INTRODUCTION
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.
MATERIALS AND METHODS
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 ≥ 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 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.
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.
Statistical analysis was performed using the χ2 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 ≥ 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 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 non-endemic 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
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.
Egg positive rates and intensities of Clonorchis sinensis infection by age
| Egg positive | ||||
|---|---|---|---|---|
| Age | Total | N | % | EPG* |
| * Numbers of eggs per gram of feces, mean ± SE. | ||||
| 0–9 | 12 | 6 | 50.0 | 62 ± 24 |
| 10–19 | 146 | 119 | 81.5 | 1,566 ± 428 |
| 20–29 | 223 | 205 | 91.9 | 4,161 ± 1,107 |
| 30–39 | 410 | 361 | 88.0 | 3,210 ± 360 |
| 40–49 | 352 | 317 | 90.1 | 4,485 ± 925 |
| 50–59 | 169 | 146 | 86.4 | 3,676 ± 890 |
| 60+ | 72 | 61 | 84.7 | 3,505 ± 954 |
| Total | 1,384 | 1,215 | 87.8 | 3,559 ± 339 |
Number of subjects by grades of major sonographic findings according to the intensity of Clonorchis sinensis infection
| No. with IHDD | No. with IPDE | No. with GBS | |
|---|---|---|---|
| Fecal examination | Grade 1*/2/3/4 | Grade 1*/2/3/4 | Grade 1*/2/3 |
| IHDD, intrahepatic duct dilatation; IPDE, increased periductal echo; GBS, gallbladder sludge. * Grade 1 means negative of the sonographic finding. | |||
| Egg negative, N = 169 | 139/23/5/2 | 161/7/1/0 | 160/8/1 |
| Egg positive | |||
| Light infection, N = 532 | 193/255/81/3 | 466/65/12/0 | 478/53/1 |
| Moderate infection, N = 322 | 73/145/89/15 | 238/76/7/1 | 248/66/8 |
| Heavy infection, N = 361 | 32/86/170/73 | 180/158/23/0 | 210/132/19 |
Diagnostic usefulness of sonographic findings for determining the presence and intensity of Clonorchis sinensis infection
| Sonographic findings by infection intensity | Sensitivity (%) | Specificity (%) | PPV | NPV | Diagnostic accuracy |
|---|---|---|---|---|---|
| PPU, positive predictive value; NPU, negative predictive value; IHDD, intrahepatic duct dilatation; IPDE, increased periductal echo; GBS, gallbladder sludge. | |||||
| IHDD | |||||
| Infection of any degree | 75.5 | 82.2 | 96.9 | 31.8 | 76.3 |
| Moderate or heavy infection | 84.6 | 47.3 | 61.0 | 76.0 | 65.8 |
| Heavy infection | 91.1 | 39.6 | 34.7 | 92.7 | 53.0 |
| IPDE | |||||
| Infection of any degree | 27.2 | 95.3 | 97.6 | 15.4 | 35.5 |
| Moderate or heavy infection | 38.8 | 89.4 | 78.2 | 60.0 | 64.5 |
| Heavy infection | 50.1 | 84.6 | 53.4 | 82.8 | 75.6 |
| GBS | |||||
| Infection of any degree | 23.0 | 94.7 | 96.9 | 14.6 | 31.7 |
| Moderate or heavy infection | 32.9 | 91.0 | 78.1 | 58.2 | 62.3 |
| Heavy infection | 41.8 | 86.6 | 52.4 | 80.8 | 74.9 |
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) |
| IHDD, intrahepatic duct dilatation; IPDE, increased periductal echo; GBS, gallbladder sludge. | ||||||
| Epigastic fullness | 26 (6.9%) | 13 (9.7%) | 11 (8.8%) | 28 (7.2%) | 9 (8.7%) | 30 (7.3%) |
| Abdominal pain | 24 (6.3%) | 5 (3.7%) | 7 (5.6%) | 22 (5.7%) | 6 (5.8%) | 23 (7.4%) |
| Anorexia | 10 (2.6%) | 4 (3.0%) | 4 (3.2%) | 10 (2.6%) | 4 (3.8%) | 10 (2.4%) |
| Chronic fatigue | 23 (6.1%) | 4 (3.0%) | 5 (4.0%) | 22 (5.7%) | 5 (4.8%) | 22 (5.4%) |
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.
Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 73, 6; 10.4269/ajtmh.2005.73.1139
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.
Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 73, 6; 10.4269/ajtmh.2005.73.1139
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.
Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 73, 6; 10.4269/ajtmh.2005.73.1139
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.
Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 73, 6; 10.4269/ajtmh.2005.73.1139
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.
Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 73, 6; 10.4269/ajtmh.2005.73.1139
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.
Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 73, 6; 10.4269/ajtmh.2005.73.1139
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.
Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 73, 6; 10.4269/ajtmh.2005.73.1139
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.
Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 73, 6; 10.4269/ajtmh.2005.73.1139
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.
Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 73, 6; 10.4269/ajtmh.2005.73.1139
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).
Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 73, 6; 10.4269/ajtmh.2005.73.1139
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).
Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 73, 6; 10.4269/ajtmh.2005.73.1139
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).
Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 73, 6; 10.4269/ajtmh.2005.73.1139
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: hst@snu.ac.kr.
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: 82-2-3410-3409, Fax: 82-2-3410-3849, E-mail: mschoi@smc.samsung.co.kr. Dongil Choi, Department of Radiology, Samsung Medical Center, Sungkyunkwan University School of Medicine, 50 Irwon-Dong, Gangnam-Gu, Seoul 135-710, Korea, Telephone: 82-2-3410-2518, Fax: 82-2-3410-2559, E-mail: dichoi@smc.samsung.co.kr. Min-Ho 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: mhchoi@snu.ac.kr. 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: 82-451-5566-4031, 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: seungyl@med.skku.ac.kr. Kwang-Seon Hong, Bureau of Health Promotion, Korea Association of Health Promotion, Seoul, 157-704, Korea, Telephone: 82-2-2601-6144, Fax: 82-2-2690-4905, E-mail: kah6144@yahoo.co.kr. 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 Yongon-Dong, Jongno-Gu, Seoul 110-779, Korea, Telephone: 82-2-740-8343, Fax: 82-2-765-6142, E-mail: hst@snu.ac.kr.
Financial support: This study was supported by a research grant from the Korea Research Foundation, KRF-2003-042-E00034 (2003).
REFERENCES
- 1↑
Rim HJ, 1986. The current pathobiology and chemotherapy of clonorchiasis. Korean J Parasitol 24S :7–121.
- 2
Chen M, Lu Y, Hua X, Mott KE, 1994. Progress in assessment of morbidity due to Clonorchis sinensis infection: a review of recent literature. Trop Dis Bull 91 :R7–R65.
- 3↑
Hong ST, 2003. Clonorchis sinensis. Miliotis MD, Bier JW, eds. International Handbook of Foodborne Pathogens. New York: Marcel Dekker, 581–592.
- 4↑
Choi BI, Han JK, Hong ST, Lee KH, 2004. Clonorchiasis and cholangiocarcinoma: etiologic relationship and imaging diagnosis. Clin Microbiol Rev 17 :540–552.
- 5↑
Hong ST, Choi MH, Kim CH, Chung BS, Ji Z, 2003. The Kato-Katz method is reliable for diagnosis of Clonorchis sinensis infection. Diagn Microbiol Infect Dis 47 :345–347.
- 6↑
Choi MH, Park IC, Li S, Hong ST, 2003. Excretory-secretory antigen is better than crude antigen for the serodiagnosis of clonorchiasis by ELISA. Korean J Parasitol 41 :35–39.
- 7↑
Lim JH, Ko YT, Lee DH, Kim SY, 1986. Clonorchiasis: sonographic findings in 59 proved cases. AJR 152 :761–764.
- 8↑
Choi D, Hong ST, Lim JH, Cho SY, Rim HJ, Ji Z, Yaun R, Wang S, 2004. Sonographic findings of active Clonorchis sinensis infection. J Clin Ultrasound 32 :17–23.
- 9↑
Choi MH, Ryu JS, Lee M, Li S, Chung BS, Chai JY, Sithithaworn P, Tesana S, Hong ST, 2003. Specific and common antigen of Clonorchis sinensis and Opisthorchis viverrini (Opisthorchidae, Trematoda). Korean J Parasitol 41 :155–163.
- 10↑
Hong ST, Yoon K, Lee M, Seo M, Choi MH, Sim JS, Choi BI, Yun CK, Lee SH, 1998. Control of clonorchiasis by repeated praziquantel treatment and low diagnostic efficacy of sonography. Korean J Parasitol 36 :249–254.
- 11↑
Ryu KN, Kim JH, Bho YJ, Yang MH, 1993. Comparative study of radiologic-pathologic study of experimental clonorchiasis in rabbits. J Korean Radiol Soc 29 :1–8.
- 12↑
Hong ST, Park KH, Seo M, Choi BI, Chai JY, Lee SH, 1994. Correlation of sonographic findings with histopathological changes of the bile ducts in rabbits infected with Clonorchis sinensis. Korean J Parasitol 32 :223–230.
- 13↑
Choi D, Hong ST, Li S, Chung BS, Lim JH, Lee SH, 2004. Bile duct changes in rats reinfected with Clonorchis sinensis. Korean J Parasitol 42 :7–17.
- 14↑
Lee KH, Hong ST, Han JK, Yoon CJ, Lee S, Kim SH, Choi BI, 2003. Experimental clonorchiasis in dogs: CT findings before and after treatment. Radiology 228 :131–138.
- 15↑
Mairiang E, Elkins D, Mairiang P, Chaiyakum J, Chamadol N, Loapaiboon V, Posri S, Sithithaworn S, Haswell-Elkins M, 1992. Relationship between intensity of Opisthorchis viveririni infection and hepatobiliary disease detected by ultrasonography. J Gastroenterol Hepatol 7 :17–21.
- 16↑
Choi D, Lim JH, Hong ST, 2004. Relation of cholangiocarcinomas to clonorchiasis and bile duct stones. Abdom Imaging 29 :590–597.