Abstract
Trichinosis is a food-borne zoonotic disease caused by the nematode, Trichinella spp., and had been reported several times in Korea. Recently, there was an additional outbreak, involving 5 patients, the findings from which are reported herein. On 30 November 2010, 8 persons ate sashimi of the meat of a wild boar. Then, 2-3 weeks later, they complained of myalgia and fever. Unfortunately, muscle biopsy was not performed, but ELISA was performed using their sera. Two people among 8 were positive for Trichinella on the 34th day post-infection (PI), and 3 patients who initially revealed negative ELISA were additionally proved to be positive for trichinosis on the 42nd day PI. Hence, the confirmed patients of trichinosis were 5 in total in the present outbreak. They were treated with albendazole and discharged uneventfully. This was the fifth outbreak of trichinosis in Korea.
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Key words: Trichinella, trichinosis, wild boar, ELISA, outbreak
INTRODUCTION
Trichinosis is a food-borne zoonotic disease caused by
Trichinella spp. [
1]. The source of infection is mostly uncooked or poorly processed meat, whether pork or wild animal meat [
2]. It has been a major public health problem worldwide, and human trichinosis has been reported in 55 (27.8%) of the world's 198 countries [
3]. Among the 7 species of
Trichinella,
T. spiralis is the most prevalent etiologic agent of human trichinosis, and the isolate in the Korean case was proven to be
T. spiralis [
2,
4]. It has been suggested that
T. spiralis originated from Europe and subsequently spread anthropogenically to other continents, such as Africa and America [
5].
There have been numerous outbreaks of trichinosis in Asia, particularly in China and Thailand [
6]. From 1964 to 2003, in China, 247 people died from trichinosis, and in Thailand 97 died from 1962 to 2005 [
7,
8]. Recently, an outbreak from eating raw soft-shelled turtles (
Pelodiscus sinensis) was also reported in Taiwan [
9]. The first occurrence of trichinosis among humans in Korea was related to consumption of the meat of badgers,
Meles meles melanogenys [
10], and several outbreaks followed after then. This paper reports the fifth outbreak of human trichinosis from consumption of a wild boar (
Sus scrofa).
CASES RECORD
In December 2010, 2 patients were admitted to the Department of Internal Medicine, Dankook University Hospital, due to complaints of generalized myalgia, headache, and facial edema. They were living in Cheonan-si, Chungcheongnam-do, and had dinner with their colleagues on 30 November, 2010. The main dishes were barbecue and sashimi, both from the meat of a wild boar. Among the participants of the dinner, 2 patients and 6 other people ate the sashimi. Two weeks after the dinner, the aforementioned symptoms developed in the former, and they visited Dankook University Hospital. After then, the rest of the people also complained of similar symptoms, such as myalgia, fever, and headache in 10 days, and were admitted to Dankook University Hospital. The incubation period of 8 patients was 16.3 days on average (
Table 1).
The laboratory findings revealed elevation of the eosinophil count in all patients (14.2-41.2%), and elevation of C-reactive protein (CRP) in 6 patients. Leukocytosis was observed in only 2 patients, and muscle enzymes, creatine kinase (CK) and lactate dehydrogenase (LDH), increased in 2 patients. ELISA using the sera of the patients was performed in the Department of Parasitology, Seoul National University College of Medicine on the 34th day post-infection (PI). The positive criterion of ELISA absorbance was 0.25, but only 2 serum samples were positive for
T. spiralis antigen in the first ELISA. Sera collection was performed from 4 ELISA-negative patients 8 days later, and they were re-examined by ELISA for
Trichinella. Among them, 3 samples were additionally proved to be positive (
Table 2). Since the 2 ELISA-negative patients could not be followed-up, the confirmed cases of trichinosis were 5 in number. They were treated with albendazole for 2 weeks, and all the patients were discharged without any remaining clinical signs of trichinosis.
DISCUSSION
Including the first outbreak in 1997, there had been 4 reports of trichinosis outbreaks in Korea [
10-
13]. Since the first outbreak was separated into 2 reports, and the report on the outbreak in Inje-gun, Gangwon-do in 2001 has not yet been published, the present case is regarded the fifth outbreak in Korea (
Table 3). Among the 34 Koreans diagnosed with trichinosis, only 27 could be located. Nineteen of them were males and 8 were females, with a mean age of 45.6 years. Their most common symptom was fever (27/27), followed by myalgia (25/27) and facial edema (18/27). Eosinophilia (>5%) was observed in all of them. The record of trichinosis mainly depends on consumption of the meat of domestic or wild animals, but the recognition of trichinosis by a clinician is important for detection of the outbreak. Thus, if a patient complains of myalgia and fever with eosinophilia, the doctor should consider the possibility of trichinosis. In our cases, muscle enzymes, such as CK and LDH were not always elevated, and leukocytosis was not an essential criterion of
Trichinella infection (
Table 1).
Trichinosis is definitively diagnosed by revealing the encysted larva through a muscle biopsy [
1], but such method could not be applied to each patient. Serologic tests may be helpful for the diagnosis, and ELISA using an excretory-secretory (ES) antigen is the most commonly used assay, with 99% sensitivity and 91-96% specificity [
14]. In particular, ELISA has an advantage over digestion method in lightly infected animals [
14], and it could be the useful diagnostic method in Korea, where trichinosis has not been rampant. A disadvantage of ELISA is occurrence of false-negative results during the early stages of infection [
14]. In the first outbreak in Korea, the result of the antibody test was positive on the 34th day PI [
10]. In our cases, the results of ELISA for the
Trichinella antigen were positive only in 2 sera among 8 collected on the 34th day PI, and positivity was additionally recorded in 3 more sera out of 4 examined on the 42nd day. In the fifth patient, ELISA negative conversion was reported on the 42nd day PI (
Table 1), whose complaint was only a febrile sensation without myalgia. It was suggested that the infection density of
Trichinella larvae might have been low in that patient. Since the 2 negatives on the 32nd day PI could not be followed-up by ELISA, the confirmed patients of trichinosis were only 5 in the present outbreak.
Although the first outbreak was caused by eating of the raw badger meat,
M. meles melanogenys, the rest was due to eating the wild boar meat,
S. scrofa [
10-
13]. Because 4 of the outbreaks were concentrated in Gangwon-do, it is supposed that the life cycle of
T. spiralis is maintained in Gangwon-do. Examinations of wild animals to determine the prevalence of
Trichinella have been frequently performed in other countries. A national survey on 4,517 wild boars revealed 4% seropositive animals in Corsica, France, and 1.4% ELISA-positive wild boars in Germany and 8.7% in Switzerland [
15,
16]. A survey to estimate the prevalence of trichinosis in wild boars in Korea is thus urgently needed.
Domesticated animals could also be the source of human trichinosis. The outbreaks were caused by eating raw or undercooked pork in China, and the main sources of infection in Thailand have been pigs [
7,
8]. In China, the seroprevalence of swine trichinosis ranged from 0.01% to 30.0%, and the prevalence of
Trichinella was from 0.06% to 5.6% in the pork sold in markets [
7]. The prevalence of native
Trichinella is 11.4% in red foxes in Otaru, Japan [
17]. The surveillance of
Trichinella infection in pig-breeding farms, however, revealed no positivity for infection in Korea [
12]. Although their study [
12] is the only one on domesticated animals in Korea, the infection rate of the pork with
Trichinella is expected to be low, considering the small number of outbreaks. The risk of
Trichinella infection should be publicized, however, since some Koreans enjoy eating raw wild animal meat.
In this report, the species of
Trichinella could not be identified due to the unavailability of larvae. The
Trichinella found in Asia and the Pacific Rim include both encapsulated (
T. spiralis,
T. britovi, and
T. native) and non-capsulated species (
T. pseudospiralis,
T. papuae) [
6]. In Japan,
T. britovi was reported [
6]. In Korea, only 1 species,
T. spiralis, was identified [
4,
18]. Possible presence of other species in Korea should be determined in the near future.
ACKNOWLEDGMENT
This work was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education, Science and Technology (2011-0009312). We are grateful to Hye-Sung Kim, Department of Parasitology and Tropical Medicine, Seoul National University College of Medicine, for performing ELISA.
References
- 1. John DT, Petri WA. Markell and Voge's Medical Parasitology. 2006, 9th ed. St. Louis, Missouri, USA. Elsevier Inc. pp 305-310.
- 2. Murrell KD, Pozio E. Trichinellosis: The zoonosis that won't go quietly. Int J Parasitol 2000;30:1339-1349.
- 3. Pozio E. World distribution of Trichinella spp. infections in animals and humans. Vet Parasitol 2007;149:3-21.
- 4. Sohn WM, Huh S, Chung DI, Pozio E. Molecular identification of Korean Trichinella isolates. Korean J Parasitol 2003;41:125-127.
- 5. Rosenthal BM, LaRosa G, Zarlenga D, Dunams D, Chunyu Y, Mingyuan L, Pozio E. Human dispersal of Trichinella spiralis in domesticated pigs. Infect Genet Evol 2008;8:799-805.
- 6. Takahashi Y, Mingyuan L, Waikagul J. Epidemiology of trichinellosis in Asia and the Pacific Rim. Vet Parasitol 2000;93:227-239.
- 7. Cui J, Wang ZQ. An epidemiological overview of swine trichinellosis in China. Vet J 2011;Epub ahead of print.
- 8. Kaewpitoon N, Kaewpitton SJ, Philasri C, Leksomboon R, Maneenin C, Sirilaph S, Pengsaa P. Trichisosis: Epidemiology in Thailand. World J Gastroenterol 2006;12:6440-6445.
- 9. Lo YC, Hung CC, Lai CS, Uu Z, Nagano I, Maeda T, Takahashi Y, Chiu CH, Jiang DD. Human trichinosis after consumption of soft-shelled turtles, Taiwan. Emerg Infect Dis 2009;15:2056-2058.
- 10. Sohn WM, Kim HM, Chung DI, Yee ST. The first human case of Trichinella spiralis infection in Korea. Korean J Parasitol 2000;38:111-115.
- 11. Lee HC, Kim JS, Oh HY, Kim JH, Km HG, Lee MS, Kim WJ, Kim HT. A case of trichinosis caused by eating a wild badger. Korean J Med 1999;56:134-138.
- 12. Kim E, Pyun RH, Park JH, Kim KH, Choi I, Park HH, Lee YH, Yong TS, Hong SK. Family outbreak of trichinosis after eating a raw meat of wild swine. Infect Chemother 2003;35:180-184.
- 13. Hur GY, Hwang BY, Lee JG, Lee MG, Cheong HJ, Cho SW, Joo KH. An outbreak of trichinellosis caused by ingestion of raw wild boar. Korean J Int Med 2004;67:S917-S922.
- 14. Gajadhar AA, Pozio E, Gamble HR, Nockler K, Maddox-Hyttel CM, Forbes LB, Vallee I, Rossi P, Marinculic A, Boireau P. Trichinella diagnostics and control: Mandatory and best practices for ensuring food safety. Vet Parasitol 2009;159:197-205.
- 15. Richomme C, Lacourc SA, Ducrota C, Gilot-Fromontd E, Casabiancab F, Maestrinib O, ValleecI , Grassetc A, van der Giessenf J, Boireauc P. Epidemiological survey of trichinellosis in wild boar (Sus scrofa) and fox (Vulpes vulpes) in a French insular region, Corsica. Vet Parasitol 2010;172:150-154.
- 16. Gottstein B, Pozio E, Connolly B, Gamble HR, Eckert J, Jakob HP. Epidemiological investigation of trichinellosis in Switzerland. Vet Parasitol 1997;72:201-207.
- 17. Yimam AE, Oku Y, Nonaka N, Sakai H, Morishima Y, Matsuo K, Rosa G la, Pozio E, Yagi K, Kamiya M. First report of Trichinella native in red foxes (Vulpes vulpes schrencki) from Otaru City, Hokkaido, Japan. Parasitol Int 2001;50:121-127.
- 18. Kwon HS, Chung MS, Joo KH. PCR-RFLP patterns of four isolates of Trichinella for rDNA ITS1 region. Korean J Parasitol 2001;39:43-48.
Table 1.Hospital records of 8 trichinosis patients
Table 1.
|
No. |
Age/sex |
Symptoms |
Date of onset |
WBC count (eosinophil; %) |
Others |
|
1 |
48/F |
Generalized myalgia, headache, eyelid edema |
12.15 |
9,430 (29.6) |
CRP+ |
|
2 |
39/M |
Myalgia, headache, fever, facial edema |
12.15 |
4,760 (23.7) |
CRP+ |
|
|
|
|
|
CK/LDH+/+ |
|
3 |
48/M |
Myalgia, fever, chill |
12.23 |
12,510 (41.2) |
CRP+ |
|
4 |
62/M |
Headache, myalgia |
12.24 |
14,770 (24.6) |
CRP+ |
|
|
|
|
|
CK/LDH+/+ |
|
5 |
37/M |
Febrile sense |
12.25 |
4,640 (24.4) |
|
|
6 |
56/M |
Headache, sweating diarrhea (3 wk ago) |
12.21 |
4,930 (26.0) |
|
|
7 |
34/M |
Fever, myalgia |
12.21 |
12,720 (39.0) |
CRP+ |
|
8 |
37/M |
Facial edema, myalgia, fever |
12.21 |
5,130 (14.2) |
CRP+ |
Table 2.ELISA results in sera of 8 patients
Table 2.
|
No. |
Date of serum collection |
Positive control |
Negative control |
Patient’s ELISA titera
|
|
1 |
2011. 1. 3 |
0.346 |
0.002 |
0.026 |
|
2 |
2011. 1. 3 |
0.346 |
0.002 |
0.097 |
|
2011. 1. 11 |
0.376 |
0.005 |
0.253
|
|
3 |
2011. 1. 3 |
0.346 |
0.002 |
0.361
|
|
4 |
2011. 1. 3 |
0.346 |
0.002 |
0.255
|
|
5 |
2011. 1. 3 |
0.346 |
0.002 |
0.041 |
|
2011. 1. 11 |
0.376 |
0.005 |
0.107 |
|
6 |
2011. 1. 3 |
0.346 |
0.002 |
0.068 |
|
7 |
2010. 12. 30 |
0.346 |
0.002 |
0.175 |
|
2011. 1. 11 |
0.376 |
0.005 |
0.273
|
|
8 |
2011. 1. 4 |
0.346 |
0.002 |
0.240 |
|
2011. 1. 11 |
0.376 |
0.005 |
0.267
|
Table 3.Outbreaks of trichinosis occurred in Korea
Table 3.
|
No. |
Date |
No. of patients |
Infection source |
Locality |
Diagnosis [Reference No.] |
|
1 |
December 1997 |
4 |
Badger |
Geochang, Gyeongsangnam-do |
Muscle biopsy, Ab test [10,11] |
|
2 |
February 2001 |
5 |
Wild boar |
Inje-gun, Gangwon-do |
Muscle biopsy, ELISA |
|
3 |
February 2002 |
4 |
Wild boar |
Gangwon-do |
Muscle biopsy, PCR [12] |
|
4 |
March 2003 |
13 |
wild boar |
Inje-gun, Gangwon-do |
Muscle biopsy, ELISA [13] |
|
5 |
November 2010 |
8 |
wild boar |
Yanggu-gun, Gangwon-do |
ELISA (+) in 5 patients |
