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Parasitology International 5

Taeniasis, cysticercosis and echinococcosis in Thailand

Jitra Waikagul *, Paron Dekumyoy, Malinee T. Anantaphruti

Department of Helminthology, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand

Available online 9 December 2005

Abstract

Taeniasis is one of the major food-borne parasitic zoonoses in Thailand. During the years 1957–1997, the prevalence was low in most parts of

the country. Recent (2000–2005) country prevalence was lower than 1%. A high prevalence (5.9%) was found among 1450 villagers from 30

villages in the North, and among 1233 stool samples from 19 provinces in the Northeast (2.8%). Taenia saginata was the dominant species.

Cysticercosis in Thailand is somewhat under-reported/recorded. During the period 1965–2005, diagnosis was based on techniques other than

serodiagnosis, giving a total of cysticercosis cases of less than 500. However, an immunoblot technique using delipidized cyst antigen showed 314

positive cases out of 754 samples tested in 2000–2005. Reports of neurocysticercosis appeared more often than cutaneous cysticercosis. A total of

24 cases of echinococcosis, mostly hydatid cysts (only 2 cases of alveolar cysts), were recorded during 1936–2005. These records included 3

cases of foreigners seeking surgery in hospitals in Bangkok. Most Thai patients were migrant workers from the Middle East, and only a few cases

were indigenous. The prevalence of cysticercosis and echinococcosis is increasing resulting from sensitive modern diagnostic tests. Taeniasis will

persist in Thailand as the consumption of raw/half-cooked meat dishes is still a normal practice for Thai people.

D 2005 Elsevier Ireland Ltd. All rights reserved.

Keywords: Taeniasis; Cysticercosis; Echinococcosis; Thailand

1. Introduction

Thailand is located in the Tropical zone of Southeast Asia

with a total population of over 63 million. Current prevalence

of parasitic infection is not high. National survey in 2001

recovered 11.2% hookworm infection, 9.4% opisthorchiasis,

1.5% trichuriasis, 1.2% ascariasis, 0.6% strongyloidiasis,

echinostomiasis and taeniasis, and 0.2% enterobiasis [Jong-

suksantigul P. Seminar on Parasitic infections in Northeast

Thailand, 22–23 November 2001; Khon Kaen, Thailand.

2001.p. 3–18 (in Thai)]. In remote area, particularly near the

country borders where minority ethnic groups are resided, soil-

borne and food-borne parasitic infections are still high. Cultural

habit of raw meat consumption and unhygienic way of living

are major risk factors of the infection to the natives in the

region.

This paper summarized taeniasis, cysticercosis and echino-

coccosis reported and recorded in concerned institutions in

Thailand.

1383-5769/$ - see front matter D 2005 Elsevier Ireland Ltd. All rights reserved.

doi:10.1016/j.parint.2005.11.027

* Corresponding author. Tel.: +662 354 9100; fax: +662 643 5600.

E-mail address: tmjwk@mahidol.ac.th (J. Waikagul).

2. Taeniasis

The nationwide stool survey was conducted using the

cellophane thick smear method during the years 1991–1992

among 45,163 populations of all ages. The overall prevalence

was 1.0%. Higher prevalence was observed in the north (2.3%)

and northeast (1.2%), low infection rate was found in the central

region (0.2%) and no case was observed among residents of the

south of the country [1]. A similar result was obtained in the

national investigation, in 1997 [Jiradit C, et al., Report of the

study. General Communicable Diseases Division, Department

of Communicable Control, Ministry of Public Health, 1997 (in

Thai)]. There were two previous nationwide surveys performed

in 1957 and 1982 [2,3]. The overall prevalence of taeniasis had

dropped from the two previous reports, but infection in the north

increased from 1.2% in 1957 to 2.3% in 1992 [1,2]. The last

national stool survey showed that country prevalence of

taeniasis was 0.6% [Jongsuksantigul P. Seminar on Parasitic

infections in Northeast Thailand, 22–23 November 2001; Khon

Kaen, Thailand. 2001.p. 3–18 (in Thai)]. However, high

prevalence (5.9%) was found among 1,450 villagers from 30

villages in the upper northern provinces [Wijit A, Kraewsan C.

Abstract, Joint International Tropical Medicine Meeting 2001,

5 (2006) S175 – S180

www.el

J. Waikagul et al. / Parasitology International 55 (2006) S175–S180S176

8–10 August 2001, Bangkok, Thailand]. Prevalence in the

Northeast among 1,233 stool samples from 19 provinces

examined by the cellophane thick smear method was 2.8%

[Jongsuksantigul P. Seminar on Parasitic infections in Northeast

Thailand, 22–23 November 2001; Khon Kaen, Thailand.

2001.p. 3–18 (in Thai)] and in 5,125 samples from six provinces

was 3.3% [Sithtithaworn P. Seminar on Parasitic infections in

Northeast Thailand, 22–23 November 2001; Khon Kaen,

Thailand. 2001. p. 115–21 (in Thai)]. Taeniasis was common

among the natives of the northern and northeastern provinces of

Thailand, where the people customarily eat raw or undercooked

beef or pork. In the endemic northern and northeastern regions,

different specific areas had different infection rates.

A high prevalence was elucidated by worm purging. An

investigation performed in 16 provinces of northeastern Thai-

land, revealed a 14.9% infection rate, Taenia worms were

expelled from 102 cases out of 681 subjects whose stools were

positive with eggs of other helminths [4]. A similar investiga-

tion was performed in 16 provinces of north Thailand, with an

average prevalence of 4.9(0–18.2)% [5]. Approximately 50

taeniasis cases attended yearly at the Out Patient Clinic of the

Hospital for Tropical Diseases, Faculty of Tropical Medicine,

Mahidol University, Bangkok [Anonymous, Annual Report

2002, Hospital for Tropical Diseases. Bangkok, 2002. (in

Thai)]. During the years 1977–1978, 39 patients who attended

the Out Patient Clinic of the Hospital for Tropical Diseases,

discharged segments of Taenia sp. in their stools [6] and the

figure in 2002 was slightly greater than the previous report.

This demonstrates that the rate of taeniasis has not decreased.

Furthermore, the results obtained from stool examination for

Taenia eggs do not represent the real infection rate, since

taeniid eggs are not generally discharged with feces. More

often, the proglottids are discharged with feces or emerge freely

from anus.

Among adults, the infection rate among males was two-fold

or more than that of females [2,4,7]. The percentage of

infection increases with age, with the highest incidence among

those aged 45–64 yr (12.5%), and 25–44 yr (11.4%). The

youngest infected child was only 2 years old [8]. Similarly, the

maximum infection rate was found in persons aged over 15

years (9.5%), whereas the rate was 1.2% in children aged 0–4

years in Sakhon Nakhon Province, northeastern Thailand [2].

3. Taenia species

Cases of taeniasis saginata are more common compared with

taeniasis solium, which is seldom found. From the scolices

purged from 26 cases after treatment, 24 were identified as T.

saginata, while only 2 were T. solium [6]. Chirasiri found a

similar result; from 9 scolices expelled from 10 patients, one

was T. solium and the rest were T. saginata [7]. In addition, 34

evacuated scolices [8] and proglottids from 23 infected

volunteers [9] were identified as T. saginata. T. solium infection

is rarely reported in the literature, with only 3 cases from the

above two reports. Stool examination and treatment for taeniasis

were performed in the central region of the country and

preliminary data showed that 4 patients expelled worms with

scolex; 2 cases of T. solium were found with 3 and 6 scolices in

each patient (Anantaphruti, unpublished data). Generally, only

one worm was harbored by an individual patient; however, the

maximum number of scolices of T. solium found in one patient

was 6 (Anantaphruti, unpublished data) and of T. saginata

scolices 5 [10]. Moreover, 2–3 scolices were seldom found (8 /

48 taeniasis saginata cases) [6,8]. Mixed infections of T. solium

and T. saginata in the same patient do occur [7].

In Thailand, gravid proglottids were taken from a patient in

Chiang Mai Province; the segments were identified as T.

saginata-like, according to the criterion that the number of

uterine branches ranged from 12 to 19 with a mean of 16. The

eggs from these gravid proglottids, 3000 in number, were orally

inoculated into small-eared-miniature pigs and Holstein calves.

Cysticerci were recovered from the livers of both pigs and

calves; the cysts from pigs were all alive, while those from the

calves had all degenerated and/or calcified. No cysticerci were

found from the muscles and other parts of the carcasses. The

mature cysticerci had two rows of tiny hooklets. Moreover, the

sizes of the cysticerci found in the liver were much smaller than

those of T. saginata and T. solium. On the other hand, they were

quite similar to those of Taenia from Taiwan, Korea and

Indonesia. The people from these countries are fond of

consuming raw and/or improperly cooked pork, as well as pig

viscera; hence they acquire taeniasis resembling T. saginata.

Nevertheless, the results of subsequent genetic studies demon-

strated that the gravid proglottids obtained from several patients

of Maharaj Nakorn Chiang Mai Hospital and of several districts

of Chiang Mai Province were all classical T. saginata [11,12].

4. Cysticercosis

4.1. Animal cysticercosis

Report on cysticercus infection in animals was very few. A

survey of cysticercosis in slaughter houses was conducted all

over Thailand in 1963, Manmontri [The 7th Scientific Meeting

of the Medical Association of Thailand, Chiangmai, Nov. 19–

22, 1963] found that 58 out of 63 slaughter houses had swine

infected with T. solium cysticerci, with a 1.1% average

infection rate. In Bangkok, 0.4% (2,019) of 514,387 pigs from

slaughterhouses harbored cysticerci. No current investigation

into swine cysticercosis is underway. Nevertheless, cysticerci

were found sporadically in pigs, and seen especially in wild

boars in mountainous areas (unpublished data). In 1995, meat

from a wild boar heavily infected with cysticerci was sent to

the Department of Helminthology, Faculty of Tropical Medi-

cine, from Saraburi Province in central Thailand, cysticercosis

cellulosae was diagnosed. No evidence of bovine cysticercus

infection was found, but in general, Cysticercus cellulosae in

pork is more prevalent than Cysticercus bovis in beef in

slaughterhouses.

4.2. Human cysticercosis

Cysticercosis, especially the cerebral type, has been sporad-

ically reported [13,14]. Furthermore, the racemosus type has

J. Waikagul et al. / Parasitology International 55 (2006) S175–S180 S177

also been reported [15]. Other sites of infection than subcuta-

neous cysticercosis have been rarely found, but do exist [16,17].

Taeniasis co-existing with cysticercosis in the same patient is

not uncommon. Chotmongkol reported the stool examination of

3 neurocysticercosis (NCC) patients, one of them had Taenia

eggs [14]. During the period 1979–1988, 4% of 98 NCC

registered at the Prasat Neurological Hospital had proglottids in

their stools [18]. In addition, a number of cases diagnosed as

NCC in hospitals in Bangkok and Chiang Mai had a history of

discharging Taenia proglottids in their stools [19–21].

Several retrospective studies were reported during the past

seven decades, some of the cases in those reports might be the

same. It was difficult to find out the exact number of

cysticercosis cases occurred in Thailand. However, in this

review, data of human cysticercosis will be summarized from

the existing publications, with no sorting out the repetition of

data.

During 1947 to 1979, 120 cases of cysticercosis and NCC

were reported [[22,23], Pradatsundarasar A. Commemoration

of the 20th Anniversary of the Faculty of Tropical Medicine,

Mahidol University: Bangkok, 1960–1980. 1980: 136–41 (in

Thai)]. Among these, twenty cases of subcutaneous cysticer-

cosis were reported from Phramongkutklao Hospital in 1966

[23]. When imaging devices were effectively used in the

diagnosis of cysticercosis, the numbers of cases detected

increased. During the period 1979–1988, 98 NCC cases were

recorded at the Prasat Neurological Hospital, all examined by

CT scan. Most patients resided in the central part of Thailand,

including Bangkok (over 50%), the north (27.6%), the east

(10.2%) and the northeast (11.2%). It was not recorded in the

south [18].

During the period 1965–1997, there were more than 103

cases from the north, Chiang Mai, Lamphun, Phae, Phayao,

and unidentified areas [18,24–27]. In the northeast, there were

more than 43 cases, 12 patients lived in Khon Kaen and

adjacent provinces [28], 14 cysticercosis cases were reported in

Mukdahan, and Sakhon Nakhon [29,30]. For another 17 cases,

the provinces of origin were not recorded [18,27,31]. About 60

cases were reported in the central part of Thailand; Nakhon

Sawan (1 case), and Bangkok and many adjacent provinces (59

cases) [18,27,32–34] and only one case has been reported in

the south [27].

In a study during the years 1981–1986, 132 patients were

concluded on characteristic CT and clinical findings. Eight

patients had pathological confirmation and 13 had associated

subcutaneous nodules or characteristic calcification in the

muscles. Several other patients, whose CT findings were

suggestive of cerebral cysticercosis but for whom the data were

inadequate to support the diagnosis, were excluded. Three

patients were initially diagnosed based on CT findings as

cerebral cysticercosis versus brain tumor; one of these was

surgically proved later to be a cystic cerebella hemangioblas-

toma, and the other two to be cerebral gliomas. One patient

presented with a large solitary cyst in the right frontal lobe,

which was diagnosed as a cystic tumor or an arachnoid cyst but

surgically proved to be a cysticercosis cyst. The CT findings

from those patients were present, and 30% of the patients’ data

had multiple findings. In this series, punctuate parenchymal

calcifications were most commonly found. The median age of

the patients was 48 years. Large, thin-walled parenchymal

cysts appeared to be rather uncommon in this series especially

a single large cyst, which had to be differentiated from cystic

lesions, such cystic astrocytoma and arachnoid cyst. Small

parenchymal cysts of less than 1 cm in diameter are more

common and rather pathognomonic when a mural nodule

containing scolex was present, producing a characteristic ‘‘ring-

with-eccentric-dot’’. The thin wall of the parenchymal cyst was

not imaged on CT per se; it could only be inferred from the

sharps, and smooth outline of the cyst fluid [35].

In a five-year review (1993–1997) of 25 cases diagnosed as

cysticercosis at Rajvithi Hospital, Bangkok, and the distribu-

tion of cases was highest in the north, followed by central,

northeast and southern Thailand. Higher proportion of NCC

(60%, 15 /25) was diagnosed. CT scan examined only 12 cases

of this cohort, and 11 cases presenting calcified cysts [27].

Cases of parenchymal cysticercosis with seizures were also

reported; they may be focal seizures or generalized tonic clonic

seizures. Infrequent records were of the subarachnoid space

and ventricular forms. Subarachnoid space cysticercosis

caused eosinophilic meningitis and this form is rare [Chot-

mongkol V. Seminar on Parasitic infections in Northeast

Thailand, 22–23 November 2001; Khon Kaen, Thailand.

2001. p. 78–98 (in Thai)]. The Hospital for Tropical Diseases,

Faculty of Tropical Medicine, Bangkok recorded over 10 NCC

cases, which examined by CT scan, showed cysts in the brain

and other soft tissues (personal communication, Prof. Sirivan

Vanijanonta).

Among 390 reported cases, cysticercus was reported in

brain in 271 cases, in subcutaneous tissue in 82 cases, in parts

of the eyes in 16 cases and other parts 21 cases. Other parts of

the human body where T. solium metacestodes have developed

were one case of myocardium cysticercosis [36], 5 cases of

generalized cysticercosis [19]. Twenty-three cases were

reported in many parts of the body [24,27,35]. One post-

mortem case of cysticercosis was found to have infection of the

brain, heart and lung [32]. A large T. solium metacestode cyst

(6�3�2 cm) was found at the anterior abdominal wall of a

Chinese woman [34]. One autopsy case was reported as

cerebral cysticercosis, and was accompanied by infection of the

lungs and thyroid gland, which was very rare [17]. Cysticer-

cosis at the chest wall was shown by X-ray film [16].

Cases of cysticercosis from publication, official and unof-

ficial sources seem to be underreported. Cases under 50 years

reviewed from 1947–1997 accumulated to less than 500. Since

1995, the Department of Helminthology, Faculty of Tropical

Medicine, Mahidol University, has served as the serodiagnosis

laboratory for cysticercosis using homemade antigen. From 754

suspected cases submitted to immunoblot testing; 314 cases

(41.8%) were found positive during 2000–2005.

5. Echinococcosis

It was believed that echinococcosis did not occur in

Thailand because mutton was not popular meat for consump-

J. Waikagul et al. / Parasitology International 55 (2006) S175–S180S178

tion and as a result, sheep raising was not common, and the

fresh internal organs of animals were not normal feed for dogs.

In 1936, the first echinococcosis case was reported [37]. From

1936–2005, a total of 24 cases were identified, and are

summarized in Table 1; full papers have not been published for

all cases. The following information is based on those

publications, personal communications, and the records of

concerned institutions.

The lung is the most commonly infected organ with

hydatid cysts, and more cases showed the cysts on the left

lobe than on the right lobe [[38–40], Na Songkhla, the

Annual Meeting of the Thailand Society of Chest Diseases,

1978, Bangkok] Pulmonary hydatidosis is generally associat-

ed with repeated hemoptysis, anemia, and general weakness

[38] and might be confused with tuberculosis, particularly at

the early stage in which imaging shows a small spot [40]. The

second most common location for cyst formation is the liver.

Hepatic hydatidosis is associated with chronic abdominal

pain, low fever, yellowish skin, nausea and vomiting. It might

be confused with amebic liver abscess [41]. In severe cases, it

might appear similar to gastrointestinal bleeding with black

stool and vomit stained with blood, with headache, nausea,

weakness but no abdominal pain; it might be confused with

stomach cancer [42]. The case having abdominal cavity cyst,

complained of swelling of the abdomen, together with a sense

of heaviness. The abdomen was distended and contained free

fluid; it might be diagnosed as abdominal carcinomatosis

[37].

Radiograph, ultrasound and CT scan are normal tools for

demonstrating cysts in the human body. The diagnostic

Table 1

Summarized echinococcosis cases in Thailand from 1936-March 2005

No. Province Previous residence Yea

1. Chiang Mai Thailand 193

2. Bangkok India 195

3. – – 196

4. Bangkok Thailand 197

5. Rachaburi Thailand 198

6. Nakhon Pathom – 198

7. Krabi Thailand 199

8. Ratchaburi Thailand 199

9. Lamphun Thailand 199

10. – Middle east 199

11. Lamphun – 199

12. Chiang Mai – 199

13. Chiang Mai – 199

14. Lamphun – 199

15. Bangkok Thailand 199

16. Lamphun Thailand 199

17. Nepal Nepal 199

18. – Middle east 199

19. – Thailand 200

20. Nakhon Si Thammarat Thailand 200

21. Phetchabun Switzerland 200

22. Middle east Middle east 200

23. Middle east Middle east 200

24. – – 200

* Alveolar cyst.

** Trop. Med. Data (unclear!).

procedure would start with ultrasound or either one of the

imaging tools, followed by needle aspiration. Aspirated fluid is

examined for protoscolices for confirmation of parasite species.

Serodiagnosis is a useful tool for identifying infection. At

present, serodiagnosis to detect antibodies against the Echino-

coccus parasite has been developed in two laboratories in

Thailand, at the Department of Parasitology, Faculty of

Medicine, Chiang Mai University, and at the Department of

Helminthology, Faculty of Tropical Medicine, Mahidol Uni-

versity. During 1986–2005, 47 sera samples were submitted to

the Department of Helminthology for testing echinococcosis

antibody. ODs-ELISA of 6 samples had showed higher values

than the positive control samples, and then using immunoblot

three out of ten samples were positive. Six samples of aspirated

fluid from liver cysts were submitted for parasite confirmation.

Scolicies of Echinococcus were detected in four samples.

Sequencing of scolicies from two samples confirmed species of

E. granulosus sheep strain.

Echinococcosis is a rare disease in Thailand. Since 1936,

only 24 cases of indigenous and imported echinococcosis have

been reported. Only two cases of alveolar echinococcosis were

recorded [37,43], while the other cases were cystic echinococ-

cosis [[38–42,44–49], Thamtakerngkit S, Noppahkun N. An

abstract presented at the First National Congress of Pathology,

Thailand, 22 March 1989.]. 7 cases were residents of the

northern part of the country, one case was from the south, and

the others resided in the central region. Information on how the

patients were infected is scanty rare. Most hydatid cysts were

found in lungs and liver, while they were also found in the

abdomen, kidney, jaw and foot.

r Nationality Sex Age Affected site

6 Thai M 52 Abdomen*

2 Indian M 16 Lung

0 Non-Thai F 63 Liver

8 Thai F 56 Lung

0 Thai F 32 Lung

9 Thai F 45 Foot

1 Thai M 32 Lung

2 Thai M 27 Lung

3 Thai F 39 Kidney

4 Thai M 50 Liver

4 – M 32 Jaw

4 – M 12 Liver, lung

4 – F 31 Liver

4 – F 71 Lung

5 Thai F 32 Abdomen

5 Thai F 61 Lung

5 Nepalese M 36 Liver

6 Thai M 50 Liver

3 Thai F – –**

4 Thai F 58 Liver

4 Thai F 40 Liver*

4 Non-Thai M 20 Liver**

4 Non-Thai M 28 Liver**

4 Thai M 15 Liver**

J. Waikagul et al. / Parasitology International 55 (2006) S175–S180 S179

The reports of indigenous cases show that echinococcosis

exists where it was believed in the past that Thailand was not

an endemic area for this parasite. Infections in humans proved

that dogs must be infected though this has never been

reported. The prevalence should be very low. There has been

no record of animal infection with echinococcosis in Thai-

land. However, there was verbal information that, in the past,

pigs, cattle, and buffalo slaughtered in Bangkok and Chiang

Mai harboured hydatid cysts. The infection rate was not high

and cysts were not found in the past ten years. Infection in

dogs has never been reported. Disease surveillance should be

carried out in cattle and sheep farming areas. Dog’s fecal

samples should be examined to confirm infection rates,

transmission profile, and to plan for prevention and control

policies.

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