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Original Article

Epidemiological Survey on the Infection of Intestinal Flukes in Residents of Muan-gun, Jeollanam-do, the Republic of Korea

Shin-Hyeong Cho1, Pyo-Yun Cho1, Dong-Min Lee1, Tong-Soo Kim2, In-Sang Kim3, Eun-Jung Hwang3, Byoung-Kuk Na4, Woon-Mok Sohn4
The Korean Journal of Parasitology 2010;48(2):133-138.
Published online: June 17, 2010

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Corresponding author (wmsohn@gnu.ac.kr)
• Received: April 26, 2010   • Revised: May 24, 2010   • Accepted: May 25, 2010

Copyright © 2010 by The Korean Society for Parasitology

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  • Infection status of intestinal flukes was investigated in residents of Muan-gun, Jeollanam-do, the Republic of Korea. Total 1,257 fecal samples of residents were examined by formalin-ether sedimentation technique and Kato-Katz thick smear method. Helminth eggs were detected from 95 (7.6%) residents, and eggs of heterophyid flukes and Clonorchis sinensis were found from 62 (4.9%) and 40 (3.2%) cases, respectively. The larger heterophyid eggs, somewhat dark-brown in color and 37.7 × 21.5 µm in average size, and found in 32 (2.6%) out of 62 egg positive cases of heterophyid flukes. To confirm the adult flukes, we performed worm recovery from 12 cases after praziquantel treatment and purgation with MgSO4. A total of 1,281 adult flukes, assigned to 7 species, were recovered from 9 cooperative cases. Heterophyes nocens (total 981 specimens) was collected from 9 cases, Stictodora fuscata (80) from 7, Gymnophalloides seoi (75) from 5, Pygidiopsis summa (140) from 3, Stellantchasmus falcatus (3) from 2, and Stictodora lari and Acanthotrema felis (each 1 worm) from 1 case each. The intrauterine eggs of S. fuscata collected from the recovered worm were identical with the larger heterophyid eggs detected in the stool examination. By the present study, it was confirmed that A. felis is a new intestinal fluke infecting humans, and residents in Muan-gun, Jeollanam-do are infected with variable species of intestinal trematodes.
  • Key words: Stictodora fuscata, Acanthotrema felis, intestinal trematode, resident, Muan-gun
It has been known that more than 50 million people are infected with intestinal trematodes, and about 70 trematode species are involved in human infections around the world [1]. In the Republic of Korea, 17 species of 5 families, i.e. Heterophyidae, Echinostomatidae, Plagiorchiidae, Neodiplostomidae, Gymnophallidae, have been listed as human-infecting intestinal trematodes. Among them, 10 species are members of Heterophyidae which is regarded as the most important group [2].
Muan-gun, Jeollanam-do, has been known as the endemic focus of heterophyid flukes together with some areas of south and west coasts. Among 10 species of human-infecting heterophyid flukes, 6 species, namely, Heterophyes nocens, Heterophyopsis continua, Pygidiopsis summa, Stellantchasmus falcatus, Stictodora fuscata, and Stictodora lari, are prevalent among residents who frequently consumed raw flesh of estuarine fish in the south and west coastal areas [1,2].
A Parasite Eradication Program (PEP) has been performed by the Division of Malaria and Parasitic Diseases, National Institute of Health (NIH), Korea Centers for Disease Control and Prevention (KCDCP) since 2005 [3]. The purpose of this program is to make an epoch-making decrease of helminth infections among residents in the city and province which revealed higher prevalence in the 7th report (2004) on the nationwide survey of the Republic of Korea [4,5]. The present study was carried out to investigate helminthic infections in residents of Muan-gun, Jeollanam-do, as a part of PEP-2007. Moreover, we intended worm recovery to know what species of intestinal flukes are infected among the residents in whom larger heterophyid eggs are detected in the stool examination.
A total of 1,257 fecal samples were collected from 9 administrative localities of Muan-gun, Jeollanam-do, in March 2007. Collected fecal samples were examined by the formalin-ether sedimentation technique and Kato-Katz method. To identify the adult worms of larger heterophyid eggs detected in the stool examination, we performed worm recovery on 12 out of 32 positive cases for larger heterophyid eggs after praziquantel (Shinpoong Pharmaceutical Co., Seoul, Korea) treatment and purgation with MgSO4 after obtaining informed consent from each person. Whole stools passed successively 3-5 times were collected from 9 helpful persons. After carrying out the methods generally used in the worm recovery [6], all samples were transported to the Department of Parasitology, Gyeongsang National University School of Medicine, and examined under a stereomicroscope. The recovered worms were fixed with 10% formalin under cover glass pressure, observed and measured under a light microscope using a micrometer. We also carried out questionnaire investigation on 12 residents selected for the worm recovery to know the infection sources of flukes recovered, and some related health problems.
Positive rates of helminth eggs in stool examination
Helminth eggs were detected in 95 (7.6%) of 1,257 fecal samples of residents examined. Among them, 9 people (0.7%) were infected with more than 2 species of helminths. Therefore, the number of cumulative egg positive cases was 104 (8.3%). Eggs of heterophyid flukes were found in 62 (4.9%) fecal samples of residents; Clonorchis sinensis in 40 cases (3.2%), and Trichuris trichiura and echinostomatid eggs in 1 person each. The larger heterophyid eggs were found in 32 (2.6%) of 62 heterophyid egg positive cases (Table 1).
Worm recovery from egg positive cases of heterophyid flukes
A total of 1,281 adult flukes, assigned to 7 species, were recovered from 9 cooperative residents after praziquantel treatment and purgation. H. nocens (total 981 specimens) was collected from all 9 cases, S. fuscata (80) from 7, G. seoi (75) from 5, P. summa (140) from 3, S. falcatus (3) from 2, and S. lari (1) and Acanthotrema felis (1) from 1 case each (Table 2).
Redescription of Stictodora fuscata recovered from humans

Eggs

The larger heterophyid eggs detected in stool examinations were 33-43 (38) × 20-25 (22) µm in size, having a thick and smooth shell, unconspicuous operculum, and miracidium (Fig. 1A, B).

Adults (n = 10)

Somewhat small and slender in shape, 850-1,380 (1,060 in average) µm long and 300-460 (380) µm wide (Fig. 1C). Oral sucker round, 70-88 (78) × 75-95 (87) µm in size. Prepharynx short, 50-70 (62) µm in length. Pharynx muscular, 68-90 (79) × 60-75 (70) µm in size. Esophagus slender, 55-80 (66) µm in length. Ceca somewhat wide, extended to posterior end of body. Ventrogenital sac ovoid, 50-88 (66) × 68-100 (79) µm in size, and armed with 15-18 gonotyl spines (Fig. 1D). Ovary transversely ovoid, 48-93 (57) × 63-138 (90) µm in size, and located just in front of right testis. Testes obliquely tandem and transversely elliptical, 45-125 (82) × 70-150 (110) µm in size, and located in posterior 1/3. Seminal vesicle constricted into 3-4 saccules, and located between gonotyl and ovary. Uterus distributed in posterior half of body, with many eggs. Intrauterine eggs oval, dark brown color, with thick shell and unconspicuous operculum, and 35-47 (39) × 20-26 (23) µm in size (Fig. 1E). Vitellaria distributed in peripheral area of post-testicular region.
Acanthotrema felis recovered from a human case
Body small, claviform, 656 × 287 µm in size (Fig. 2A). Oral sucker globular, 70 µm in diameter. Prepharynx short. Pharynx subglobular, 49 × 52 µm in size. Esophagus short, 25 µm long. Intestinal ceca terminate close to posterior end. Ventrogenital sac muscular, 94 × 71 µm in size, with 3 sclerotized pieces (Fig. 2B). The other reproductive organs were not clearly seen in a worm recovered because of it was damaged by praziquantel.
Findings obtained from the questionnaire investigation
Total 9 out of 12 residents selected for the worm recovery usually defecated mushy stools, but they have no other special gastrointestinal symptoms. Almost all enjoyed eating raw flesh of brackish water fish, i.e., common blackish goby, Acanthogobius flavimanus (66.7% of people); mullet, Mugil cephalus (41.7%); common sea bass, Lateolabrax japonicus (25.0%); gizzard shad, Konosirus punctatus (16.7%); blue-spotted mud hopper, Boleophthalmus pectinirostris (8.3%). Only 2 people (16.7%) answered that they like to eat raw oyster, Crassostrea gigas.
By the present study, it was confirmed again that Muan-gun in Jeollanam-do is an endemic focus of heterophyid fluke infections. Chai et al. [6] reported 75% egg positive rate of heterophyid flukes in the fecal examination of 108 residents in a small coastal village in Muan-gun. They recovered 4 species of heterophyid flukes, i.e., H. nocens, P. summa, H. continua, S. fuscata, and G. seoi from 20 heterophyid egg positive cases after praziquantel treatment and purgation [6]. In our study, only 62 (4.93%) out of 1,257 residents examined revealed egg positive results for heterophyid flukes. Six species of heterophyid flukes, i.e., H. nocens, S. fuscata, P. summa, S. falcatus, S. lari, and A. felis, and G. seoi, were recovered from 9 residents. The egg positive rate was much decreased, while the number of heterophyid species collected increased from 4 to 6 compared to a previous study [6].
H. nocens was the domimant species among the residents of Muan-gun. This fluke was recovered from all 9 cases examined, although the intensity of infection was a little lower in the present study (average worm burden; 109) than in Chai et al. [6] (average worm burden; 193). The dominancy of H. nocens infections has also been shown in the residents of Shinan-gun and Gangjin-gun (Jeollanam-do), Buan-gun (Jeollabuk-do), Sacheon-si (Gyeongsangnam-do), and western and southern coastal islands of the Republic of Korea [7-10].
In the fecal examination of the present study, larger heterophyid eggs were detected in 32 cases. They were 37.7 × 21.5 µm in average size, larger than eggs of other heterophyid flukes, including H. nocens, and their shell was somewhat thick and dark brown in color. S. fuscata adults were collected from 7 (77.8%) out of 9 residents in the worm recovery. Their uterine eggs were compatible with the larger heterophyid eggs detected in the fecal examination, and with those in the previously reported papers (Table 3) [11-13]. Therefore, researchers in the endemic areas of heterophyid flukes should pay attention to these larger eggs of heterophyid fluke, most probably S. fuscata.
Eggs of S. fuscata are definitely distinguished from similar trematode eggs, such as Eurytrema pancreaticum and Plagiorchis muris, in some morphological characters. Eggs of E. pancreaticum (large sized type; 53.6 × 33.0 µm in average; small sized type; 42.6 × 31.6 µm in average) are somewhat larger than those of S. fuscata, and they have thicker and deep dark-brown shells [14]. On the other hand, eggs of P. muris (34 × 22 µm in average) are broadly elliptical and more or less smaller than those of S. fuscata, and they have a conspicuous operculum and golden brown shell [15].
S. fuscata adults from a human infection case were described in the Republic of Korea under the name of Stictodora sp. by Chai et al. [12]. Worms described by Chai et al. [12] looked like somewhat deformed by drugs. Therefore, we redescribed with completely intact S. fuscata adults obtained from human cases in our study. They were more slender in body shape, when we compared with those from experimental cats [13]. Human infections with this fluke have been reported in about 18 cases so far [2,6,8-10]. Our study adds 7 cases confirmed by worm recovery and 25 egg-positive cases. In addition, G. seoi (5 cases), P. summa (3 cases), S. falcatus (2 cases), and S. lari (1 case) cases were added by the present study.
A. felis was originally described based on the specimens recovered from the small intestine of stray cats in the Republic of Korea [16]. The common blackish goby, A. flavimanus, has been confirmed to act as a second intermediate host [17]. Only the cat has been known as its natural definitive host. Therefore, it was confirmed for the first time that this fluke is a human-infecting species by the present study. In case of the other species of Acanthotrema, A. tanayensis and A. tridactyla were recovered from cats, A. cursitans from rodents, and A. martini, A. acanthotrema, A. armata, A. tridactyla and A. hancocki were found from avian hosts [18-21].
Residents selected for the worm recovery were all aged people in this study. Although they were heavily infected with intestinal flukes, they did not complain any special gastrointestinal symptoms. This phenomenon can be explained as that aged people have more chances to eat raw flesh of estuarine fish, and they are continuously reinfected with intestinal flukes in endemic areas. Some species of estuarine fish, such as L. japonicus, Clupanodon punctatus, M. cephalus, and A. flavimanus, have been reported as sources of human infections in endemic areas of heterophyid flukes [2]. Surveys on these fish intermediate hosts have been performed in southwestern coastal areas [13,22-26]. Nevertheless, more systematic surveys should be done to reveal the variety of fish hosts from endemic areas, especially Muangun, Jeollanam-do.
This study was supported by an Anti-Communicable Diseases Control Program of the National Institute of Health (NIH 348-6111-215), Ministry of Health and Welfare, the Republic of Korea. We thank Miss A-Ra Cho and Hae-In Ryu, Department of Parasitology, Gyeongsang National University School of Medicine, Jinju, Korea, for their help in the worm recovery and questionnaire investigation.
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  • 18. Lafuente M, Roca V, Carbonell E. Description of Acanthotrema armata n. sp. (Trematoda: Heterophyidae) from Larus audouinii (Aves: Laridae), with an amended diagnosis of the genus Acanthotrema Travassos, 1928. Syst Parasitol 2000;45:131-134.
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  • 22. Seo BS, Hong ST, Chai JY, Cho SY. Studies on intestinal trematodes in Korea. IV. Geographical distribution of Pygidiopsis and Heterophyes metacercariae. Seoul J Med 1981;22:236-242.
  • 23. Chai JY, Park SK, Hong SJ, Choi MH, Lee SH. Identification of Stictodora lari (Heterophyidae) metacercariae encysted in the brackish water fish, Acanthogobius flavimanus. Korean J Parasitol 1989;27:253-259.
  • 24. Sohn WM, Moon BC. Infection status with the metacercariae of heterophyid trematode in mullet and goby collected from western coastal areas of Cholla-do, Korea. J Biomed Lab Sci 2001;7:31-37.
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  • 26. Sohn WM, Na BK, Cho SH. Echinostoma hortense and heterophyid metacercariae encysted in yellowfin goby, Acanthogobius flavimanus, from Shinan-gun and Muan-gun (Jeollanam-do), Korea. Korean J Parasitol 2009;47:307-310.
Fig. 1
Eggs and an adult of Stictodora fuscata (A, B). Eggs detected in stool examinations by formalin-ether sedimentation technique (A) and Kato-Katz method (B) (scale bar = 20 µm). They have thick and smooth shells and unconspicuous operculum. (C) An adult worm recovered from a case positive for larger heterophyid eggs (scale bar = 500 µm). It is somewhat small and slender in shape, and has round oral sucker (OS), muscular pharynx (P), ventrogenital sac (circle), elliptical ovary (O), and 2 testes (RT: right testis; LT: left testis). (D) Characteristic ventrogenital sac (magnified view of round circle in Fig. 1C) armed with about 16 gonotyl spines (scale bar = 40 µm). (E) Intrauterine eggs are oval in shape, dark brown color, with thick shell and unconspicuous operculum (scale bar = 20 µm).
kjp-48-133-g001.jpg
Fig. 2
An adult of Acanthotrema felis recovered from a resident of Muan-gun, Jeollanam-do (scale bar = 200 µm). It is small and has a round oral sucker (OS), a muscular pharynx (P), and a ventrogenital sac (round circle). (B) Magnified view of the characteristic ventrogenital sac armed with 3 large sclerites (scale bar = 40 µm).
kjp-48-133-g002.jpg
Table 1.
Helminth egg positive rates in the feces of residents in Muan-gun, Jeollanam-do, Korea
Table 1.
Items and helminth species No. of cases (%)
No. examined 1,257
No. of helminth egg positive cases 95 (7.6)
No. of cumulative egg positive cases 104 (8.3)
Heterophyidsa) 62 (4.9)
Clonorchis sinensis 40 (3.2)
Echinostome 1 (0.08)
Trichuris trichiura 1 (0.08)
C. sinensis + heterophyids 7 (0.56)
Echinostome + heterophyids 1 (0.08)
T. trichiura + heterophyids 1 (0.08)

aNo. of larger heterophyid egg positive cases: 32 (2.6%).

Table 2.
Results of worm collection from positive cases of larger heterophyid eggs after praziquantel treatment
Table 2.
Resident (Age/sex) No. of worms collected
H. nocens P. summa S. falcatus S. fuscata S. lari A. felis G. seoi
75/M 43 1 - 10 - - 3
73/M 93 - - 7 - - -
70/F 33 1 - 2 - - -
70/F 148 - 1 30 1 1 65
67/M 56 - - - - - 3
65/F 15 - - 3 - - 3
63/M 488 - 2 5 - - 1
60/F 101 138 - 23 - - -
57/F 4 - - - - - -
Total 981 140 3 80 1 1 75
Table 3.
Comparison of Stictodora fuscata eggs with those of previous studies
Table 3.
Authors Size of eggs (average)
Present study (2010)
Eggs in fecal specimens (n = 30) 33.8-42.5 (37.7) × 20.0-25.0 (21.5) μm
Eggs in the uterus of worms (n = 20) 35.0-47.5 (39.1) × 20.0-26.3 (22.5) μm
Onji and Nishio (1924) 35-37 × 22-24 μm
Chai et al. (1988) 34-38 × 20-23 μm
Sohn et al. (1994) 32-38 (35) × 19-23 (20) μm

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Epidemiological Survey on the Infection of Intestinal Flukes in Residents of Muan-gun, Jeollanam-do, the Republic of Korea
Korean J Parasitol. 2010;48(2):133-138.   Published online June 17, 2010
DOI: https://doi.org/10.3347/kjp.2010.48.2.133
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Epidemiological Survey on the Infection of Intestinal Flukes in Residents of Muan-gun, Jeollanam-do, the Republic of Korea
Korean J Parasitol. 2010;48(2):133-138.   Published online June 17, 2010
DOI: https://doi.org/10.3347/kjp.2010.48.2.133
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Epidemiological Survey on the Infection of Intestinal Flukes in Residents of Muan-gun, Jeollanam-do, the Republic of Korea
Image Image
Fig. 1 Eggs and an adult of Stictodora fuscata (A, B). Eggs detected in stool examinations by formalin-ether sedimentation technique (A) and Kato-Katz method (B) (scale bar = 20 µm). They have thick and smooth shells and unconspicuous operculum. (C) An adult worm recovered from a case positive for larger heterophyid eggs (scale bar = 500 µm). It is somewhat small and slender in shape, and has round oral sucker (OS), muscular pharynx (P), ventrogenital sac (circle), elliptical ovary (O), and 2 testes (RT: right testis; LT: left testis). (D) Characteristic ventrogenital sac (magnified view of round circle in Fig. 1C) armed with about 16 gonotyl spines (scale bar = 40 µm). (E) Intrauterine eggs are oval in shape, dark brown color, with thick shell and unconspicuous operculum (scale bar = 20 µm).
Fig. 2 An adult of Acanthotrema felis recovered from a resident of Muan-gun, Jeollanam-do (scale bar = 200 µm). It is small and has a round oral sucker (OS), a muscular pharynx (P), and a ventrogenital sac (round circle). (B) Magnified view of the characteristic ventrogenital sac armed with 3 large sclerites (scale bar = 40 µm).

Fig. 1

Fig. 2

Epidemiological Survey on the Infection of Intestinal Flukes in Residents of Muan-gun, Jeollanam-do, the Republic of Korea
Items and helminth species No. of cases (%) No. examined 1,257 No. of helminth egg positive cases 95 (7.6) No. of cumulative egg positive cases 104 (8.3) Heterophyidsa) 62 (4.9) Clonorchis sinensis 40 (3.2) Echinostome 1 (0.08) Trichuris trichiura 1 (0.08) C. sinensis + heterophyids 7 (0.56) Echinostome + heterophyids 1 (0.08) T. trichiura + heterophyids 1 (0.08) Resident (Age/sex) No. of worms collected
H. nocens P. summa S. falcatus S. fuscata S. lari A. felis G. seoi 75/M 43 1 - 10 - - 3 73/M 93 - - 7 - - - 70/F 33 1 - 2 - - - 70/F 148 - 1 30 1 1 65 67/M 56 - - - - - 3 65/F 15 - - 3 - - 3 63/M 488 - 2 5 - - 1 60/F 101 138 - 23 - - - 57/F 4 - - - - - - Total 981 140 3 80 1 1 75 Authors Size of eggs (average) Present study (2010) Eggs in fecal specimens (n = 30) 33.8-42.5 (37.7) × 20.0-25.0 (21.5) μm Eggs in the uterus of worms (n = 20) 35.0-47.5 (39.1) × 20.0-26.3 (22.5) μm Onji and Nishio (1924) 35-37 × 22-24 μm Chai et al. (1988) 34-38 × 20-23 μm Sohn et al. (1994) 32-38 (35) × 19-23 (20) μm
Table 1. Helminth egg positive rates in the feces of residents in Muan-gun, Jeollanam-do, Korea

No. of larger heterophyid egg positive cases: 32 (2.6%).

Table 2. Results of worm collection from positive cases of larger heterophyid eggs after praziquantel treatment
Table 3. Comparison of Stictodora fuscata eggs with those of previous studies

Table 1.

Table 2.

Table 3.

PHD : Parasites, Hosts and Diseases

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