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Korean J Parasitol > Volume 45(1):2007 > Article
Park, Guk, Shin, Kim, Kim, Seo, Park, and Chai: A new endemic focus of Gymnophalloides seoi infection on Aphae Island, Shinan-gun, Jeollanam-do


A new endemic focus of Gymnophalloides seoi infection has been discovered on Aphae Island (Shinan-gun, Jeollanam-do), Republic of Korea. This area, which is referred to as Bokyong-ri, is a small seashore village located in the northern portion of the island. Fecal samples were collected from a total of 57 residents and examined by the Kato-Katz and formalin-ether sedimentation techniques. Helminth eggs were detected in 37 samples (64.9%); 33 samples were positive for G. seoi eggs (57.9%), 4 for Pygidiopsis summa (7.0%), 13 for other heterophyids (22.8%), 1 for Clonorchis sinensis (1.7%), and 1 for Trichuris trichiura (1.7%). Women (70.4%) revealed higher rates of G. seoi infection than did men (46.7%), and individuals older than 50 years of age also evidenced higher rates of G. seoi infection than in other age groups (P< 0.05). In worm collection from 13 G. seoi egg positive cases, G. seoi (total 86,558 specimens), Heterophyes nocens (278), Stictodora sp. (10), Heterophyopsis continua (3), P. summa (3), and unidentified flukes (42) were collected. Oysters, the source of G. seoi infection, were collected from an area proximal to the village and 50 were examined for metacercariae; 47 (94%) were found infected and the observed metacercarial density was 9.5 ± 8.9 per oyster. The results of this study indicate that Bokyong-ri is a new endemic area of G. seoi infection, with high rates of infection in humans and oysters.


Gymnophalloides seoi Lee, Chai and Hong, 1993 (Trematoda; Gymnophallidae) is a minute intestinal fluke that infects humans and migratory birds, including the Palearctic oystercatcher Haematopus ostralegus (Lee et al., 1993; Lee and Chai, 2001; Ryang et al., 2000; Chai et al., 2003). The oyster, Crassostrea gigas, has been identified as the source of human infections (Lee et al., 1995a). Until the present, G. seoi has been detected only in the Republic of Korea (Lee et al., 1993, 1995, 1996; Sohn et al., 1998; Lee et al., 1999; Chai and Lee, 2002).
The first human G. seoi infection was detected in 1988 from a 66-year-old woman suffering from acute pancreatitis (Lee et al., 1993). A small village on Aphae Island, Sinjang-3-ri, the residence of the first patient, was determined to be highly endemic for G. seoi infection. Half of the villagers residing in this area were found to be infected (Lee et al., 1994). Thereafter, oysters infected with G. seoi metacercariae were detected in 14 western coastal areas and more human infections were discovered in 24 southeastern coastal areas (Lee and Chai, 2001). It is now generally thought that human G. seoi infections may be present in a broader distribution than previously expected, as natural oysters are available all along the southwestern coast, and people can readily procure and consume raw oysters in these regions.
The prevalence and intensity of G. seoi metacercarial infection in oysters appears to vary substantially according to geographical area (Lee et al., 1996; Chai et al., 2001b). Therefore, even on Aphae Island, in which the endemic focus of G. seoi was initially discovered, the status of metacercarial infection in oysters might differ according to locality on the island. In addition, the status of human G. seoi infection may also differ in accordance with locality on the island. Up to the present, on Aphae Island, epidemiological studies have concentrated on Sinjang 3-ri, and no other information has been available regarding human G. seoi infections on different regions of Aphae Island. The objective of this study was, then, to determine the infection status of G. seoi among residents of a small coastal village on Aphae Island, and among oysters caught in a region near this village.


Fecal examination and worm collection

A total of 57 residents in Bokyong-ri, Aphae Island, were subjected to fecal examinations. Bokyong-ri is located in the northern portion of Aphae Island and is quite far (approximately 10 km) from Sinjang 3-ri, in which G. seoi infection is endemic (Fig. 1). The fecal samples were collected and examined for helminth eggs using formalin-ether sedimentation and the Kato-Katz thick smear techniques in June, 2004. Adult flukes were collected from 13 persons, all of whom evidenced relatively high numbers of eggs per gram of feces. They were treated with 10 mg/kg of praziquantel and purged with magnesium sulfate (Sigma, St. Louis, Missouri, USA). The whole diarrheic stools were collected, washed 2 times after filteration, and fixed in 2% formalin solution. Worms were collected and morphologically identified with a stereomicroscope.

Questionnaire regarding the eating habits of residents and clinical complaints

In order to characterize the relationships between parasite infections, eating habits, and clinical complaints, a paper questionnaire was distributed to inhabitants who had submitted stool samples. The contents of the questionnaires included questions concerning; 1) consumption of raw oysters, mullets, and gobies, 2) clinical complaints, including anorexia, abdominal pain, constipation, diarrhea, fatigue, indigestion, polyuria, or thirst, 3) suffering (or not) from diabetes mellitus, as adjudged via blood glucose examinations and history taking. In blood examinations, a glucose level in excess of 126 mg/dl on an empty stomach was regarded as a positive result, a level of 110 to 125 mg/dl was considered 'suspected', and a level of less than 110 was regarded as a negative result.

Oyster examination

Oysters were harvested from a tidal flat near Bokyong-ri in July 2004, and 50 oysters were selected for further evaluation, all of which were within a range of 4-6 cm in length and 20-40 g in weight. The animal part of oysters was digested for 30 min in 0.6% pepsin-HCl solution. After filtration through 1 mm diameter mesh, G. seoi metacercariae were collected and counted with a stereomicroscope.

Statistical analysis

The relationships between trematode infections, eating habits, physical complaints, and diabetes mellitus were analyzed using Spearman's correlation coefficient test. Sex-dependent prevalence was analyzed using the chi-square test. A value of P < 0.05 was considered to be significant.


Helminth infection status in residents

Out of 57 fecal samples, 37 (64.9%) revealed helminth eggs and the majority of them (33 samples, 57.9%) were positive for G. seoi eggs (Table 1). A total of 86,558 G. seoi adults were collected from 13 individuals who showed high EPGs in the stool examination (Table 2). Three residents were infected with more than 15,000 worms, i.e., 25,015, 20,155, and 15,023, respectively. Other parasites were also recovered, i.e., Heterophyes nocens, Heterophyopsis continua, Pygidiopsis summa, and Stictodora sp. The rate of G. seoi infection in women (70.4%) was higher than that in men (46.7%). However, these sex-dependent differences were statistically not significant (P > 0.05). All of the helminth positive cases were more than 30 years old and the infection rate in the 50-69 year age group (overall helminth: 95.8%; G. seoi: 83.3%) was significantly higher than those in the other age groups (P < 0.05).

Results of questionnaire

Of the 20 inhabitants that completed the questionnaire, only one was not infected with any intestinal trematode. The others (19) were infected with either G. seoi (19), P. summa (1), other heterphyids (7), or Clonorchis sinensis (1). The number of persons who reported consuming raw oysters, mullets, and gobies were 17, 10, and 10, respectively (Table 3). The inhabitants complained of several symptoms on the questionnaire, including anorexia (6), abdominal pain (8), constipation (6), diarrhea (7), fatigue (2), indigestion (7), polyuria (5), and thirst (9). Out of 20 subjects examined, 4 suffered from diabetes mellitus, and 2 were assigened to the 'suspected' category. Via statistical analysis, G. seoi infection was closely associated with the consumption of raw oysters (P = 0.017). However, heterophyid infections and consumption habits, physical complaints, and diabetes mellitus were not found to be significantly related.

Metacercarial infection in oysters

Among the 50 oysters collected from a nearby estuary in Bokyong-ri, 47 (94%) were determined to be infected with G. seoi metacercariae. However, the metacercarial density per oyster was not so high (9.5 ± 8.9).


In the present study, Bokyong-ri was identified as a new endemic focus of G. seoi infection. Among 57 residents examined, 33 (57.9%) appeared to be positive for G. seoi eggs. This rate is higher than that reported in Sinjang 3-ri, in which the G. seoi egg positive rate was 49% (Lee et al., 1994). The mean number of worms per infected individual was also higher than that recorded for Sinjang 3-ri (Lee et al., 1994).
The infection rate and intensity of G. seoi metacercariae in oysters differed significantly between the oysters collected in Bokyong-ri (present study) and previously in Sinjang 3-ri (Sohn et al., 1998). However, the mean number of metacercariae detected in the oysters from Bokyong-ri (9.5) was much lower than that observed in the oysters from Sinjang 3-ri (1,339) (Sohn et al., 1998). The number of metacercariae infected in oysters was small but residents were heavily infected. This result may be attributed to the repeated and frequent consumption of raw oysters infected with the metacercariae (Chai et al., 2000).
Among 13 areas, in which metacercarial infections were detected in oysters, the highest metacercarial density was discovered in Chungdo (203.0). In other areas, metacercarial densities tended to be lower than 67.6 (Lee et al., 1996). In the present study, the metacercarial density in the oysters was lower than that observed in the oysters from Chungdo, but the infection rate and the number of worms recovered (or EPG) was far higher than was seen in Chungdo (Chai et al., 2001b). Therefore, metacercarial infections in oysters and human infections do not appear to evidence a consistent positive relationship. More detailed studies regarding the life span of G. seoi in humans might provide more detailed information regarding the negative relationships between human infection rates and metacercarial infection in oysters.
The small intestine of G. seoi-infected mice showed villous atrophy and crypt hyperplasia in the duodenum and jejunum, with inflammatory reactions in the villous stroma and crypt, probably due to mechanical and chemical irritations by the worms (Chai et al., 2001a). Therefore, this fluke is considered to be enteropathogenic to its definitive hosts, most notably humans. From the questionnaire study, the major complaints of the individuals infected with G. seoi included thirst and abdominal pain (42.1%), followed by diarrhea (36.8%), anorexia (31.6%), indigestion (31.6%), constipation (26.3%), polyuria (26.3%), and fatigue (10.5%). G. seoi infections were significantly associated with the consumption of raw oysters, as the oyster is the only known source of human G. seoi infection.
One of the interesting things determined in this study was is that 6 (21.1%) out of 19 individuals infected with G. seoi were suffering from or suspected of diabetes mellitus. The majority of them complained of thirst (5) or polyuria (4), both of which have been implicated as clinical signs of diabetes mellitus. Diabetes mellitus and G. seoi infection are suspected to be related in some way, as 2 cases of diabetes mellitus were accompanied by G. seoi infection (Lee et al., 1995b; Chai and Lee, 2002). The first such case in a human subject was diagnosed as acute pancreatitis (Lee et al., 1993). Therefore, caution should be excercised in such cases, as G. seoi infection might eventually damage the pancreatic duct and nearby tissues. Further studies are required in order to elucidate this issue.


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Fig. 1
The area surveyed in this study (Bokyong-ri, astrix) in comparison with Sinjang 3-ri, a known endemic area of Gymnophalloides seoi infection.
Table 1.
Results of fecal examination of residents in Bokyong-ri, Aphae Island (Shinan-gun)
Items/Parasite species No. of residents (%)
No. of residents examined 57
No. of helminth egg positivea) 37 (64.9)
 Gymnophalloides seoi 33 (57.9)
 Pygidiopsis summa 4 (7.0)
 Other heterophyid flukes 13 (22.8)
 Clonorchis sinensis 1 (1.7)
 Trichuris trichiura 1 (1.7)

a) A total of 11 persons had 2-3 different parasite eggs.

Table 2.
Results of fecal examination and worm collection in 13 residents of Bokyong-ri, Aphae Island (Shinan-gun)
Resident code Age/Sex Fecal examination
No. of worms collected
Kato-Katza) F-Eb) Gsc) Hnc) Hcc) Psc) Sspc)
1 48/F Gs123 Gs 25,015 39 0 0 0
2 69/M Gs43 Gs 20,155 24 0 3 0
3 68/M Gs29 Gs 15,023 1 0 0 0
4 66/M Gs39 Gs 6,524 0 0 0 0
5 65/F Gs12 Gs 6,386 0 0 0 0
6 57/M Gs2 Hd) 3,772 0 0 0 0
7 44/M Gs10 Gs, H 3,036 160 3 0 10
8 61/F Gs14 Gs 2,313 8 0 0 0
9 50/F Gs32, H2 Gs, H 1,706 0 0 0 0
10 64/M Gs29 Gs, H 1,309 43 0 0 0
11 62/F Gs21 Gs 921 3 0 0 0
12 56/M Gs16, H2, Ps2 Gs, H 377 0 0 0 0
13 51/F Gs2, H2, Csd)1 Gs, Cs 21 0 0 0 0
Total 86,558 278 3 3 10

a) Number represents the number of eggs detected on one Kato-Katz smear.

b) F-E: formalin-ether sedimentation

c) Gs: Gymnophalloides seoi, Hn: Heterophyes nocens, Hc: Heterophyopsis continua, Ps: Pygidiopsis summa, Ssp: Stictodora sp.

d) H: eggs of heterophyids, Cs: eggs of Clonorchis sinensis

Table 3.
Summary of questionnaire from residents of Bokyong-ri, Aphae Island (Shinan-gun)
Resident code Age/sex Results of stool exam.a) Consuming raw
Complaintsb) Hx of diabetes mellitusc)
Oysters Mullets Gobies
A 43/M Gs, H + + + AP, D, F, P, T +
B 65/M Gs + - - AP, P, T +
C 61/F Gs - - - AP +
D 64/M Gs, H + + + D, T +
E 68/M Gs + + + A, P, T ±
F 70/M Gs + - - A, C, I, P, T ±
G 56/M Gs, H, Ps + + + - -
H 51/F Gs, H, Cs + + + D, I -
I 68/M Gs + + + T -
J 66/F Gs + + - A, I -
K 58/M Gs, H + + + AP, D, I -
L 49/F Gs, H + + + AP, C, F, P -
M 47/F Gs + + + A, AP, C, D, T -
N 62/F Gs + - + AP, C -
O 65/F Gs + - - A, AP, I -
P 63/F Gs, H + - - C, D -
Q 75/M Gs + - - D, I, T -
R 85/F Gs + - - - -
S 72/F Gs - - - A -
T 76/M Gs - - - C, I, T -

a) Gs: G. seoi, H: heterophyids, Ps: P. summa, Cs: C. sinensis

b) A: anorexia, AP: abdominal pain, C: constipation, D: diarrhea, F: fatigue, I: indigestion, P: polyuria, T: thirst

c) History of diabetes mellitus (+: positive, ±: suspected, -: negative)

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