Am. J. Trop. Med. Hyg., 73(6), 2005, pp. 1139–1144
Copyright © 2005 by The American Society of Tropical Medicine and Hygiene
CORRELATION BETWEEN SONOGRAPHIC FINDINGS AND INFECTION
INTENSITY IN CLONORCHIASIS
MOON SEOK CHOI, DONGIL CHOI, MIN-HO CHOI, ZHUO JI, ZHIMIN LI, SEUNG-YULL CHO, KWANG-SEON HONG,
HAN-JONG RIM, AND SUNG-TAE HONG*
Departments of Medicine and Radiology, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea;
Department of Molecular Parasitology, Sungkyunkwan University School of Medicine, Suwon, Korea; Department of Parasitology
and Entomology, Heilongjiang CDC, China; Korea Association of Health Promotion, Seoul, Korea; Department of Parasitology and
Tropical Medicine, and Institute of Endemic Diseases, Seoul National University College of Medicine, Seoul, Korea
Abstract. This prospective study was performed to evaluate the diagnostic usefulness of sonography in terms of the
intensity of Clonorchis sinensis infection. Total 1,384 residents were subjected to this study at an endemic area in China,
in which a clonorchiasis control program had been performed. History taking, fecal examination, and sonography were
performed, and 87.8% of the subjects were found to be egg positive. Sonography showed intrahepatic bile duct dilatation
(IHDD) in 68.4% of the subjects, increased periductal echogenicity (IPDE) in 24.5%, and gallbladder sludge (GBS) in
20.8%. Moreover, the grades of these sonographic findings were higher in subjects with heavier infections as determined
by egg counts. IHDD was found to be the most accurate sonographic indicator of any infection degree (76.3), whereas
IPDE and GBS were useful only in cases of heavy infection. Subjective symptoms were found to be only poorly
correlated with sonographic findings or infection intensity.
INTRODUCTION
MATERIALS AND METHODS
Clonorchis sinensis is one of the major food-borne pathogens in China, Far Eastern Russia, Taiwan, Vietnam, and
Korea, and it remains common even after the introduction of
praziquantel. Moreover, high-intensity chronic clonorchiasis
is associated with serious medical complications, thus the liver
fluke remains a major public health concern and requires
immediate active control in endemic areas.1–4
Human clonorchiasis is primarily diagnosed by detection of
eggs in feces. The Kato-Katz method is accepted as the best
for fecal examination even in cases with a light burden of the
fluke.5 However, because fecal examination is becoming difficult to perform in the field, alternative diagnostic measures
are required. Intradermal testing, serology, and radiologic imaging are currently used but they lack sensitivity and/or specificity.3,6–10
Abdominal sonography is a popular imaging technique for
screening of the general health status of abdominal organs. In
clonorchiasis patients, sonography demonstrates pathologic
changes of the intrahepatic bile duct and gallbladder induced
by the fluke.7,8 However, its diagnostic sensitivity and specificity are dependent on the sonographic criteria used, and
individual case features, for example, intensity of infection as
determined by egg counts, endemicity, chronicity, and medication history.8 Moreover, the diagnostic utility of sonography with respect to intensity of infection in the field has not
been fully evaluated.8,10 Furthermore, no data are available
concerning any relationship between the subjective symptoms
of clonorchiasis and sonographic findings.
Thus in the current study, we undertook evaluation of the
diagnostic usefulness of sonography in terms of its ability to
determine the intensity of Clonorchis sinensis infection and
subjective clinical symptoms in a statistically meaningful
population.
Study population. Residents (N ⳱ 1,348) who voluntarily
accepted the current examination program were subjected to
the present study at a village in Zhaoyuan county in
Heilongjiang province, China, where a clonorchiasis control
program was operated from 2001 to 2004. The control program was implemented in 6 villages of Zhaoyuan. The current
subjects were originally recruited for the control program,
and screened by fecal examination, subjective history taking,
and abdominal sonography altogether. Also control subjects
(N ⳱ 220) were selected from residents of a nonendemic area
(Harbin, capital city in Heilongjiang province). This study was
approved by the institutional review board of the Center for
Disease Control and Prevention of Heilongjiang Province in
2001. Oral informed consent was obtained from all subjects
before enrollment.
History taking and fecal examinations. Baseline characteristics such as age, sex, and any clinical symptom associated
with clonorchiasis were recorded. A fecal examination was
performed on all subjected residents of Zhaoyuan, an endemic area. Eggs per gram of feces (EPG) were calculated
using the Kato-Katz method,5 and these subjects were classified as egg negative (EPG ⳱ 0), lightly infected (EPG ⳱ 1 to
500), moderately infected (EPG ⳱ 501 to 2,000), or as heavily
infected (EPG ⱖ 2,001).8,9 All of the egg positive subjects
were treated with praziquantel, 3 oral doses of 25 mg/kg.
Sonographic examination. One sonography specialist unaware of the clinical information or the status of C. sinensis
infection performed the examinations using a SonoAce 5500
Ultrasound scanner (Medison, Seoul, Korea) equipped with a
3–6 MHz convex-array transducer. Any evidence of intrahepatic duct dilation (IHDD), increased periductal echogenicity
(IPDE), gallbladder sludge (GBS), fatty liver, extrahepatic
duct dilatation, gallbladder (GB) stone, or bile duct stone was
noted.7,8 The criteria used for the diagnosis and grading of
IHDD, IPDE, and GBS are shown in Figures 1 to 3.
Data analysis and statistical procedures. The prevalence
and intensities of C. sinensis infection among Zhaoyuan residents were analyzed. To assess the relationship between
* Address correspondence to Sung-Tae Hong, Department of Parasitology and Tropical Medicine and Institute of Endemic Diseases,
Seoul National University College of Medicine, 28 Yongon-Dong,
Jongno-Gu, Seoul 110-779, Korea. E-mail: [email protected].
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FIGURE 1. Sonograms showing variable grades of intrahepatic duct (IHD) dilatation. (A) Grade 1: No IHD dilatation is seen. (B) Grade 2:
IHD is dilated but its diameter is smaller than that of the adjacent portal vein. (C) Grade 3: Diameter of the IHD is similar to that of the nearby
portal vein. (D) Grade 4: Diameter of the IHD is definitely larger than that of the adjacent portal vein.
sonographic findings and C. sinensis infection, findings showing high diagnostic accuracy were selected and their diagnostic values were assessed versus the intensity of infection. Finally, the diagnostic accuracies of findings, alone or in combination, were evaluated to identify sonographic criteria
capable of diagnosing clonorchiasis. Diagnostic accuracy was
calculated using the following equation.
Diagnostic accuracy ⳱ [(number of true positives
+ number of true negatives) / total number] × 100
In addition, the sonographic findings of Zhaoyuan residents and of the control subjects were compared and the
relationships between clinical symptoms and sonographic
findings were evaluated.
FIGURE 2. Sonograms showing variable grades of increased periductal echogenicity (PDE). (A) Grade 1: PDE is normal. (B) Grade 2: PDE
is mildly increased. (C) Grade 3: PDE is moderately increased. (D) Grade 4: PDE is severely increased.
SONOGRAPHY IN CLONORCHIASIS
1141
FIGURE 3. Sonograms showing variable grades of gallbladder (GB) sludge. (A) Grade 1: No floating echogenic material in the GB. (B) Grade
2: A few echogenic materials in the GB. (C) Grade 3: Many floating echogenic materials in the GB.
Statistical analysis was performed using the ␹2 test to compare discrete variables and using the Student t test or analysis
of variance (ANOVA) to compare continuous variables.
SPSS for Windows (version 11.0; SPSS Institute, Inc., Chicago, IL) was used for the analysis. P values < 0.05 were
considered statistically significant.
RESULTS
The results of fecal examination among Zhaoyuan residents. In total, 1,384 residents from Zhaoyuan (the endemic
area) were enrolled. They comprised 754 males and 630 females with a median age of 37 years (range; 4–78). Among the
1,384 subjects, 1,215 (87.8%) were egg positive with a median
EPG of 480 (range; 0–280,512). They were classified as egg
negative (EPG 0, N ⳱ 169, 12.2%), light infection (EPG
1-500, N ⳱ 532, 38.4%), moderate infection (EPG 501–2000,
N ⳱ 322, 23.3%), and heavy infection groups (EPG ⱖ 2001,
N ⳱ 361, 26.1%). Males showed a higher egg positive rate
(92.8%) and a heavier intensity of infection (EPG 4,723 ± 574,
mean ± SE) than females (egg positive rate 81.7%, EPG 2,165
± 281, P < 0.001 for each). Comparing the egg positive rates
and the intensities of C. sinensis infection between age
groups, the egg positive rate was highest (91.9%) in the 30s,
but peak intensity was observed in the fifth decade (EPG
4,485 ± 925, Table 1).
Sonographic findings of subjects in Zhaoyuan residents.
Sonographic examinations showed IHDD in 68.4% of subjects, IPDE in 24.5%, and GBS in 20.8% of the 1,348 subjects.
In addition, fatty liver (2.0%), extrahepatic duct dilatation
(2.0%), GB stone (1.1%), and bile duct stone (0.4%) were
also observed. Most of the positive subjects showed mild
grades of the 3 major findings: IHDD, Grade 1 (negative)
31.6%, Grade 2 (mild) 36.8%, Grade 3 (moderate) 24.9%,
Grade 4 (severe) 6.7%; IPDE, Grade 1 (negative) 75.5%,
Grade 2 (mild) 22.1%, Grade 3 (moderate) 2.3%, Grade 4
(severe) 0.1%; GBS, Grade 1 (negative) 79.2%, Grade 2
(mild) 18.7%, Grade 3 (moderate) 2.1%. The 3 major findings
were evaluated according to the intensity of C. sinensis infection (Figure 4). The positive rates of IHDD, IPDE, and GBS
significantly increased as the intensity of infection increased
(P < 0.001 for each). The grade of all major sonographic
findings also increased as the intensity of infection increased
(Table 2, P < 0.001 for each).
The diagnostic values of the sonographic findings for prediction of C. sinensis infection were estimated according to
the degree of the findings, and their diagnostic accuracy of
sonographic findings was highest when Grade 2 or higher was
used as a positive criterion. As the grades of IHDD increased,
diagnostic sensitivity decreased as 75.5% by Grade 2, 35.5%
by Grade 3, and 7.5% by Grade 4, but its diagnostic specificity
increased accordingly as 82.2% by Grade 2, 95.9% by Grade
TABLE 1
Egg positive rates and intensities of Clonorchis sinensis infection
by age
Egg positive
Age
Total
N
%
EPG*
0–9
10–19
20–29
30–39
40–49
50–59
60+
Total
12
146
223
410
352
169
72
1,384
6
119
205
361
317
146
61
1,215
50.0
81.5
91.9
88.0
90.1
86.4
84.7
87.8
62 ± 24
1,566 ± 428
4,161 ± 1,107
3,210 ± 360
4,485 ± 925
3,676 ± 890
3,505 ± 954
3,559 ± 339
* Numbers of eggs per gram of feces, mean ± SE.
FIGURE 4. Major sonographic findings and the intensity of
Clonorchis sinensis infection. The positive rates of intrahepatic duct
dilatation (IHDD), increased periductal echogenicity (IPDE), and
gallbladder (GB) sludge were higher in patients with heavy infections
(P < 0.001).
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CHOI AND OTHERS
TABLE 2
Number of subjects by grades of major sonographic findings according to the intensity of Clonorchis sinensis infection
Fecal examination
Egg negative, N ⳱ 169
Egg positive
Light infection, N ⳱ 532
Moderate infection, N ⳱ 322
Heavy infection, N ⳱ 361
No. with IHDD
No. with IPDE
No. with GBS
Grade 1*/2/3/4
Grade 1*/2/3/4
Grade 1*/2/3
139/23/5/2
161/7/1/0
160/8/1
193/255/81/3
73/145/89/15
32/86/170/73
466/65/12/0
238/76/7/1
180/158/23/0
478/53/1
248/66/8
210/132/19
IHDD, intrahepatic duct dilatation; IPDE, increased periductal echo; GBS, gallbladder sludge.
* Grade 1 means negative of the sonographic finding.
3, and 98.8% by Grade 4. Diagnostic sensitivity of IPDE and
GBS was as low as 27.2% and 23.0%, respectively, when their
Grades 2 or higher grades are considered together. However,
their specificity was 95.3% by IPDE and 94.7% by GBS. As
their grade increased, the specificity increased up to 100%.
The diagnostic accuracy of the sonographic findings for
Grade 2 or higher was found to increase according to the
intensity of infection (Table 3). As a whole, as the infection
intensity (EPG) increased the sensitivity of the 3 findings
increased while the specificity decreased. In terms of the diagnosis of an infection of any degree, the diagnostic accuracy
of IHDD was 76.3%, but the accuracies of IPDE and GBS
were only 35.5% and 31.7%, respectively. IPDE and GBS
showed high diagnostic accuracy only for heavy infections
(75.6% and 74.9%, respectively). Diagnostic accuracies of
sonographic findings (Grade 2 or higher), single and in combination were evaluated versus the infection of C. sinensis,
but no other findings or their combinations had a higher accuracy than the IHDD of Grade 2.
Comparison of Zhaoyuan residents with controls. We compared the sonographic findings of 220 egg negative controls
(50 males and 170 females, median age 44 years, range 18–72)
with those of 169 egg-negative Zhaoyuan residents (54 males
and 115 females, median age 35 years, range 6–78). No significant differences were found in terms of sex or age distribution between the two groups. On comparing the sonographic findings of egg negative residents between the nonendemic area and high endemic area, we found that IHDD
(4.5% versus 17.8%, P < 0.001), IPDE (0% versus 4.7%, P <
0.001), and GBS (0.5% versus 5.3%, P ⳱ 0.001) were more
frequent in the high endemic group.
Correlation with clinical symptoms. We evaluated the subjective clinical symptoms in 513 egg positive Zhaoyuan residents, and 108 (21.1%) of them reported one or more symptoms; epigastric fullness (7.6%), abdominal pain (5.7%), anorexia (2.7%), or chronic fatigue (5.3%). However, these
symptoms were not correlated with either the intensity of
infection (P ⳱ 0.84) or the major sonographic findings (P ⳱
0.98, Table 4).
DISCUSSION
The current study confirms that sonographic findings of the
liver (i.e., IHDD, IPDE, and GBS) are good diagnostic indicators for clonorchiasis. Of these findings, IHDD shows high
diagnostic accuracy regardless of intensity of infection, but
IPDE and GBS show high accuracy when the infection is
heavy. In a previous study, we suggested that the sonographic
findings of IPDE and GBS indicate active clonorchiasis but
lack sensitivity, and that IHDD is sensitive but not specific for
active clonorchiasis.8 Moreover, both studies indicate that the
diagnostic usefulness of sonography significantly depends on
infection intensity.
Sonographic findings mainly reflect resultant pathologic
changes of the bile duct or gallbladder in clonorchiasis. Studies that compared pathologic and radiologic findings in rabbits infected with C. sinensis disclosed that IHDD reflects bile
duct obstruction and dilatation by the flukes. Further, GBS
indicates the presence of the fluke, whereas IPDE is due to
periductal inflammation.11–13 Recently, the dynamic CT visualized a C. sinensis fluke itself in the intrahepatic bile duct and
also the bile duct changes.14
TABLE 3
Diagnostic usefulness of sonographic findings for determining the presence and intensity of Clonorchis sinensis infection
Sonographic findings by infection intensity
IHDD
Infection of any degree
Moderate or heavy infection
Heavy infection
IPDE
Infection of any degree
Moderate or heavy infection
Heavy infection
GBS
Infection of any degree
Moderate or heavy infection
Heavy infection
Sensitivity (%)
Specificity (%)
PPV
NPV
Diagnostic accuracy
75.5
84.6
91.1
82.2
47.3
39.6
96.9
61.0
34.7
31.8
76.0
92.7
76.3
65.8
53.0
27.2
38.8
50.1
95.3
89.4
84.6
97.6
78.2
53.4
15.4
60.0
82.8
35.5
64.5
75.6
23.0
32.9
41.8
94.7
91.0
86.6
96.9
78.1
52.4
14.6
58.2
80.8
31.7
62.3
74.9
PPU, positive predictive value; NPU, negative predictive value; IHDD, intrahepatic duct dilatation; IPDE, increased periductal echo; GBS, gallbladder sludge.
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TABLE 4
Number of subjects complaining symptoms according to major sonographic findings
No. (%) with IHDD
No. (%) with IPDE
No. (%) with GBS
Symptoms
Positive (N ⳱ 379)
Negative (N ⳱ 134)
Positive (N ⳱ 125)
Negative (N ⳱ 388)
Positive (N ⳱ 104)
Negative (N ⳱ 409)
Epigastic fullness
Abdominal pain
Anorexia
Chronic fatigue
26 (6.9%)
24 (6.3%)
10 (2.6%)
23 (6.1%)
13 (9.7%)
5 (3.7%)
4 (3.0%)
4 (3.0%)
11 (8.8%)
7 (5.6%)
4 (3.2%)
5 (4.0%)
28 (7.2%)
22 (5.7%)
10 (2.6%)
22 (5.7%)
9 (8.7%)
6 (5.8%)
4 (3.8%)
5 (4.8%)
30 (7.3%)
23 (7.4%)
10 (2.4%)
22 (5.4%)
IHDD, intrahepatic duct dilatation; IPDE, increased periductal echo; GBS, gallbladder sludge.
Because pathologic changes reflect severity and chronicity
of clonorchiasis, sonographic findings were also correlated
with the intensity and duration of C. sinensis infection. The
sonographic finding of IHDD was more frequently found in
heavily than in lightly infected rabbits (50% versus 12% at
week 3 and 100% versus 65% at week 12).12 A significant
correlation between infection intensity and the severities of
the gallbladder and bile duct lesions by sonography was also
reported in a human study of opisthorchiasis.15
Hereby, we assessed the diagnostic usefulness of sonography for clonorchiasis in 3 steps. First, we evaluated the accuracy of sonographic findings by their degree. The major sonographic findings of Grade 2 or higher were then selected.
Second, the diagnostic accuracies of the sonographic findings
of Grade 2 or higher were re-evaluated with respect to infection intensity. The diagnostic accuracy of IHDD was 76.3%
for the presence of clonorchiasis, but that of IPDE or GBS
was low. In heavy infections of EPG over 2,001, however,
IPDE and GBS showed higher diagnostic accuracies. Finally,
the diagnostic accuracies of sonographic findings (Grade 2
or higher) and of their combinations for the presence of
infection were evaluated. However, no other finding or combination of the findings had a higher accuracy than IHDD
Grade 2.
On comparing the sonographic findings in egg negative
Zhaoyuan residents and in controls, we found that IHDD,
IPDE, and GBS were significantly more frequent in the endemic group. This finding demonstrates that the sonographic
findings suggesting clonorchiasis can be found in egg negatives in high endemic areas, which is probably attributable to
past infection or to a false negative fecal examination.7,8,10,13
Moreover, as our subjects from the nonendemic control area
have never been exposed to C. sinensis, the presence of
IHDD and GBS among them suggests that these findings may
be caused by conditions other than clonorchiasis although
their frequency was very low.
Among the subjects in an endemic area who were evaluated for clinical symptoms, 21.1% reported one or more
symptoms. However, their symptoms bore no relationship
with infection intensity or major sonographic findings. These
findings demonstrate that the clinical symptoms of C. sinensis
infection are non-specific and subjective, and that most of the
infected residents are asymptomatic until serious complications occur.
In the current study, 87.8% of the Zhaoyuan residents examined were egg positive by the Kato-Katz method. Zhaoyuan is located in the middle of the highest endemic zone in
Northeast China. Males showed a higher egg positive rate and
heavier infection intensities than females, which is consistent
with other epidemiologic studies on clonorchiasis. The egg
positive rate by age among Zhaoyuan residents was highest in
the 30s (91.9%), and the egg counts were highest in the 50s. In
a study conducted in 1983 in Gimhae, which has the highest
prevalence of clonorchiasis in Korea, egg positivity increased
by age until the 50s and then reduced.1 This increase with age
is regarded to be the result of an accumulation due to the long
life span of C. sinensis, and the observed decrease beyond the
50s is attributed to a higher death rate among the infected
people.3 Zhaoyuan represents a hyperendemic state of natural equilibrium, and thus highest prevalence was observed in
the 50s. In such an endemic area of clonorchiasis, sonographic
screening of the liver is important and essential to detect any
hidden cholangiocarcinoma as its complication.16
In conclusion, IHDD, IPDE, and GBS may be useful sonographic findings, as they show significant correlations with the
prevalence and intensity of C. sinensis infection. However,
IHDD is an indicator of clonorchiasis whereas the presence of
IPDE or GBS is suggestive of heavy infection. Moreover,
clinical symptoms appear to be unrelated with either infection
intensity or sonographic findings.
Received November 26, 2004. Accepted for publication July 27, 2005.
Financial support: This study was supported by a research grant from
the Korea Research Foundation, KRF-2003-042-E00034 (2003).
Authors’ addresses: Moon Seok Choi, Department of Medicine, Samsung Medical Center, Sungkyunkwan University School of Medicine,
50 Irwon-Dong, Gangnam-Gu, Seoul 135-710, Korea, Telephone: 822-3410-3409, Fax: 82-2-3410-3849, E-mail: [email protected]
.co.kr. Dongil Choi, Department of Radiology, Samsung Medical
Center, Sungkyunkwan University School of Medicine, 50 IrwonDong, Gangnam-Gu, Seoul 135-710, Korea, Telephone: 82-2-34102518, Fax: 82-2-3410-2559, E-mail: [email protected]. MinHo Choi, Department of Parasitology and Tropical Medicine, and
Institute of Endemic Diseases, Seoul National University, College of
Medicine, 28 Yongon-Dong, Jongno-Gu, Seoul 110-799, Korea, Telephone: 82-2-740-8341, Fax: 82-2-765-6142, E-mail: [email protected].
Zhuo Ji and Zhimin Li, Department of Parasitology and Entomology,
Heilongjiang Province Center for Disease Control and Prevention,
Xiangfang-qiu, Harbin, Heilongjiang Province, China, Telephone: 82451-5566-4031, Fax: 82-451-5565-1447. Seung-Yull Cho, Department
of Molecular Parasitology, Sungkyunkwan University School of
Medicine, Suwon 440-746, Korea, Telephone: 82-31-299-6250, Fax:
82-31-293-3813, E-mail: [email protected]. Kwang-Seon Hong,
Bureau of Health Promotion, Korea Association of Health Promotion, Seoul, 157-704, Korea, Telephone: 82-2-2601-6144, Fax: 82-22690-4905, E-mail: [email protected]. Han-Jong Rim, Korea Association of Health Promotion, Seoul, 157-704, Korea, Telephone:
82-2-2601-6141, Fax: 82-2-2690-4905. Sung-Tae Hong, Department of
Parasitology and Tropical Medicine, and Institute of Endemic Diseases, Seoul National University, College of Medicine, 28 YongonDong, Jongno-Gu, Seoul 110-779, Korea, Telephone: 82-2-740-8343,
Fax: 82-2-765-6142, E-mail: [email protected].
Reprint requests: Sung-Tae Hong, Department of Parasitology and
Tropical Medicine, and Institute of Endemic Diseases, Seoul National University College of Medicine, 28 Yongon-Dong, Jongno-Gu,
Seoul 110-779, Korea, Telephone: 82-2-740-8343, Fax: 82-2-765-6142,
E-mail: [email protected].
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