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Articles from Symposium on Asian Taenia (October 2011, Osong, Korea)

Historical Overview of Taenia asiatica in Taiwan

Hong Kean Ooi1, Chau-Mei Ho2, Wen-Cheng Chung3
The Korean Journal of Parasitology 2013;51(1):31-36.
Published online: February 18, 2013

1Department of Veterinary Medicine, National Chung Hsing University, Taiwan.

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Corresponding author (hkooi@mail.nchu.edu.tw)
• Received: October 24, 2012   • Revised: December 18, 2012   • Accepted: December 18, 2012

© 2013, Korean Society for Parasitology and Tropical Medicine

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  • An overview of the epidemiological, biological, and clinical studies of Taenia and taeniasis in Taiwan for the past century is presented. The phenomenal observations that led to the discovery of Taenia asiatica as a new species, which differ from Taenia solium and Taenia saginata, are described. Parasitological surveys of the aborigines in Taiwan revealed a high prevalence of taeniasis, which might be due to the culture of eating raw liver of hunted wild boars. Chemotherapeutic deworming trials involving many patients with taeniasis were discussed. Praziquantel was found to be very effective, but sometimes complete worms could not be recovered from the feces after treatment, probably due to the dissolution of the proglottids. Atabrine, despite some side effects, can still be used, in properly controlled dosages, as the drug of choice for human T. asiatica infection if we need to recover the expelled worms for morphological examinations. Research results on the infection of T. asiatica eggs from Taiwan aborigines in experimental animals were also noted. Since the pig serve as the natural intermediate host of T. asiatica and the predilection site is the liver, a differential comparison of other parasitic pathogens that might cause apparently similar lesions is also presented.
  • Key words: Taenia asiatica, Taiwan Taenia, chemotherapy, symptoms, pig liver lesion, Taiwan
Taiwan and the offshore island of Penghu came under the Japanese rule in 1895 under the Treaty of Shimonoseki, when the Ching government of China ceded the islands to the Japanese government. In 1911, the Republic of China was founded, replacing the Ching government in China. However, Japanese ruled Taiwan until the end of the Second World War in 1945. Then, the Nationalist government of China came over and took control of Taiwan until this day.
The first report of taeniasis in Taiwan was made by Oi in 1915 [1], when he found 2 positive cases in a fecal parasitological survey of 301 persons composing of prisoners, students, and patients in Taichung, central Taiwan. In 1927, Oi [2] reported that 2 Japanese immigrants were shedding taeniid eggs out of 220 people surveyed for intestinal parasites in Hualien port city. Then, in 1928, Yokogawa and his associates [3] reported that out of 812 aborigines surveyed in Hsinchu, 163 (20%) were found to be excreting taeniid eggs. The locations of the study areas are shown in Fig. 1.
It was not until 1952, when Huang and associates [4-6] reported that 20.5% (130/634) of the aborigines surveyed in Wulai, Taipei prefecture [4], 16.3% (300/1,839) in Lotung, Ilan prefecture [5], and 9.7% (49/503) in Nan-ao, Ilan prefecture [6], were positive for taeniid eggs shedding, respectively. Since then, about 20 reports on the prevalence of taeniasis in humans in Taiwan had been published in the 1960s, all under the assumption that the causative agent was Taenia saginata. Taenia solium is extremely rare in Taiwan with only 5 cases being reported from 1957 to 1970 by Hsieh in southern Taiwan (Cited in Chung & Liu [7]).
It was only in 1966, when Huang and associates [8] first proposed that the Taenia tapeworm infecting the Taiwan aborigines in such high prevalences might not be the same as the classical T. saginata. They observed that the aborigines do not have access to beef, and their main animal protein source came mainly from wild boars and other hunted wildlife [8,9].
It was only in the 1970s that experimental infection of the eggs of Taiwan taeniid and that of the American T. saginata was carried out in bovine calf and goats for comparison [10]. The cysticerci of the American isolate were found in the muscles of the neck, rib, heart, and legs but not in the liver. Whereas, about half of the cysticerci of the Taiwan isolate were found in the liver of the infected calf. Moreover, no hooklets were observed in any of the American isolate cysticerci, but 88% of the Taiwan isolate cysticerci had hooklets on their rostellum. In addition, it was also observed that the various morphormetric parameters, such as the body length and width, protoscolex, and sucker diameter were larger for the American isolate than the Taiwan isolate. All the cysticerci of the Taiwan isolate in the experimentally infected goat were recovered only from the liver, and all of them had hooklets. It was later observed that the cysticerci of Taiwan Taenia could not grow in the liver of the cow because they degenerate at 2 months post-infection.
In the 1980s, it was apparently becoming clear that Taiwan Taenia might be a different species than that of the classical T. saginata, based on the site of predilection being in the liver, its developmental morphology, and the pig serving as its natural intermediate host (Table 1) [11,12]. The paradox of this parasite epidemiology is that in the area where T. saginata-like infection in humans is widely prevalent, the inhabitants had little chance of eating beef, and Cysticercus bovis were not present in the bovids in that area. However, the inhabitants had the habit and chance of eating raw liver of pigs. Then, Fan and collaborators from other countries observed that taeniids with similar characteristics to Taiwan Taenia were also found in other Asian countries such as Korea (Cheju-do Island), Indonesia (Samosir Island), the Philippines, Thailand (Chiang Mai), and Myanmar [13-15].
In the early 1990s, despite the overwhelming genetic evidence that the Taiwan Taenia might be a new species, American and Australian workers still suggested that it would be more appropriate to classify it as a subspecies of T. saginata [16]. Thus, in 1995, Fan and associates [17] proposed that the Taiwan Taenia be named as T. saginata asiatica, and the classical T. saginata found in America and Europe as T. saginata saginata. Today, that parasite, which is prevalent in many Asian countries, is now internationally recognized as a distinct species, namely, T. asiatica, mainly through the efforts and description of Eom and colleagues in Korea [18,19]. Fan and his coworkers published more than 100 papers on T. asiatica. He passed away on 2 September, 2008, due to an aortic aneurysm at the age of 86.
Cysticerci of T. asiatica have been recovered mainly from the liver of pig, calf, goat, and monkey after oral inoculation of the eggs. However, only calcified and degenerated cysticerci were observed in the liver of goat and monkey [13,20]. T. asiatica cysticerci were found to be able to develop to maturity in scid mice [21,22] and also Mongolian gerbil [21] after subcutaneous injection of oncospheres. These cysticerci were able to grow to maturity in the rodents and then develop into the tapeworm stage in the rodent alternative definitive host or in humans [23].
Humans infected with taeniasis infection experience many types of clinical symptoms but not all of them are the same. Table 2 shows the clinical manifestation of taeniasis among Aborigines in Taiwan and these patients were most probably infected with the Taiwan Taenia. To study the various symptoms of Taiwan taeniasis and to obtain the adult worm, many brave researchers had volunteered to orally infect themselves with cysticerci of T. asiatica by eating the raw pig liver (Fig. 2).
Since there were many taeniasis patients in Taiwan through the 6 decades, many types of drugs had been used in the chemotherapeutic deworming trials. These drugs include atabrine (quinacrine), dichlorophen (arecoline), bithionol (bithin), yomesan (niclosamide), acanil (mebendazole), albendazole, and praziquantel (Table 3). It was observed that niclosamide (Table 4) [24], albendazole (Table 5) [25,26], and mebendazole [27] were not very efficacious against human T. asiatica infections. However, Rim et al. [28,29] stated that albendazole was effective for treatment of T. saginata and T. solium. Nevertheless, it must be noted that the efficacy of anthelmintic drugs can be influenced by the patient's physiological status such as being in a fasting or non-fasting condition [30].
Praziquantel, at a single dose of 150 mg, was found to be the most effective against T. asiatica infection in humans, without causing any side reaction [27]. This efficacy is followed by atabrine and then by niclosamide [31]. However, sometimes no complete worms could be recovered from the feces of the patient after treatment, probably due to dissolution of the worm by the drug.
Atabrine, despite producing some side effects, can still be used, in properly controlled dosages, as the drug of choice for human T. asiatica infection if we need to recover the expelled worms for morphological examinations. It can be taken orally at a total of 1 gm divided into 2 equal doses given at 30 min interval, after the patient is fasted and given 4 gm of sodium bicarbonate to prevent vomiting. The patient should then be given a purgative of magnesium salt (25 g in 1 liter of water) at 1.5 hr after taking the second dose. The expelled worm can then be collected from the feces within a few hours. To date, the most number of worms collected from a single patient in Taiwan was 24 specimens, after medication with atabrine (Fig. 3).
The pig serves as the natural intermediate host of T. asiatica and the site of predilection is in the liver (Fig. 4). However, other parasitic pathogens might also cause apparently similar hepatic lesions. A differential comparison of the hepatic lesions caused by other parasites is presented in Table 6 [32-36].
T. asiatica is still present in Taiwan today but in only some aborigines who live in the mountainous areas. However, the cases are getting rarer with the improvement of rural medical health services. Taenia asiatica has always been there and has come a long way for its recognition. We just need to train our eyes to see in different dimension.
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  • 27. Fan PC, Chung WC, Chan CH, Chen YA, Cheng FY, Hsu MC. Studies on taeniasis in Taiwan. V. Field trial on evaluation of therapeutic efficacy of mebendazole and praziquantel against taeniasis. Southeast Asian J Trop Med Public Health 1986;17:82-90.
  • 28. Rim HJ, Joo KH, Lee JS, Wang JS. Anthelmintic effect of albendazole (Zentel R) against helmintic infections. Korean J Rural Med 1984;9:67-73.
  • 29. Rim HJ, Joo KH, Park HS. Anthelmintic effect of albendazole against Taenia saginata and Taenia solium infections. J Korean Soc Chemother 1989;7:29-39.
  • 30. Fan PC, Chung WC, Lin CY, Wu CC. The effect of fasting on the treatment of taeniasis. Chin J Parasitol 1990;3:93-95.
  • 31. Fan PC, Chung WC, Lin CY, Chan CH. Clinical manifestations of taeniasis in Taiwan aborigines. J Helminthol 1992;66:118-123.
  • 32. Iburg T, Johansen MV, Leifsson PS, Willingham AL, Lindberg R. Hepatic changes in congenital Schistosoma japonicum infections in pigs. J Comp Pathol 2007;136:250-255.
  • 33. Kamiya M, Ooi HK, Oku Y, Okamoto M, Ohbayashi M, Seki N. Isolation of Echinococcus multilocularis from the liver of swine in Hokkaido, Japan. Jpn J Vet Res 1987;35:99-107.
  • 34. van Veen S. Facioliasis (Fasciola gigantica) in West Africa: A review. Vet Bull 1980;50:529-533.
  • 35. Soulsby EJL. Helminths, Arthropods and Protozoa of Domesticated Animals. 1982, 7th ed. London, UK. Bailliere Tindall Publ. Ltd; pp 1-809.
  • 36. Taira K, Saeed I, Permin A, Kapel CM. Zoonotic risk of Toxocara canis infection through consumption of pig or poultry viscera. Vet Parasitol 2004;121:115-124.
Fig. 1
Map of Taiwan showing the locations where early epidemiological taeniasis surveys were carried out.
kjp-51-31-g001.jpg
Fig. 2
A volunteer, Dr. Chung WC, trying to infect himself with Taenia asiatica by eating raw wild boar liver that contained cysticerci.
kjp-51-31-g002.jpg
Fig. 3
A Taenia asiatica patient, Mr. Chen Chin-Fu, with 24 strobilae that were purged from him after using atabrine.
kjp-51-31-g003.jpg
Fig. 4
Cysts of Taenia asiatica in the liver of a pig.
kjp-51-31-g004.jpg
Table 1.
Comparison of Cysticercus bovis from Taiwan and American Originsa
Table 1.
Origin Intermediate host Cysticercus locality Cysticercus examined Hooklets on cyst
Absent Present
Taiwan aborigine Calf (cow) Liver 33 6 (18.2%) 27 (81.8%)
Taiwan aborigine Goat Liver 16 0 (0.0%) 16 (100%)
American volunteer Calf (cow) Musclesb 39b 39 (100%) 0

aFan et al. [11].

bA total of 48 cysticerci were recovered in the heart (8), neck (4), intercostal (4), foreleg (24), and hindleg (8) muscles, but only 39 were examined.

Table 2.
Clinical manifestation of taeniasis among aborigines in Taiwana
Table 2.
Clinical signs No. of cases (Total 1,258) %
Proglottids shed in feces 1,200 95
Pruritis at perianal area 963 77
Nausea 584 46
Abdominal pain 564 45
Dizziness 523 42
Increased appetite 374 30
Headache 321 26
Diarrhea 222 18
Weakness/Lethargy 210 17
Feeling of hunger 200 16
Constipation 135 11
Weight loss 71 6
Abdominal discomfort 66 5
Tiredness 53 4
Loss of appetite 52 4
Vomiting 50 4
No appetite despite fasting 14 1
Muscular pain 13 1
Stomach discomfort 9 < 1
Gastric pain 8 < 1
Feeling sleepy 4 < 1
Convulsion 2 < 1
Anxiety 2 < 1
Skin pruritis 1 < 1
Respiratory irregularity 1 < 1
Hunger pain 1 < 1

aChung et al. [16], Fan et al. [12,15,31].

Table 3.
Chemotherapeutic agents for cestode infections
Table 3.
Chinese herbs (plant name, effective compound) Drug name
Pumpkin seed (Cucurbita pepo, Cucurbitine) Atabrine (Quinacrine)
Betel nut (Areca catechu, Arecoline) Dichlorophen
Somegranate root (Pumca granatum, Pelletierrine) Bithionol (Bithin)
Filix mas (Oleoresin aspidium) Yomesan (Niclosamide)
Kamala (Mollotus philippinensis) Acanil (Mebendazole)
Table 4.
Efficacy of niclosamide in the treatment of human taeniasisa
Table 4.
No. of worms expelled No. of cases Deworming results
 Questionaire
Worm With scolex No. cases Worm expelled
1 13 13 4 3 3c
2 3 6 2 0
3 2 6 0 0
8 1 8 5 0
Total 19b 33 11 3 3

aFan et al. [24].

bCure rate, 84.2% (16/19); dose of niclosamide, 2 g/case.

cWorms were expelled with atabrine 4 months later.

Table 5.
Efficacy of albendazole in the treatment of human taeniasisa
Table 5.
Dose (mg×days) No. cases treated No. follow-up exam. Deworming results
 Retreatmentb
 Cure rate (%)
Worm Not-noticed No. cases/cured
400×1 54 30 22 8 30 0 0.0
800×1 10 8 7 1 8 0 0.0
800×2 20 14 11 3 14 2 14.3
800×3 10 7 5 2 4 2 50.0
1,200×2 10 6 5 1 6 3 50.0
1,200×3 12 11 8 3 4 2 50.0
Total 116 76 58 18 76 9 12.0

aChung et al. [25], Fan et al. [26].

bCure rate of albendazole, 12.0% (9/76). The cases not cured by albendazole treatment and still expelling worms were retreated with atabrine 3 months later.

Table 6.
Parasites that produce lesions in the liver of pigsa
Table 6.
Parasite Location Principal lesions in the liver
Clonorchis sinensis Bile duct Dilation of the bile duct, periductal fibrosis
Opisthorchis tenuicollis Bile duct Dilation of the bile duct, periductal fibrosis
Dicrocoelium dendriticum Bile duct Dilation of the bile duct, periductal fibrosis
Fasciola hepatica Bile duct Dilation of the bile duct, periductal fibrosis
Fasciola gigantica Bile duct Dilation of the bile duct, periductal fibrosis
Schistosoma japonicum Liver Pinpoint white spot, granuloma
Taenia hydatigena Liver White cyst
Echinococcus granulosus Liver White cyst
E. multilocularis Liver White cyst
Taenia asiatica (Taiwan taenia) Liver White cyst
Ascaris suum Liver Pinpoint white spot
Toxocara canis Liver Pinpoint white spot
Stepahnurus dentatus Liver Pinpoint white spot

aIburg et al. [32], Kamiya et al. [33], Schilhorn van Veen [34], Soulsby [35], Taira et al. [36].

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Historical Overview of Taenia asiatica in Taiwan
Korean J Parasitol. 2013;51(1):31-36.   Published online February 18, 2013
DOI: https://doi.org/10.3347/kjp.2013.51.1.31
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Historical Overview of Taenia asiatica in Taiwan
Korean J Parasitol. 2013;51(1):31-36.   Published online February 18, 2013
DOI: https://doi.org/10.3347/kjp.2013.51.1.31
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Historical Overview of Taenia asiatica in Taiwan
Image Image Image Image
Fig. 1 Map of Taiwan showing the locations where early epidemiological taeniasis surveys were carried out.
Fig. 2 A volunteer, Dr. Chung WC, trying to infect himself with Taenia asiatica by eating raw wild boar liver that contained cysticerci.
Fig. 3 A Taenia asiatica patient, Mr. Chen Chin-Fu, with 24 strobilae that were purged from him after using atabrine.
Fig. 4 Cysts of Taenia asiatica in the liver of a pig.

Fig. 1

Fig. 2

Fig. 3

Fig. 4

Historical Overview of Taenia asiatica in Taiwan
Origin Intermediate host Cysticercus locality Cysticercus examined Hooklets on cyst
Absent Present Taiwan aborigine Calf (cow) Liver 33 6 (18.2%) 27 (81.8%) Taiwan aborigine Goat Liver 16 0 (0.0%) 16 (100%) American volunteer Calf (cow) Musclesb 39b 39 (100%) 0 Clinical signs No. of cases (Total 1,258) % Proglottids shed in feces 1,200 95 Pruritis at perianal area 963 77 Nausea 584 46 Abdominal pain 564 45 Dizziness 523 42 Increased appetite 374 30 Headache 321 26 Diarrhea 222 18 Weakness/Lethargy 210 17 Feeling of hunger 200 16 Constipation 135 11 Weight loss 71 6 Abdominal discomfort 66 5 Tiredness 53 4 Loss of appetite 52 4 Vomiting 50 4 No appetite despite fasting 14 1 Muscular pain 13 1 Stomach discomfort 9 < 1 Gastric pain 8 < 1 Feeling sleepy 4 < 1 Convulsion 2 < 1 Anxiety 2 < 1 Skin pruritis 1 < 1 Respiratory irregularity 1 < 1 Hunger pain 1 < 1 Chinese herbs (plant name, effective compound) Drug name Pumpkin seed (Cucurbita pepo, Cucurbitine) Atabrine (Quinacrine) Betel nut (Areca catechu, Arecoline) Dichlorophen Somegranate root (Pumca granatum, Pelletierrine) Bithionol (Bithin) Filix mas (Oleoresin aspidium) Yomesan (Niclosamide) Kamala (Mollotus philippinensis) Acanil (Mebendazole) No. of worms expelled No. of cases Deworming results
Questionaire
Worm With scolex No. cases Worm expelled 1 13 13 4 3 3c 2 3 6 2 0 3 2 6 0 0 8 1 8 5 0 Total 19b 33 11 3 3 Dose (mg×days) No. cases treated No. follow-up exam. Deworming results
Retreatmentb
Cure rate (%) Worm Not-noticed No. cases/cured 400×1 54 30 22 8 30 0 0.0 800×1 10 8 7 1 8 0 0.0 800×2 20 14 11 3 14 2 14.3 800×3 10 7 5 2 4 2 50.0 1,200×2 10 6 5 1 6 3 50.0 1,200×3 12 11 8 3 4 2 50.0 Total 116 76 58 18 76 9 12.0 Parasite Location Principal lesions in the liver Clonorchis sinensis Bile duct Dilation of the bile duct, periductal fibrosis Opisthorchis tenuicollis Bile duct Dilation of the bile duct, periductal fibrosis Dicrocoelium dendriticum Bile duct Dilation of the bile duct, periductal fibrosis Fasciola hepatica Bile duct Dilation of the bile duct, periductal fibrosis Fasciola gigantica Bile duct Dilation of the bile duct, periductal fibrosis Schistosoma japonicum Liver Pinpoint white spot, granuloma Taenia hydatigena Liver White cyst Echinococcus granulosus Liver White cyst E. multilocularis Liver White cyst Taenia asiatica (Taiwan taenia) Liver White cyst Ascaris suum Liver Pinpoint white spot Toxocara canis Liver Pinpoint white spot Stepahnurus dentatus Liver Pinpoint white spot
Table 1. Comparison of Cysticercus bovis from Taiwan and American Originsa

Fan et al. [11].

A total of 48 cysticerci were recovered in the heart (8), neck (4), intercostal (4), foreleg (24), and hindleg (8) muscles, but only 39 were examined.

Table 2. Clinical manifestation of taeniasis among aborigines in Taiwana

Chung et al. [16], Fan et al. [12,15,31].

Table 3. Chemotherapeutic agents for cestode infections
Table 4. Efficacy of niclosamide in the treatment of human taeniasisa

Fan et al. [24].

Cure rate, 84.2% (16/19); dose of niclosamide, 2 g/case.

Worms were expelled with atabrine 4 months later.

Table 5. Efficacy of albendazole in the treatment of human taeniasisa

Chung et al. [25], Fan et al. [26].

Cure rate of albendazole, 12.0% (9/76). The cases not cured by albendazole treatment and still expelling worms were retreated with atabrine 3 months later.

Table 6. Parasites that produce lesions in the liver of pigsa

Iburg et al. [32], Kamiya et al. [33], Schilhorn van Veen [34], Soulsby [35], Taira et al. [36].

Table 1.

Table 2.

Table 3.

Table 4.

Table 5.

Table 6.

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