Historical Overview of <italic>Taenia asiatica</italic> in Taiwan

Hong Kean Ooi; Chau-Mei Ho; Wen-Cheng Chung

doi:10.3347/kjp.2013.51.1.31

Korean J Parasito > Volume 51(1):2013 > Article

Ooi, Ho, and Chung: Historical Overview of Taenia asiatica in Taiwan

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

The Korean Journal of Parasitology 2013; 51(1): 31-36.

Published online: February 18, 2013

DOI: https://doi.org/10.3347/kjp.2013.51.1.31

Historical Overview of Taenia asiatica in Taiwan

Hong Kean Ooi¹, Chau-Mei Ho², Wen-Cheng Chung³

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

²Institute of Tropical Medicine, National Yang Ming University, Taiwan.

³Indigenous Health Research Center, Taipei Medical University, Taiwan.

Corresponding author (hkooi@mail.nchu.edu.tw)

Received October 24, 2012 Revised December 18, 2012 Accepted December 18, 2012

(open-access, http://creativecommons.org/licenses/by-nc/3.0/):

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

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

EARLY REPORTS OF HUMAN TAPEWORM INFECTIONS IN 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]).

DISCOVERY OF TAIWAN TAENIA

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.

EXPERIMENTAL ANIMAL INFECTION WITH T. ASIATICA EGGS

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].

CLINICAL MANIFESTATIONS AND CHEMOTHERAPY OF TAENIASIS PATIENTS IN TAIWAN

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).

LESIONS IN THE PIG LIVER

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].

PRESENT STATUS OF TAENIASIS IN TAIWAN

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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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.

Table 1.

Comparison of Cysticercus bovis from Taiwan and American Origins^a

Origin	Intermediate host	Cysticercus locality	Cysticercus examined	Hooklets on cyst
Origin	Intermediate host	Cysticercus locality	Cysticercus examined	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	39^b	39 (100%)	0

^a Fan et al. [11].

^b 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 Taiwan^a

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

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

Table 3.

Chemotherapeutic agents for cestode infections

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 taeniasis^a

No. of worms expelled	No. of cases	Deworming results		Questionaire
No. of worms expelled	No. of cases	Worm	With scolex	No. cases	Worm expelled
1	13	13	4	3	3^c
2	3	6	2	0
3	2	6	0	0
8	1	8	5	0
Total	19^b	33	11	3	3

^a Fan et al. [24].

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

^c Worms were expelled with atabrine 4 months later.

Table 5.

Efficacy of albendazole in the treatment of human taeniasis^a

Dose (mg×days)	No. cases treated	No. follow-up exam.	Deworming results		Retreatment^b		Cure rate (%)
Dose (mg×days)	No. cases treated	No. follow-up exam.	Worm	Not-noticed	No.	cases/cured	Cure rate (%)
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

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

^b 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 pigs^a

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

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