Lee, Song, Park, Kang, Lee, Han, Kim, Shin, and Chai: A case of Diphyllobothrium latum infection with a brief review of diphyllobothriasis in the Republic of Korea
Abstract
A case of Diphyllobothrium latum infection in a 49-year old man is described, and diphyllobothriasis latum in the Republic of Korea is briefly reviewed. An incomplete strobila of a tapeworm, 95 cm in length, without scolex and neck, was spontaneously discharged in the feces of a patient. On the basis of morphologic characteristics of the worm and eggs, the worm was identified as D. latum. The patient was successfully treated with a single dose (15 mg/kg) of praziquantel. The most probable source of infection was salmon flesh according to the past history of the patient. The first case of D. latum infection was documented in 1971, and this is the 43rd recorded case in the Republic of Korea. The 43 cases were briefly reviewed. The patients' main complaints were gastrointestinal troubles, such as mild abdominal pain, indigestion, and diarrhea, and discharge of tapeworm segments in the feces. The suspected infection sources included raw or improperly cooked flesh of fresh or brackish water fish, including the perch, mullet, salmon, and trout.
Key words: Diphyllobothrium latum, salmon, praziquantel, case report, review
INTRODUCTION
Diphyllobothrium latum is an intestinal tapeworm of mammals, such as humans, dogs, cats, foxes, and other wild canines ( Beaver et al., 1984). In the Republic of Korea, the first report of D. latum infection was documented based on recovery of eggs in the feces of 2 residents in Jinju, a southern area of Korea (Kojima and Ko, 1919). After then, 18 egg positive cases were reported by other workers (Hara and Himeno, 1923). An adult tapeworm was collected for the first time from a human in 1971 and morphologically identified as D. latum ( Cho et al., 1971). Until present, a total of 42 cases have been documented. The recent advancement of life quality with improvement of dietary conditions in the Republic of Korea, in particular, increased consumption of raw fish, is presumed to be a factor for an increase in D. latum infections. We report here a case of D. latum infection, and a total of 43 documented cases reported after 1971 were briefly reviewed.
CASE RECORD
A 49-year-old man visited our hospital with a segment of a tapeworm, naturally discharged in his feces. He was a resident of Seoul, without any recent history of travel abroad or to coastal areas. He reported an otherwise non-specific history except for consumption of raw salmon in autumn of 2005 at a restaurant in Seoul. He was a construction worker, with height of 157 cm and weight of 52 kg. He didn't have any special medical history.
He reported lower abdominal pain and diarrhea from February 2006, and from March of the same year, he experienced a total of 4 episodes of fecal discharge of several segments of a tapeworm, 1 to 5 m in length. CBC was in normal range without signs of anemia (WBC: 5,900/ µl, Hb: 15.8 g/dl, Hct: 45.9%, MCV: 87.9 fL, MCH: 29.6 pg, PLT: 327,000/ µl). Blood chemistry and serology were all within normal ranges.
The specimen was brought to the Department of Parasitology and Tropical Medicine, Seoul National University College of Medicine, Seoul, Korea, and was identified as D. latum according to the characteristic morphology of the worm and the eggs. The worm was creamy-white and 95 cm long without scolex and neck. Some proglottids were fixed with 10% formalin under a pressure of a glass slide. The size of a proglottid was 8.2 x 2.7 mm, and the number of proglottids was 330. Gravid proglottids stained with acetocarmine revealed a rosette-shape uterus with 4-5 times piled-up uterine loops ( Fig. 1). The eggs collected from the proglottids were oval with an operculum at the anterior end and an abopercular protuberance at the posterior end, grayish brown, and 63.5 µm in average length and 42.5 µm in average width. The patient was treated with a single dose (15 mg/kg) of praziquantel, and there was no evidence of relapse during the next 9 mo.
DISCUSSION
Since 1971 when the first worm-proven D. latum case was reported in the Republic of Korea ( Cho et al., 1971), the total number of cases documented so far is 43, including the present case ( Table 1). All cases of D. latum and D. latum parvum type infections ( Lee et al., 1994) were included, but a case of D. yonagoense infection has been excluded from this study ( Lee et al., 1988). The adult worm of D. latum was not collected in the case numbers 36, 38, and 42 ( Table 1); therefore, the number of worm-proven D. latum cases in the Republic of Korea becomes 40. We briefly reviewed the 43 cases in terms of epidemiological, clinical, and parasitological aspects.
The age and sex distribution of D. latum infection revealed a predominance of infection among middle-aged men, i.e., 30-49 years ( Table 2), which agrees to Sohn et al. ( 1996). The number of males was 31 and that of females 12 ( Table 2). In general, Korean men tend to eat raw fish more frequently than women, and this tendency seems to be responsible for the higher number of D. latum cases in men. With regard to the residence of the cases, the majority of the 43 patients were citizens of Seoul or metropolitan Seoul (Bucheon), and the others were citizens of or visitors to coastal or lakeside cities like Chuncheon, Ullungdo (Island), Sokcho, and Busan ( Table 3).
The major symptoms complained by D. latum cases were gastrointestinal troubles, such as abdominal pain, vomiting, diarrhea, and dyspepsia in 20 cases ( Table 1). Other symptoms included anemia, fatigue, anorexia, fever, and myalgia in a few cases. In a total of 17 cases, there were natural discharge of proglottids in the feces, and in 4 cases no symptoms were complained ( Table 1). Except a child reported by Joo et al. ( 1983), there were no other cases that showed significant signs and symptoms of anemia.
Adult worms were identified in 40 of the 43 cases, and from the 40 cases a total of 46 worms were collected; 2 cases were infected with 3 worms each, 2 cases were with 2 worms, and 36 cases were with a single worm ( Table 1). Among the 46 worms recovered, 21 were with scolices. The longest worm was 1,250 cm, and 13 worms were longer than 500 cm ( Table 1). For D. latum, the largest size of the eggs was 72.4 x 47.2 µm, and the smallest size 59.0 x 41.0 µm. The eggs of the 30th and 31st cases, identified as D. latum parvum type infections, were 57.5 x 37.4 µm.
The medication was atabrine in 1971, and since then until 1986, either niclosamide, bithionol, or praziquantel was used. From 1987 up to present, praziquantel has been used as the drug of choice. There was no treatment failure among the 43 cases. In our case, the treatment with praziquantel in a single dose (15 mg/kg) was successful as revealed by the disappearance of eggs in the feces at 9 mo after the treatment.
As to the second intermediate hosts for D. latum, freshwater fishes, such as pikes, burbots, trouts, salmons, and perches were listed ( Beaver et al., 1984). In Japan, Eguchi ( 1973) listed 4 salmon species as the major second intermediate hosts for D. latum, i.e., Onchorhychus masou (masu salmon), O. gorbusha (pink salmon), O. keta, and O. nerka. However, the species of the broad fish tapeworm, i.e., D. latum, transmitted by salmonid fish was put to question, and the one in Japan by O. masou and O. gorbusha was assigned as a new species D. nihonkaiense ( Yamane et al., 1986), and another in Siberia transmitted by 2 salmonid fish species, O. gorbuscha and O. keta, was assigned as D. klebanovskii ( Muratov and Posokhov, 1988). The Republic of Korea and Japan share the sea and fish. Therefore, human-infecting Diphyllobothrium spp. may be taxonomically similar. In particular, the worms from cases who consumed salmonid fish among the Korean patients may have been D. nihonkaiense. However, the validity of D. nihonkaiense and D. klebanovskii remains to be further clarified, and we regarded all worms as D. latum in order to avoid taxonomic confusion.
With the exception of 2 cases in which the suspected source of infection is uncertain, all cases had the history of eating raw freshwater or brackish water fish ( Table 4). The number of cases that ate salmon and mullet was equally 8 (16.6%), and those that consumed perch and trout were 7 (14.6%) and 5 (10.4%), respectively ( Table 4). Most of the remaining cases recalled that they had eaten any type of raw fish. Before the 1990s, perch was most frequently reported as the suspected second intermediate host in the Republic of Korea ( Lee et al., 1983, 1989), but nowadays, salmon, trout, and mullet are mainly concerned ( Table 1). It is regretted that there have been no reports on D. latum plerocercoid infections in fishes; studies on the life cycle of D. latum are required in the Republic of Korea.
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Fig. 1
Gravid proglottids of D. latum discharged from the present patient, acetocarmine-stained. Note 4-5 uterine loops in rosette form. × 40.
Table 1.
Summary of 43 D. latum cases reported in the Republic of Korea (1971-2007)
Case No |
Author (year) |
Age (Sex) |
Residence/ visit |
Complaints |
Suspected source of infection |
Size of eggs (μm) |
Lengh of strobila (cm) |
Collection ofscolex |
Drug (dosage) |
1 |
Cho et al. (1971) |
50(M) |
Seoul |
Passage of proglottids |
Raw fishes |
66.5 × 41.2 |
198 |
No |
Atabrine (0.9 g) |
2 |
Min et al. (1975) |
37(M) |
Seoul |
Passage of proglottids |
Unknown |
N.m.a)
|
N.m. |
No |
Niclosamide (2.0 g) |
3 |
Jeonget al. (1980) |
14(M) |
Seoul |
Fatigue, anorexia |
Perch |
64.3 × 41.4 |
685 |
No |
Bithionol (40 mg/kg) |
4 |
Kim and Lee (1981) |
26(F) |
Seoul |
Dizziness, dyspnea |
Sea fish |
63.8 × 43.6 |
40 |
No |
Niclosamide (2.0 g) |
5 |
Kim and Lee (1982) |
42(M) |
Seoul |
Abd. pain |
Sea fishes |
N.m. |
635 |
Yes |
Bithionol (3.0 g) |
6 |
Song and Jung (1983) |
48(M) |
Busan |
Abd. pain |
Perch |
N.m. |
N.m. |
- |
Niclosamide (3.0 g) |
7 |
Lee et al. (1983) |
10(M) |
Seoul |
Abd. pain |
Perch |
64 × 45 |
454 |
Yes |
Bithionol (40 mg/kg) |
8 |
|
48(M) |
Seoul |
Passage of proglottids |
Sea fish |
62 × 42 |
30 |
No |
Niclosamide (2.0 g) |
9 |
|
64(M) |
Seoul |
No symptoms |
Sea fish |
67 × 48 |
320 |
Yes |
Bithionol (40 mg/kg) |
10 |
|
53(F) |
Seoul |
Abd. pain, vomiting |
Sea fish |
59 × 41 |
680 |
Yes |
Praziquantel (20 mg/kg) |
11 |
|
23(M) |
Seoul |
Abd. pain, indigestion |
Perch, mullet |
67 × 45 |
565 |
Yes |
Praziquantel (15 mg/kg) |
12 |
Joo et al. (1983) |
17(M) |
Seoul |
Passage of proglottids |
Salmon |
N.m. |
1250 |
No |
Bithionol (40 mg/kg) |
13 |
|
17(M) |
Seoul |
Passage of proglottids |
Sea fishes |
N.m. |
854 |
No |
Bithionol (40 mg/kg) |
14 |
|
6(F) |
Seoul |
Anemia |
Sea fishes |
N.m. |
45-50 |
Yes |
Bithionol (40 mg/kg) |
15 |
|
35(M) |
Seoul |
Diarrhea |
Perch, salmon |
N.m. |
830, 850 |
Yes |
Bithionol (40 mg/kg) |
16 |
|
14(M) |
Seoul |
Passage of proglottids |
Sea fishes |
N.m. |
620 |
No |
Bithionol (40 mg/kg) |
17 |
|
17(F) |
Seoul |
Passage of proglottids |
Salmon |
N.m. |
1050 |
Yes |
Bithionol (40 mg/kg) |
18 |
|
10(M) |
Seoul |
Passage of proglottids |
Unknown |
N.m. |
460 |
No |
Bithionol (40 mg/kg) |
19 |
Cho et al. (1986) |
29(M) |
Seoul |
Abd. pain |
Sea fish |
64 × 44 |
92 |
No |
Unknown |
20 |
|
41(M) |
Seoul |
Diarrhea, constipation |
Salmon |
62 × 43 |
>20 |
No |
Unknown |
21 |
Lee et al. (1987) |
14(M) |
Seoul |
No symptoms |
Mullet, salmon, perch |
62 × 46 |
650 |
Yes |
Praziquantel (13 mg/kg) |
22 |
|
31(M) |
Seoul |
Abd. pain, diarrhea |
Perch, mllet |
61 × 42 |
300 |
Yes |
Praziquantel (13.6 mg/kg) |
23 |
Lee et al. (1989) |
20(M) |
Ullungdo |
Fever, passage of proglottids |
Sea fish |
63.0 × 44.0 |
152, 123, 100 |
Yes (n=2) |
Praziquantel (10 mg/kg) |
24 |
|
30(M) |
Ullungdo |
Passage of proglottids |
Sea fish |
63.0 × 44.0 |
240 |
No |
Praziquantel (10 mg/kg) |
25 |
|
36(M) |
Seoul |
No symptoms |
Fishes |
63.0 × 44.0 |
265, 423 |
No |
Praziquantel (10 mg/kg) |
26 |
|
44(M) |
Seoul |
Passage of proglottids |
Sea foods |
63.0 × 44.0 |
119, 114, 85 |
Yes (n=3) |
Praziquantel (10 mg/kg) |
27 |
|
41(M) |
Seoul |
Passage of proglottids |
Sea fish |
63.0 × 44.0 |
N.m. |
Yes |
Praziquantel (10 mg/kg) |
28 |
|
25(M) |
Seoul |
Passage of proglottids |
Sea fish |
63.0 × 44.0 |
100 |
Yes |
Praziquantel (600 mg) |
29 |
|
31(M) |
Seoul |
Abd. pain, dyspepsia |
Sea fish |
63.0 × 44.0 |
N.m. |
No |
Praziquantel (10 mg/kg) |
30 |
Lee et al. (1994)b)
|
46(F) |
Seoul |
No symptoms |
Trout |
57.5 × 37.4 |
120 |
Yes |
Praziquantel (13 mg/kg) |
31 |
|
22(M) |
Seoul |
Passage of proglottids |
Sea fish |
N.m. |
15 |
No |
Praziquantel (10 mg/kg) |
32 |
Ahn et al. (1996) |
43(M) |
Chuncheon |
Passage of proglottids |
Trout |
62.4 × 41.5 |
665 |
No |
Praziquantel (15 mg/kg) |
33 |
|
39(F) |
Chuncheon |
Dyspepsia, abd. pain |
Trout |
N.m. |
550 |
No |
Praziquantel (15 mg/kg) |
34 |
Ha et al. (1997) |
60(F) |
Unknown |
Abd. pain |
Trout (cultured) |
55-70 × 45-60 |
50 |
No |
Praziquantel (10 mg/kg) |
35 |
Chung et al. (1997) |
35(F) |
Bucheon |
Abd. pain |
Mullet |
72.4 × 47.2 |
310 |
Yes |
Praziquantel (15 mg/kg) |
36 |
|
39(M) |
Bucheon |
Abd. pain, dyspepsia |
Mullet |
67 × 45 |
- |
No |
Praziquantel (15 mg/kg) |
37 |
|
43(F) |
Bucheon |
Dizziness, abd. pain |
Mullet |
70.4 × 46.4 |
340 |
Yes |
Praziquantel (15 mg/kg) |
38 |
|
43(F) |
Bucheon |
Headache, abd. pain |
Mullet |
N.m. |
- |
No |
Praziquantel (15 mg/kg) |
39 |
|
42(M) |
Bucheon |
Abd. pain |
Mullet |
N.m. |
100 |
No |
Praziquantel (15 mg/kg) |
40 |
Jang and Cho (2000) |
42(M) |
Chuncheon |
Abd. pain |
Trout |
N.m. |
300 |
Yes |
Praziquantel (10 mg/kg) |
41 |
Lee et al. (2001) |
7(F) |
Sokcho |
Passage of proglottids |
Salmon |
N.m. |
42 |
- |
Praziquantel (15 mg/kg) |
42 |
|
35(F) |
Sokcho |
Passage of proglottids |
Salmon |
N.m. |
- |
No |
Praziquantel (600 mg) |
43 |
The present study (2007) |
49(M) |
Seoul |
Abd. pain, diarrhea |
Salmon |
63.5 × 42.5 |
95 |
No |
Praziquantel (15 mg/kg) |
Table 2.
Age and sex distribution of D. latum cases reported in the Republic of Korea (1971-2007)
Age |
No. of cases
|
Male |
Female |
Total (%) |
< 9 |
0 |
2 |
2 (4.7) |
10 ~ 19 |
7 |
1 |
8 (18.6) |
20 ~ 29 |
5 |
1 |
6 (13.9) |
30 ~ 39 |
7 |
3 |
10 (23.2) |
40 ~ 49 |
10 |
3 |
13 (30.2) |
50 ~ 59 |
1 |
1 |
2 (4.7) |
60 ~ 69 |
1 |
1 |
2 (4.7) |
Total |
31 (72.1) |
12 (27.9) |
43 (100.0) |
Table 3.
Residence distribution of D. latum cases (1971-2007)
Residence/place of visit |
No. of cases (%) |
Seoul |
29 (67.4) |
Bucheon |
5 (11.6) |
Chuncheon |
3 (7.0) |
Ullungdo |
2 (4.7) |
Sokcho |
2 (4.7) |
Busan |
1 (2.3) |
Unknown |
1 (2.3) |
Total |
43 (100.0) |
Table 4.
Suspected sources of infection in D. latum infection cases (1971-2007)
Source of infection |
No. (%) of cases |
Fish (undefined) |
18 (37.5) |
Salmon |
8 (16.6) |
Mullet |
8 (16.6) |
Perch |
7 (14.6) |
Trout |
5 (10.4) |
Unknown |
2 (4.2) |
Total |
48 (100.0)a)
|
|
|