Epidemiological study of clonorchiasis and metagonimiasis along the Geum-gang (River) in Okcheon-gun (County), Korea

Gye-Sung Lee; In-Sung Cho; Young-Ha Lee; Hyung-Jun Noh; Dae-Whan Shin; Sok-Goo Lee; Tae-Yong Lee

doi:10.3347/kjp.2002.40.1.9

Korean J Parasito > Volume 40(1):2002 > Article

Lee, Cho, Lee, Noh, Shin, Lee, and Lee: Epidemiological study of clonorchiasis and metagonimiasis along the Geum-gang (River) in Okcheon-gun (County), Korea

Original Article

The Korean Journal of Parasitology 2002; 40(1): 9-16.

Published online: March 31, 2002

DOI: https://doi.org/10.3347/kjp.2002.40.1.9

Epidemiological study of clonorchiasis and metagonimiasis along the Geum-gang (River) in Okcheon-gun (County), Korea

Gye-Sung Lee¹, In-Sung Cho², Young-Ha Lee³, Hyung-Jun Noh³, Dae-Whan Shin³, Sok-Goo Lee⁴, Tae-Yong Lee⁴

¹Department of Internal Medicine, Sun General Hospital, Daejeon 301-131, Korea.

²Department of Internal Medicine, Eulji University School of Medicine, Daejeon 301-131, Korea.

³Department of Parasitology, College of Medicine, Chungnam National University, Daejeon 301-131, Korea.

⁴Department of Preventive Medicine, College of Medicine, Chungnam National University, Daejeon 301-131, Korea.

Corresponding author (yhalee@cnu.ac.kr)

Received January 07, 2002 Accepted February 16, 2002

Abstract

The endemic status of clonorchiasis and metagonimiasis along the Geum-gang (River) in Okcheon-gun (County) in Korea was examined. From February to December 2000, stools of total 1,081 inhabitants living in 5 villages were examined. Each stool specimen was examined by both the cellophane thick smear method and the formalin-ether sedimentation technique. Egg-positive cases were further analyzed by Stoll's egg-counting technique, and praziquantel was administered to positive cases. The egg-positive rates for Clonorchis sinensis and Metagonimus species were 9.3% and 5.5%, respectively, and the double infection rate was 3.5%. The numbers of eggs per gram (EPG) of feces of C. sinensis and Metagonimus sp. were 918±1,463 and 711±947, respectively. The egg-positive rates for C. sinensis and Metagonimus sp. in the riverside area were 14.2% and 8.4%, respectively, which were significantly higher than those of the inland area (3.2% and 1.7%, respectively). The egg-positive rates of C. sinensis and Metagonimus sp. in males (16.7% and 10.0%) were significantly higher than those of females (3.5% and 1.8%). However, there were no significant differences of EPG values between localities and sexes. The prevalence of clonorchiasis and metagonimiasis in this survey was significantly lower than that in the previous reports. However, there is still a high prevalence of infection with C. sinensis and Metagonimus sp. in this region, especially in the riverside area.

Key words: Clonorchis sinensis, Metagonimus sp., epidemiology, Okcheon-gun

INTRODUCTION

In the past, parasitic infections were regarded as a major public health problem in Korea. Over the past three decades, the prevalence of such infections has been decreasing rapidly, accompanied by an increase in the GNP, improvements in sanitation and hygiene, changes in agricultural management, and a nationwide control plan (Cho, 1994; Rim, 1997). Infection by soil-transmitted helminths, such as Ascaris and Trichuris, decreased dramatically: the egg-positive rates for these parasites were 13.0-23.4% in 1981 and 0.04-0.06% in 1997 (MHW and KAH, 1997). However, the pattern of prevalence of snail-transmitted trematode infections seems to be quite different from that of soil-transmitted helminth infections. The nationwide egg-positive rates for Clonorchis sinensis and Metagonimus sp. were 2.6% and 1.2% in 1981, and 1.4% and 0.3% in 1997, respectively (MHW and KAH, 1997). These data show that clonorchiasis and metagonimiasis are still common parasitic diseases in Korea.

C. sinensis, the liver fluke, is a well-known parasite that is of major public health importance in Korea and several other Asian countries. Infection with C. sinensis occurs by eating uncooked freshwater fish that harbors the metacercariae. In Korea, human infection has been shown to have a high prevalence along several major Korean rivers (Seo et al., 1981; Kim et al., 1994; Rim, 1997). The Geum-gang (River) basin is a well-known endemic area, where the prevalence of clonorchiasis over the last two decades has been in the range of 30.8 to 50.7% (Chang, 1979; Seo et al., 1981; Kim et al., 1994). Metagonimiasis is a fish-borne trematodiasis that is also of medical importance in Korea; it is endemic along the southern and eastern coasts (Seo et al., 1981; Kim et al., 1987; Chai et al., 1993 and 2000). In addition to these areas, the Geum-gang (River) basin, western coastal areas, and the Namhan-gang (River) basin have also been reported to be endemic areas (Kim 1980; Chai et al., 1993; Kim et al., 1994).

Even today, snail-transmitted trematodes infections are the most significant parasitic diseases in Korea, especially in rural and riverside areas, and the Geum-gang basin is an endemic area for clonorchiasis and metagonimiasis. Although there have been a few surveys of the prevalence of snail-transmitted trematode infection in this area in the past (Chang, 1979; Kim, 1980; Seo et al., 1981; Kim et al., 1987; Kim et al., 1994), there is no up-to-date survey reports. Therefore, we examined the endemicity and intensity of infection by C. sinensis and Metagonimus sp. in inhabitants of Okcheon-gun (County) living near the Geum-gang (River), and also obtained the follow up results after treatment of C. sinensis-positive cases with praziquantel.

MATERIALS AND METHODS

Area surveyed and population

This epidemiological study was undertaken during the period of February to December 2000. Total of 1,081 inhabitants (479 males, 602 females) of 5 villages in Okcheon-gun in Chungcheongbuk-do (Province), Korea, were examined. The subject villages were divided into riverside and inland areas. Subug-ri Okcheon-eup, Yegog-ri Cheongsan-myeon, and Usan-ri Dongyi-myeon belonged to the riverside area, which is within 2 km of the main channel of the Geum-gang. Okgag-ri Okcheon-eup and Eunhaeng-ri Gunseo-myeon were in the inland area which is farther than 5 km from the main channel of the river (Fig. 1). The age of the subject population ranged from 7 to 88 years, and the average age was 56.9±15.2 years (Table 1).

Stool examination and treatment of C. sinensis egg-positive cases

Fecal specimens were collected during the period of February and April 2000 from 1,081 inhabitants, including both sexes and all age groups, residing in the five villages (Table 1). The specimens were examined once each by the cellophane thick smear method (Kato's method) and the formalin-ether sedimentation (FES) technique.

After the fecal examination, Stoll's egg-counting technique was applied to specimens that were positive for the eggs of C. sinensis or Metagonimus sp.. Based on the eggs per gram of feces (EPG), the specimens were classified as Grade I (EPG 100-900), Grade II (EPG 1,000-4,900), Grade III (EPG 5,000-9,900) and Grade IV (EPG over 10,000) as described in previous reports (Cho 1994). C. sinensis egg-positive inhabitants were treated with 75 mg/kg praziquantel, administered as three 25mg/kg doses on a single day in August 2000. Stool samples of those treated were collected in November 2000, and the infection status of clonorchiasis was again examined by both the cellophane thick smear method and the FES technique.

Statistical analysis

We used SPSS 10.0 software to analyze the data from these experiments. The chi-square test and Student's t-test were used to check for statistical differences. Differences between two groups were considered significant when the p value was < 0.05.

RESULTS

Analysis of positive cases for eggs of C. sinensis or Metagonimus sp.

The results obtained from the stool examinations are summarized in Tables 2 and 3. The overall egg-positive rates for C. sinensis and Metagonimus sp. were 9.3% (101 cases) and 5.5% (59 cases), respectively. The rate of double infection with both parasites was 3.5% (38 cases). Among the 101 C. sinensis-positive cases, 99 were identified by the FES technique, 94 were detected by the cellophane thick smear method, and 92 were identified by both methods. In the 59 cases positive for eggs of Metagonimus sp., 58 cases were identified by the FES technique, 51 were identified by the cellophane thick smear method, and 50 were identified by both methods. Beside clonorchiasis and metagonimiasis, three cases positive for eggs of Ascaris lumbricoides, two positive for Trichuris trichuria, and one cyst-positive case of Entamoeba histolytica were also found.

As shown in Table 2, the egg-positive rates for C. sinensis by locality ranged from 3.0% in Eunhaeng-ri Geunseo-myeon to 19.4% in Usan-ri Dongyi-myeon. The highest egg-positive rate for Metagonimus sp. was 10.7% in Yegog-ri Cheongsan-myeon, whereas the lowest was 1.1% in Okgag-ri Okcheon-eup. When we divided the subject areas by distance from the main channel of the Geum-gang (River), 14.2% of 605 inhabitants in the riverside area showed egg-positive for C. sinensis, whereas 3.2% of the inland residents examined were infected. The difference in the C. sinensis egg-positive rates between the two areas was significant (p < 0.0001). Similarly, a significant difference between the riverside and inland areas was also observed in the egg-positive rates for Metagonimus sp. (8.4% vs 1.7%, p < 0.0001).

In Fig. 2, the egg-positive rates for C. sinensis and Metagonimus sp. were significantly higher in males than in females (16.7% vs. 3.5% for C. sinensis infection; 10.0% vs. 1.8% for Metagonimus infection). The egg-positive rates for C. sinensis by age group ranged from 3.1 to 11.7%, and was the highest in subjects in their fifties (11.7%), followed by subjects in their forties (11.2%) (Table 3). In the cases of Metagonimus infection, subjects in their forties showed the highest egg-positive rate (7.6%).

EPG counts of cases positive for eggs of C. sinensis and Metagonimus sp.

The EPG counts of the 101 C. sinensis egg-positive cases ranged from 200 to 10,800, and the mean EPG was 918±1,463 (Table 2). The mean EPG for C. sinensis egg-positive cases in the riverside area was 967±1,565, whereas it was 640±561 in the inland area (p=0.426). When EPG values were classified by grade, 82.2% were Grade I, 13.9% Grade II, 3.0% Grade III, and 1.0% Grade IV (Table 4). The proportions of each EPG grade in males and females were 80.0% and 90.5% in Grade I, 16.3% and 4.8% in Grade II, 2.5% and 4.8% in Grade III, and 1.3% and 0.0% in Grade IV, respectively. The mean EPG of males was 1,005±1,535, whereas that of females was 590±1,121, and the difference was not significant (p=0.249) (Fig. 3).

In cases positive for the eggs of Metagonimus sp., the mean EPG was 711±947 (range, 200 to 5,400) (Table 2). The mean EPG of inhabitants of the riverside area was 760±1,010, which was higher than that of inhabitants of the inland area (400±151) (p=0.321). The proportions of Grade I, II, and III EPGs were 89.8, 6.8, and 3.4%, respectively (Table 4). In males, the proportions of Grade I, II, and III EPGs were 87.5, 8.3, and 4.2%, respectively. However, all the infected females had Grade I EPG. The mean EPGs of males and females were 775±1,040 and 436±150, respectively (p=0.289) (Fig. 3).

Follow up results of C. sinensis egg-positive cases after treatment

The 101 C. sinensis egg-positive inhabitants were administered an one-day oral dose of 3×25 mg/kg praziquantel. Three months later, stool samples were obtained from 85 of these cases. The samples were again examined by both the cellophane thick smear method and the FES technique. Five cases had C. sinensis eggs in their stools, while no parasites were found in the other 80 cases. The five positive cases were all male, and all had eaten raw freshwater fish after the praziquantel treatment.

DISCUSSION

Okcheon-gun lies in the Geum-gang (River) basin in Chungcheongbuk-do, Korea. Among the 1,081 inhabitants surveyed in this area, we found overall egg-positive rates of 9.3% for C. sinensis and 5.5% for Metagonimus sp.. The mean EPG counts for egg-positive cases were 918±1,463 and 711±947, respectively. The egg-positive rates for both snail-transmitted trematodes were significantly higher in both males or inhabitants of the riverside area than in other groups. These data show that the egg-positive rates for both parasites were significantly lower than those reported earlier in similar regions. However, this area still has a high prevalence of infection with these parasites.

The prevalence of soil-transmitted helminth infections in Korea has sharply decreased over the last three decades. The overall helminthes egg-positive rate was 84.3% in 1971, 41.1% in 1981, 3.8% in 1992, and 2.4% in 1997 (MHK and KAH, 1997). We also confirmed very low egg-positive rates of soil-transmitted helminthes; among the 1,081 subjects surveyed, only five cases of soil-transmitted helminthes were found. The egg-positive rates for C. sinensis decreased steadily from 4.6% in 1971, 2.6% in 1981, and 2.2% in 1992, to 1.4% in 1997 (MHK and KAH, 1997). A nationwide survey of clonorchiasis showed that endemic areas were scattered throughout the country along several major rivers, including the Geum-gang (River), and the most intensive endemic regions were mainly found along the Nakdong-gang (Seo et al., 1981; Rim, 1997). Clonorchiasis is a common infectious disease in Korea. For example, the yearly egg-positive rate for C. sinensis among outpatients nationally ranged from 2.3 to 3.9% between 1984 and 1992 (Lee et al., 1994), indicating the infection of this trematode infection in the general population.

The Geum-gang basin is one of the endemic regions for snail-transmitted trematode infections in Korea. The egg-positive rate for C. sinensis in Okcheon-gun was 50.7% in 1979 (Chang, 1979), 40.4% in 1994 (Kim et al., 1994), and 9.3% in the present study, confirming that the local prevalence of clonorchiasis has significantly decreased over the past 6 years. Whereas Kim et al. (1994) previously surveyed the riverside within 1 km of the main channel of the river, the present study examined both the riverside and the inland areas within 5 km from the main channel. Generally, the prevalence of C. sinensis is higher in males and in inhabitants living in rural areas, and increases with age (MHW and KAH, 1997; Rim, 1997). We also found that egg-positive rates were higher among inhabitants of the riverside area than in those of the inland area, and also higher in males than in females. Although the fifties were the highest egg-positive rates for C. sinensis in both riverside and inland areas, there were no significant differences of egg-positive rates among age groups, except the thirties. However, the egg-positive rates of the fifties or forties were significantly higher rates than that of the other age groups in the riverside areas, except age group of 0-9 years. The EPG counts were also much lower than those previously reported. In the Geum-gang basin, the mean EPG value was 5,760 (range, 100-26,600) in 1981 (Seo et al., 1981), whereas it was 918±1,463 in this study. The low EPG counts in this area may be due to the government-supported control program, which includes praziquantel treatment and health education. However, these EPG counts may not be enough to develop apparent clinical features in humans, thus they may have repeated to eat the raw fish. The EPG for Clonorchis in most cases with clinical symptoms and abnormal liver function tests is more than 10,000 (Rim et al., 1981).

Three species of Metagonimus are known to occur in Korea; M. yokogawai (Chai and Lee, 1990), M. miyatai (Kim et al., 1987; Chai et al., 1993), and M. takahashii (Chai and Lee, 1990). M. yokogawai is widely distributed in large and small rivers of the southern and eastern coasts of Korea (Seo et al., 1981; Chai et al., 2000). According to a previous survey along the Geum-gang basin, human infections with Metagonimus sp. different from M. yokogawai were first noticed by Kim (1980), and Kim et al. (1987) later reported it as Metagonimus Miyata type. In this study, we did not classify the species of Metagonimus. In the Geum-gang basin in Okcheon-gun, the egg-positive rate for Metagonimus sp. was 25.9 % in 1979 (Chang 1979) and 9.8% in 1994 (Kim et al., 1994). In this study, the egg-positive rate and EPG count for Metagonimus sp. were 5.5% and 711±947, which are lower than those observed in the previous reports (Chang, 1979; Kim, 1980; Seo et al., 1981; Kim et al., 1994).

Praziquantel is a very well tolerated drug; occasional side effects consist of mild and transient headache and dizziness. In this study, C. sinensis-positive cases were given 3×25 mg/kg in one day at the Okcheon-gun Public Health Center. Five of the 85 specimens collected after praziquantel treatment were positive for C. sinensis eggs. Treatment failure in these 5 cases was thought to be due to either an insufficient treatment dosage of the drug or reinfection after treatment. The most practical method of preventing human reinfection is to avoid eating raw or undercooked freshwater fishes. All five treatment failure cases had eaten raw freshwater fishes after praziquantel treatment.

Human infection with C. sinensis and Metagonimus sp. is usually acquired by eating uncooked fishes containing infectious metacercariae. The intensity of human infection is dependent upon the eating habits of the population. In rural and riverside areas of Korea, eating raw fish is a deeply rooted traditional custom. The results described in this study indicated that the overall prevalence for C. sinensis and Metagonimus infections in Okcheon-gun was significantly lower than that in the previous reports. However, this area still has high prevalence of clonorchiasis and metagonimiasis. Therefore, practical prevention or health education programs as well as mass chemotherapy are needed to reduce the prevalence of snail-transmitted trematodiasis in endemic areas.

REFERENCES

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Fig. 1

Map of the areas surveyed in Okcheon-gun, Chungcheongbuk-do, Korea. ①, Subug-ri Okcheon-eup; ②, Yegog-ri Cheongsan-myeon; ③, Usan-ri Dongyi-myeon; ④, Okgag-ri Okcheon-eup; ⑤, Eunhaeng-ri Gunseo-myeon.

Fig. 2

Egg positive rates of C. sinensis and Metagonimus sp. based on stool examination according to sex in Okcheon-gun, Chungcheongbuk-do

Fig. 3

EPG counts of egg positive cases of C. sinensis and Metagonimus sp. according to sex in Okcheon-gun, Chungcheongbuk-do. Cs males of C. sienesis egg positive cases; Cs female, females of C. sinensis egg positive cases; Cs total, both sexes of C. sineneis egg positive cases; My male, males of Metagonimus sp. egg positive cases; My female, females of Metagonimus sp. egg positive cases; My total, both sexes of Metagonimus sp. egg positive cases.

Table 1.

Locality, sex and age distribution of surveyed population in Okcheon-gun, Chungcheongbuk-do, Korea

Localities	Sex	No. of exam.	Age group (year)
Localities	Sex	No. of exam.	0-9	10-19	20-29	30-39	40-49	50-59	60-69	70-79	80-
Subug-ri	Male	130	2	2	3	5	17	27	40	26	8
Okcheon-eup^a)	Female	157	1	3	4	9	20	29	56	29	6
	Subtotal	287	3	5	7	14	37	56	96	55	14
Yegog-ri	Male	103	-	10	1	3	15	17	35	17	5
Cheongsan-myeon^a)	Female	122	-	3	-	2	18	29	45	22	3
	Subtotal	225	-	13	1	5	33	46	80	39	8
Usan-ri	Male	35	-	4	1	3	9	5	12	1	-
Dongyi-myeon^a)	Female	58	2	3	4	10	12	11	10	6	-
	Subtotal	93	2	7	5	13	21	16	22	7	-
Okgag-ri	Male	120	3	7	3	7	19	23	33	23	2
Okcheon-eup^b)	Female	158	10	10	5	8	20	29	41	27	8
	Subtotal	278	13	17	8	15	39	52	74	50	10
Eunhaeng-ri	Male	91	-	2	2	9	21	22	19	14	2
Gunseo-myeon^b)	Female	107	-	-	1	9	19	22	43	13	-
	Subtotal	198	-	2	3	18	40	44	62	27	2
Total	Male	479	5	25	10	27	81	94	139	81	17
	Female	602	13	19	14	38	89	120	195	97	17
	Total	1,081	18	44	24	65	170	214	334	178	34

^a) Riverside area; villages within 2 km from the main stream of Geum-gang (River).

^b) Inland area; villages 5 km apart from the main stream of Geum-gang (River).

Table 2.

Number of egg-positive cases and their EPG counts of C. sinensis and Metagonimus sp. depending on localities in Okcheon-gun, Chungcheongbuk-do

Localities	No. of cases Examined	C. sinensis		Metagonimus sp.
Localities	No. of cases Examined	Egg-positive cases^a)(%)	EPG counts of positive	Egg-positive cases (%)	EPG counts of positive
Riverside areas	605	86 (14.2)^b)	967 ± 1,565^c)	51 (8.4)	760 ± 1,010
Subug-ri Okcheon-eup	287	35 (12.2)	582 ± 516	20 (7.0)	520 ± 119
Yegog-ri Cheongsan-myeon	225	33 (14.6)	1,260 ± 2,002	24 (10.7)	841 ± 1,126
Usan-ri Dongyi-myeon	93	18 (19.4)	1,177 ± 1,913	7 (7.5)	1,171 ± 1,782
Inland areas	476	15 (3.2)^b)	640 ± 561	8 (1.7)	400 ± 151
Okgag-ri Okcheon-eup	278	9 (3.2)	688 ± 609	3 (1.1)	400 ± 200
Eunhaeng-ri Gunseo-myeon	198	6 (3.0)	566 ± 527	5 (2.5)	400 ± 141
Total	1,081	101 (9.3)	918 ± 1,463	59 (5.5)	711 ± 947

^a) Egg positive cases of stool examination were found eggs either by formalin-ether sedimentation technique or cellophane thick smear method (Kato’s method).

^b) The difference of egg positive rates between the riverside and inland areas was statistically significant (p<0.05).

^c) Mean±SD of EPG counts of egg positive cases.

Table 3.

Egg-positive cases of C. sinensis and Metagonimus sp. according to age group in Okcheon-gun, Chungcheongbuk-do, based on stool examination

Age group	No. of cases examined			Egg-positive cases of C. sinensis (%)			Egg-positive cases of Metagonimus sp.(%)
Age group	Riverside areas	Inland areas	Subtotal	Riverside areas	Inland areas	Subtotal	Riverside	Inland	Subtotal
0-9	5	13	18	1 (20.0)	-	1 (7.6)	-	-	-
10-19	25	19	44	3 (12.0)	1 (5.3)	4 (9.1)	1 (4.0)	-	3 (6.8)
20-29	13	11	24	1 (7.6)	1 (9.1)	2 (8.3)	-	1 (9.1)	1 (4.1)
30-39	32	33	65	1 (3.1)	1 (3.0)	2 (3.1)	-	-	-
40-49	91	79	170	17 (18.8)	2 (2.5)	19 (11.2)	12 (13.2)	1 (1.3)	13 (7.6)
50-59	118	96	214	23 (19.5)	2 (2.1)	25 (11.7)	9 (7.6)	2 (2.1)	11 (5.1)
60-69	198	136	334	25 (12.6)	5 (3.7)	30 (9.0)	19 (9.6)	2 (1.5)	21 (6.3)
70-79	101	77	178	10 (10.0)	5 (6.5)	15 (8.4)	6 (5.9)	2 (2.6)	8 (4.5)
80-	22	12	34	3 (13.6)	-	3 (8.8)	2 (9.1)	-	2 (5.9)
Total	605	476	1,081	86 (14.2)	15 (3.2)	101 (9.3)	51 (8.4)	8 (1.7)	59 (5.5)

Table 4.

EPG grade of C. sinensis and Metagonimus sp. egg-positive cases of surveyed population according to sex in Okcheon-gun, Chungcheongbuk-do

EPG grade^a)	Egg-positive cases of C. sinensis (%)			Egg-positive cases of Metagonimus sp. (%)
EPG grade^a)	Male	Female	Subtotal	Male	Female	Subtotal
Grade I	64 (80.0)	19 (90.5)	83 (82.2)	42 (87.5)	11 (100.0)	53 (89.8)
Grade II	13 (16.3)	1 (4.8)	14 (13.9)	4 (8.3)	-	4 (6.8)
Grade III	2 (2.5)	1 (4.8)	3 (3.0)	2 (4.2)	-	2 (3.4)
Grade IV	1 (1.3)	-	1 (1.0)	-	-	-
Total	80 (100.0)	21 (100.0)	101 (100.0)	48 (100.0)	11 (100.0)	59 (100.0)

^a) Grade I, EPG 100-900; Grade II, EPG 1,000-4,900; Grade III, EPG 5,000-9,900; Grade IV, over 10,000