place , W1N 4AT London , United Kingdom. (Tel : 071-5804085; Fax: 071 -255 3209) 1992/05/18-20

39th Annual Meeting Society for Nuc1ear Medicine venue: L.A. Convention Center Los Angeles , California, USA. contact: Soc . of Nuclear Medicine ,

136 Madison Ave .. 8th fl. , NY 10016 New York , USA. (Tel: ; Fax: 1992/06/09-12

Car ’92. Computer Assisted Radiology venue : Baltimore , Maryland , USA. contact: Prof. Heinz U. Lemke , Univ. Klinikum , Raum 1005 ,

Augustenburger Platz 1, D-1000 Berlin 65 , Germany. (Tel: 49-30 45052044; Fax : 49-30 45052043) 1992/06/14-17

3rd Annual Meeting Eur. Soc. of Gastrointestinal Radiologists (ESGR) venue: Hotel Beach Regency Nice , France. contact: SOCFI - ESGR,

14 rue Mandar , 75002 Paris , France. (Tel: ; Fax: 1-40260444) 1992/06/22-24

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