S. S. Margono et al.

115

Taeniasis and Cysticercosis in Indonesia

Sri S. Margonol, Toni Wandra2, Thomas Suroso2 and Akira Ito3

lDepartment
of Parasitology, Faculty of Medicine, University of Indonesia, 2Directorate
General Communicable Disease Control and Environmental Health, Ministry of Health,
Indonesia, Jakarta, Indonesia; 3Department of Parasitology, Asahikawa Medical College,
Asahikawa, Japan E-mail: mardiastutiw@yahoo.com

The most important human cestodes in lndonesia
arc Taenia solium, Taenia saginata, and Taenia
asiatica, known to be found in several provinces of
the country. Taeniasis and cysticercosis are mostly
found in three provinces oflndonesia: Papua (the
present name of Irian Jaya), Bali and North
Sumatra. Cases were also discovered in Lampung,
North Sulawesi, South-East Sulawesi, East
Nusatenggara, East Kalimantan, West Kalimantan,
East Java and Jakarta. Although the majority of
Indonesian people are Muslim and do not eat pork,
some areas or islands of lndonesia have been
known to be contaminated with the pork tapeworm,
T. solium, where the most of local people are
Christian or Hindi.
Neurocysticercosis (NCC) caused by the larvae
of Taenia solium is now highly endemic in lipua
Province, Indonesia. An international collaboration
project on an epidemiological study of
taeniasis/cysticercosis inIndonesia has been
carried out in Jayawijaya District, Papua since
1996. lt consists of sero-epidemiological analysis
of local persons, detection of pigs and dogs
infected with Z. solium based on serology, since
both pigs and dogs are roaming free access to
human feces. Copro-antigen test for detection of
taeniasis worm carriers and mitochondrial DNA
analysis was performed. Eggs prepared from
gravid segments were also used for experimental
infection in NOD/Shi-scid mice. From 1996,
several funds from Japan were available through
Gifu University and Asahikawa Medical College.
WHO has funded for training and education of
local health workers and school children.
Technical transfer has been carried out several
times in Gifu University and Asahikawa Medical
College, Japan. Asahikawa Medical College has
been supporting to establish the laboratory
reference center in Indonesia.
l. Introduction
The most important human cestodes in Indonesia
are T. solium, T. saginata, and T. asiatica, known
to be found in several provinces of the country.
Taeniasis, the disease in humans, is caused by the
adult worm of T. solium as well as T. saginata,
whereas the cysticercus, the larva of T. solium,
cause cysticercosis, not only in humans but also in
pigs and dogs. The cysticercus of T. saginata is
found in muscles of cattle, however we can find
the cysticercus of Z. asiatica in the liver of pigs.
Taeniasis and cysticercosis are mostly found in
three provinces of Indonesia: Papua (the present
116 Taeniasis and Cysticercosis in Indonesia
name of Irian Jaya), Bali and North Sumatra.
Cases were also discovered in Lampung, North
Sulawesi, South-East Sulawesi, East Nusaten War a,
East Kalimantan, West Kalimantan, East Java and
Jakarta [-4].
Surveys conducted since the 1970e were mostly
based on examinations of stool samples by direct
smear or concentration technique. In North
Sumatra 9.5Vo of 285 stool samples were found
positive with Taenia eggs (1972), in Papua, 9Yo of
170 stool samples (1973), in Bali 2.2%o of 548
samples (1977), again in Papua 2%o of 350 samples
(1979) and in Bali 7.2%o of 515 samples were
positive. Variations of prevalence depended on
examination methods and intensity of infections in
the community. Microscopic examinations of stool
samples could not differentiate between eggs of
soliam and eggs of T. saginata, therefore the
surveys did not reveal the exact prevalence ofeach
species. To establish proper strategies in
controlling the diseases caused by these tapeworms
more sensitive and specific diagnostic methods
were developed. Coker-Vann et al. [5] used a
serodiagnostic method (ELISA) for the detection
of antibodies against cysticerci of T. solium
several population groups in Indonesia. Ito et
[6,7] developed a highly specific and sensitiv6
method, using glycoprotein components of the
antigens for the diagnosis ofcysticercosis.
After the computed tomography (CT)-Scan or
magnetic resonance imaging was available for
evaluation of neurocysticercosis, could
diagnosed more often and more accurate, which
was the case in Bali [8,9].
Cysticercosis of the central nervous system
one of the major causes of neurological diseases in
many developing countries where cysticercosis is
endemic [10-12]. Although the majority of
Indonesian people are Muslim and do not eating
pork, some areas or islands of Indonesia have been
known to be contaminated with the pork tapeworm,
T. solium, where the most of local people are
Christian or Hindi [, 3, l3-15].
NCC caused by the larva of T. solium is now
highly endemic in Papua Province, Indonesia.
Many people with NCC simultaneously have
subcutaneous cysticerci nodules. Special effort in
controlling the disease in this province should be
given high priority in health programs.
Reports on taeniasis/cysticercosis, caused by 7.
solium in Indonesia will be discussed in this
document from the past to the present time. In
addition taeniasis, caused by T. saginata, which
Z. sometimes caused difficulties in the differential
diagnosis, will be reported.
2. History
Reports since long ago mentioned the prevalence
of T. saginata as well as T. solium. In 1867
Luchtmans reported on the finding of taeniasis
in among Dutch people in Malang, East Java. Dutch
al. people were fond of eating rare cooked beef; no
taeniasis was found in other people [16]. A report
in 1885 was on a case of taeniasis in an l8-month-
old baby, who was regularly fed with chopped beef
[17]. Another report by Hehewerth [18] mentioned
4 cases of taeniasis saginata without any
be specification on gender, age or origin of the
patients. Kroonenberg I7l reported 9 cases
suffering from taeniasis saginata (n=7) and
is taeniasis solium (n=2), whereas Grzyma [19,20]
detected a living proglottid in an infected appendix
U9-201. Muller [21] demonstrated a 4.5 m long Z.
 S. S. Margono et al.
saginata with scolex in 1935. In the year 1937 and
1939, 3 cases and one case were reported
respectively at the Eykman Institute in Jakarta [16].
Bonne [22] identified an adult T. solium from a
Chinese female living in Samarinda, East
Kalimantan. Lie et al. [23] reported also on a case
of a Chinese woman with cerebral cysticercosis in
Jakarta, showing neurological and psychiatric
symptoms. In the last patient, cysts found on the
cortical tissue of the frontal lobes and floating in
the cerebral spinal fluid, were surgically removed
and histopathologically diagnosed as cysts of Z.
solium.
3. Epidemiology
3.1. Papua (=former Irian faya)
Humans: For the first time T. solium infections
were detected in Enarotali, Paniai District by
Tumada et al. 124,251. Stool examination among
170 hospitalized patients revealed Taeniq eggs in
9o/o of the samples and in 6 (8%) among 74
ambulatory patients. Thirteen cases suffered from
neurocysticercosis with epileptic seizures and
several other symptoms [24,25]. All cases were
assumed infected with Z. solium, considering the
local people had only pigs. Only newcomers in this
area had a few cows.In 1978, Subianto et al. [26]
described cases of bums as results of epileptic
seizures associated with NCC. Before 1973 only a
few cases of bums were admitted to the hospital
Enarotali, Paniai District, whereas 1973-1976 the
number of cases of burns increased to 257. Based
on anamnesis of the family patients with epileptic
seizures felt into the fire used to warm them selves
during the cold night. Eighty-eight cases with
epileptic seizures were detected before or during
117
hospitalization among 121 cases with burns in the
age group over I I years. Most of them suffered
from severe bums (grades 3 and 4), whereas it was
found necessary that 17 among them should be
treated by amputation. Physical examination
revealed 33.1% individuals with subcutaneous
nodules and stool examinations found 16.60/o
positive for Taenia eggs and/or proglottids.
Autopsy of a patient who died due to burns,
revealed 20 cysticerci distributed in the two lobes
of the brain.
Margono et al. l27l conducted a survey on
intestinal parasites in Obano, a village in the
district of Paniai, Irian Jaya (Papua), with an
altitude of 1745-2100m above sea level.
Mountains are surrounding Obano except on the
southem side, which is bordered by Lake Paniai.
The survey revealed 2.0Yo of 350 stool samples
positive with Taenia eggs; males and females were
found infected for 3.0% and l.lYo, respectively, in
the age group of I l-50 years.
In Jayawijaya, during 1993-1995, a total of
3,632 cases with epileptic seizures were reported
from 20 local health centers. The number of death,
due to the disease was 14 during three years [28].
In 1996, the survey on secondary data was carried
out at the local health centre of Assologaima Sub-
District, Jayawijaya District. Assologaima Sub-
District is located northwest of Wamena, the
capital of Jayawijaya District. Review of disease
incidence in Assologaima during l99l-1995
revealed 293 new cases of epileptic seizures and
1,120 new cases of burns. Among 15,939
inhabitants the number of new cases with epileptic
in 1991, 1992, 1993,
seizures increased each year:
1994 and 1995 there were 4 cases, 41 cases, 68
cases, 35 cases and 145 cases, respectively. In the
118 Taeniasis and Cysticercosis in Indonesia

year 1995, epileptic seizures ranked 2od and burns [29]. Among 4l persons with suspected NCC, 12
ranked 9th as thecause of death t3l. with SCC and NCC, 18 with SCC, 16 with
Microscopically examination of extirpated cysts taeniasis and 68 PAR, 8 (l9.5lo/o),12 (100o/o), 10
from patients and a pig revealed that these were (55.55o/o), 6 (37.50%) and, 16 (23.52%) were
cysticerci of T. solium. DNA analysis of the cysts immunoblot positive by immunoblot [6],
showed that the nucleotide sequences of39l base- respectively (Tablel) 1291. Among 103 persons in
pair fragments of the mitochondrial cytochrome c the three villages, 46 of 65 (70.77oh) males
oxidase subunit 1 gene were exactly the same in suffered from seizures, whereas 6 of 38 females
those from patients and a pig. Although 3 of 391 (15.79%) were expected to have history of seizures.
base pairs might differ from those of T. solium Margono and her group reported on clinical
reported previously, there were no differences in symptoms and sero-positivity of persons from
the amino acid sequences [3]. Wamena Kota and Assologaima Sub-District,
A total of 96 local people, 18 years old or more Jayawijaya respectively. Among 82 persons, 4
from Assologaima, Jayawijaya District, and Papua with suspected SCC, 17 with suspected NCC, 5
were examined by serologic testing. The 96 people with suspected NCC plus SCC, and 19 PAR were
were divided into three on the basis of epileptic positive, whereas 3, 10, 4 and 20 individuals were
seizures (ES, n=17), physical examination of sub- negative respectively [4].
cutaneous nodule (SCN) by palpation (n:32), or Taeniasis/cysticercosis have been spreading
good health (including no ES or SCN; n=47). On from the west (Paniai) to the east (Jayawijaya) part
the basis of serologic results, 12 (70.6%) of 17,20 of Papua [1] and then to west (Manokwari) area
(62.5%) of 32, 12 (25.5%) of 47 of ES, SCN, and where 54 cases of NCC-suspected cases were
healthy group, respectively, were infected with the reported (Papua Province Health Office Services,
larval stage of T. solium. Serologically positive 1997, unpublished data). Papuan (Papua New
rates increased to 83.3yo (l0ll2) of people with Guinea, PNG) and Australian groups carried out a
subcutaneous nodules in the ES groups [15]. field health survey in Alice River Village, pNG
In the year 1998 a total of 155 cases from three along the border with the Papua Province of
villages in Jayawijaya was examined serologically , Indonesia in 1977. Tests done included serum
Table 1. Secondary epilepsy and other data on suspected antibody responses against Japanese encephalitis
taeniasis/cysticercosis in three villages of Jayawijay4 Papua.
and against T. solium cysticerci, considering some
Immunoblot of the Villagers were Irianese (Papua) refugees.
Cases Number
+ (%) - (o/o)
One very strong positive case of cysticercosis,
PAR 68 t6 (23.s2) s2(76.48)
three positive cases and, 12 weak positive cases by
Taeniasis l6 6 (37.50) r0 (62.50)
both immunoblot and ELISA in 541 human
Cyst 18 l0 (55.55) 8 (44.45\
Cyst+Seizures
samples (3.0%) were detected (Ito et. al.,
t2 r2 (r00.0) 0 (0.0)

4l unpublished data).
Seizures 8 (33.55) 33 (80.4e)

155 52 (le.5l) 103(66.45)

Source: Hamid et al. [29].
 S. S. Margono et al. 119

3.l.L Pigs According to the veterinary unit of 3.2.1. Humans The first known study of T. solium
Jayawijaya District, it has been reported that infection in pigs in Bali was by Le Coultre more
fifteen pigs with cysticercosis from nine villages than 70 years ago [31]. During traditional and
during August and September 1998. A serological religious festivities the people are consuming
survey in 11 villages from Jayawijaya revealed 17 lawar, a dish consisting of raw pork, vegetables
(8.5%) positive immunoblot in 201 pig samples as and spices, covered with fresh blood pork.
is shown in Table 2. Among 7l pigs of five Through consuming this dish, which sometimes
villages (Kimbim, Wesaput, Araboda, Piramid and was contaminated with cysts of T. solium, people
Woma) 2l were strong immunoblot positive, are infected with this tapeworm. Nowadays, lawar
whereas 7 moderate and23 weak positive [1a]. is sold at the market for general consumption.
Ngoerah [32] reported on 4 cases from Bali,
Table 2. Sero-positive immunoblot of 201 pig samples in
suspected to suffer from cysticercosis ofthe central
I I villages of Jayawijay4 Papua,
nervous system. Signs of mild meningitis, epileptic
No. Villages No. of lmmunoblot
serumles positive (%) Negative (%) seizures and cysts in subcutaneous tissue as well as

I Waona 25 s(20.0%) 20 (80.0%)

in muscles were present in one of the cases, a

2 Hubikosi 30 3 (10.0%) 27 (90.0o/o)

female.

3 Honelama 15 3 (20.0v0 12 (80.0%)

Stool samples/and or proglottids were examined
4 Wesaput 26 r (3.8%) 2s (96.20/0) from 3 villages in Bali: among 133 stool samples
5 Kurulu 34 3 (8.8%) 3r (91.2%) 1(0.8%) was positive for Taenia eggs in Trunyan,
6 Kama t2 2 (16.70/o) 10 (83.3%)
irmong 199 samples 4(2.1%) and among 216
7 Wamena 16 0 (0.0%) 16 (100%)
samples 7(3.3%) was positive in Sukawati and
8 Pasar Baru 5 0 (0.0%) 5 (100%)
Padangsambian (Denpasar), respectively t331.
9 Hom-hom 4 0 (0.0%) 4 (r00%)
Rasidi et al. [34,35] reported the findings of eggs
l0 Potikelek 21 0 (0.0%) 21 (t00o/o) and/or segments of Taenia in three other villages
II Holima 2l 0 (0.0olo) 13 (100%)
of Bali: in Mendoya l.1o/o of 143 samples, in
Total 201 17 (8.5%) 184 (91.5o/o)
Kututambahan 0.4o/o of 123 samples and in
Source: Subahar et al. [4]. . Bungaya l,loh of 88 samples were positive. They
found an egg-positive female, aged 60 years and 3
3.L2. Dogs Analysis of dog sera by both ELISA males, aged 9, 42 and 50 years old [34,35]. In
and immunoblot revealed that 7 of 64 dogs were another survey in Abiansial, near Denpasar, Bali
highly positive. Necropsy of two sero-positive detected 2.6% egg positive males and l.syo
dogs found cysticerci of T. solium in the brain and females in the age group of 0 to 69 years. The
heart [30]. Another dog strongly suspected by highest prevalence was found in the age group of 0
ELISA and immunoblot was killed and found to be to 9 years (3.7yo), whereas the lowest in the age
full of cysts at least in the brain, heat and muscle. group of 10 to l9 years (0.8%) [36].
The next survey in Bali found 4 (1.0%) egg
3.2. Bali positive samples among 354 samples: 1.0% in
120 Taeniasis and Cysticercosis in Indonesia
Jembran4 0.4% in Buleleng and 1.0% in
Karangasem. Among the 4 cases one was a female,
60 years old and the other 3 cases were males, each
9,42 and 50 years old.
Two percent of 2,538 individuals of Abiansemal
District, about 12 km north of Denpasar, the
capital of Bali Province reported that they were
expelling segments of worms [36]. Another report
from the Tabanan District mentioned treatment of
taeniasis in 17 patients in December 1984,
followed by 12, 24 and, 36 patients in January,
February and March 1985 respectively by the
Health Office Services at Tabanan [37].
Sutisna et al. [38] studied prevalence rates of
taeniasis and cysticercosis in Banjar Pamesan,
Ketewel Village, Gianyar District of Gianyar,
about 7 km east of Denpasar and is near the coast.
This banjar (group of people belonging to a unit
based on the geographyoftheir houses and certain
traditional habits) consisted of 765 people.
Systematic random sampling was used from the
community, aged 1 year or more. Stool samples
were examined by the direct microscopic
technique and copro-antigen test. Serum samples
were obtained from persons 6 years old or older,
and prevalence of cysticercosis was determined by
the westem immunoblot
Copro-antigen tests were positive in 2 among 156
stool samples, therefore the prevalence of taeniasis
was l.3olo. Both cases were patients suffering from
taeniasis saginata. Six cases (5.2o/o) of the 115
serum samples were positive against antigen
cysticercus T. solium, consisted of 3 males and
females, aged between26-46 years [38].
3.2.2. Animals Reports on the distribution of
cysticercosis in cattle and pigs in the world,
including Indonesia are scarce. In general, data on
cysticercosis in animals were based on meat
inspection according to the local situation,
superficially or no attention at all, so that cases
were misdiagnosed and in general cases were
under-reported [39]. In the year 1977, a report of
the Directorate Animal Health, Directorate General
Stock-breeding, Department of Agriculture
mentioned the prevalences of cysticercosis in cows
in 4 districts of Bali, Badung, Gianyar, Klungkung
and Tabanan as follows: 3.3, 16.9, 1.2 and 8.3Vo,
respectively. In the same year in 2 districts of Bali,
Badung and Klungkung the prevalence of
cysticercosis in pigs was 2.1 and l0.5yo
respectively [37]. In the year 1989 the Stock-
is breeding Service Unit Denpasar, Bali reported on
cysticercosis of cows, buffaloes and pigs in Bali
during the years 1975-1988 (Table 3). On the other
hand, cyst positive findings were found in cows
only during the years 1977,1978,1979, 1980 and
1988 i.e. among 32,192, 33,842, 31,586, 35,288
and 34,887 cows 100, 102,476,844 and 674 were
positive, respectively (data not shown). In
buffaloes only during the years 1979 and 1980
121476 and, 21844 were found to be cyst positive.
During the years 1975 till1986 cysts were detected
; in pigs, whereas all pigs slaughtered in 1987 and
1988 were cyst negative (data not shown).
Host-parasite relationship of T. saginata in Bali
was studied by infecting two cows, each with 30
human-derived proglottids of T. saginata. The
of adult worm obtained from feces of a patient were
3 cleaned with pipe water and taken to the laboratory
for identification with pressing gravid proglottids
between two object glasses and counting the
uterine branches. The two female cows, 5 months
old, were negative for Taenia. Gravid proglottids
 S. S. Margono et al. t21

Table 3. Cysticercosis in pigs in Bali during the experiment was also shown that T. saginata are
years 1975-1988.
still found in people in Bali during recent time.
Year Number examined Number positive
t975 20,148 59
3.3. North Sumatra
r976 40,t36 201
In 1972, Kosin et al la2l reported for the first time
t977 31,706 86
on the prevalence of taeniasis among inhabitants of
1978 30,988 181
Ambarita, Samosir Island, North Sumatra. During
1979 31,187 305
this survey 9.5Vo of 285 individuals reported that
1980 15,356 90
they had expelled segments of tapeworms,
l98l 49,126 60
diagnosed as resembling T. saginata, after they
r982 69,054 69
were recovered after treatment. A survey on 154
l 983 t06,442 4t
school children found 1.3% stool samples positive
1984 122,802 23
withTaenia eggs,2 boys each aged 8 and I I years.
1985 157,585 9l
Afterwards several surveys found prevalences
1986 75,932 2
between 2-21% 142-441. One of the reasons of
t987 t48,207
variations of prevalences was possibly due to
1988 t49,lt2 different examination methods. Morphologically,
Source of data: Veterinary Health Unit, Denpasar, Bali
the adult worrn was a Taenia sp. resembling Z.

were mixed with physiological saline solution and
administered orally to both cows. Cow 1 and cow
2 were slaughtered and examined for the presence
of Cysticercus bovis, respectively, six and eight
weeks post infection. Cysticerci were found in the
of cow 1,
masseter muscle and the caudal femur
whereas in cow 2 an abundant number of cysts
were widely distributed in almost all skeletal
muscles, namely in muscles of the cheeli,
intercostals muscles, diaphragma, heart and
muscles of thighs.
In each slice of the muscles the number of cysts
found were 3 to 5. The cysticerci in cow I were
less developed (size about 3 mm x 2 mm) in
comparison with those found in cow 2 (size about
4 mm x 3 mm). Therefore, it was found that at
least the optimal development time of cysticerci
was eight weeks after infection [40]. With this
saginata Goeze, 1782 with cows as the
intermediate host. A ft er analy zing morphological ly
the worms were identified as Z. asiatica. (see
Addendum [64]). Cysts of T. asiatica are found in
livers of pigs [41].
Depary [45] obtained 9 adult worms from 6
patients, who were treated with atebrine 800-1,000
mg. In three patients one worm was recovered,
whereas from the other three patients two worms
were obtained from each of them. The lengths of
the nine worrns were 250-550 cm. The number of
proglottids of 5 worms, with a length of 550 cm, of
550 cm,520cm,480cm and 350 cm were 721,716,
693, 648, and 517, respectively. Seven scolices
were found among the nine worns. The adult
worrns were identified as Z. asiatica.
3.4. Other provinces
r22 Taeniasis and Cysticercosis in Indonesia
3.4.1. Humans Surveys in resettlement areas of
Balinese people such as Seputih Raman, District
Central Lampung District, Lampung and Werdhi
Agung, Bolaang Mongondow District, North
Sulawesi revealed stool samples positive with eggs
and/or segments of Taenia, i.e. 51476 (1.1%) and
11245 (0.4%), respectively, whereas in Kendari,
South-East Sulawesi 11243 (0.4%) was positive. In
Lampung two females and 3 males, 15-60 years
old were found positive, whereas in North
Sulawesi and South-East Sulawesi one egg
positive male, aged 58 years and one female, aged
30 years were found respectively I35,461.
Cases with taeniasis and or/cysticercosis were
also reported from other areas of Indonesia. In
Jakarta, Hadidjaja [9] described l6 cases of
taeniasis of which 7 cases were infected with Z
saginata and 6 cases with Z. soliurn. Diagnosis
could not be established in 3 cases. The cases were
from Bali, North Sumatra, Manado (North
Sulawesi) and Jaknta. Hadidjaja et al. t20)
reported on multiple nodules detected in a Chinese
woman, 23 years old, in the face, neck, hands and
thighs. The patient complained of headache,
nausea, paraesthesia ofthe face and fainting spells.
The diagnosis was microscopically confirmed as
cysticercosis T. solium after excision of several
nodules. A microscopically study in Surabayq
East Java discussed nine cases of cysticercosis
concerning religion, sex, age and size of cysts
found during 1960-1977.
Four specimens were from Buddhist patients,
three from Christians and two from Hindus. Seven
patients were Chinese descendents, whereas two of
them were patients from the island of Bali. Four of
the specimens were from patients between 2l-30
years old, whereas three were from patients aged
between 3l-40 years. The size was 0.6 to 1.1 cm,
average 0.85 cm [47].
3.4.2.Animals At a slaughterhouse in Surabaya,
East Java Province, during the first four months of
1980 thirty-two among 16,863 (0J9%) cows were
detected with cysticerci. Among 17,114 pigs
slaughtered in Surabaya 27 (0.160/o) were positive;
all the pigs were from Bali. Also 61 buffaloes were
slaughtered, however all the buffaloes were
negative. In January and February 1980 pigs from
Bali were also slaughtered in West Jakarta and 5
among 22,832 pigs (0.02%) were positive with
cysticercosis [37]. At that time most pigs and also
cows slaughtered in Jakarta were sent from Bali,
whereas at present cattle and pigs are from West
Java and Central Java.
4. Socio-culturalaspect
The impact of education was studied among 155
inhabitants in the Abiansemal District, Bali: the 52
cases with taeniasis were illiterates or had only a
primary school education. None of the high school
educated people were infected with Taenia. During
the survey it was found that only 9 among 38
families (23.7%) had a latrine. Most of the families
used the teb4 a space behind the house, used for
rearing pigs, fordefecation. Other families
considered the river as their latrine. Due to the hot,
tropical climate, people like to defecate in the open
nature without a shelter [36].
Data on socio-ecology and symptoms, collected
through questionnaires, in
Banjar Pamesan,
Ketewel Village, Gianyar District, Bali revealed
that among 104 respondents age 12 years or older,
56 (53,8yo) had no formal school education or did
 S. S. Margono et al.
not finish the primary school, 18 (17.3%) did
finish the primary school, 8 (7.7%) finished the
junior high school and 22 (21.2%) finished the
senior high school [38]. Of the respondents 77
(74.1%) had sanitary facilities, 25 (24.0%)
defecated in the river and,2 (1.9Yo) were using the
teba or scrubs as their toilet.
Characteristics of 67 respondents, head of
households were as follows: 13 (19.4%) had none
sanitary facilities, whereas 54 (80.6%) confessed
that they owned toilets. All the pig owners (af of
a total of 67 respondents (70.1%) were having pigs
in husbandry and all the cattle owners (7110.4o/o)
kept their cattle in stables.
In Assologaima, Papua" 3l questionnaires were
distributed to respondents on identity and eating
habits. It was found that 83.9% were illiterate,
93.6% were farmers, all were Christians and all
used to eat pork roasted on batu pancs, hot stones.
On behavior and environmental hygiene: 90.3%
obtain water from the river and was consumed
without boiling, 64.5% did not wash their hands
before eating, 58.1% did not wash their hands after
defecating, whereas 6450A defecated in
bushes/forest and there were no sanitation facilities
atall. By observation in the field, actually it was
suspected that higher percentages in unhygieni6
behavior were present than they admitted [28].
A study, based on questionnaires and laboratory
findings was conducted in the village of Kama,
Papua in 13 silimo's, units of huts, inhabited by
extended families. Questionnaires were distributed
to 75 respondents. Among the respondents, aged
14 years and older, 80.0% were farmers,6.7%ohad
an office job and 133% had no job, including
respondents who were still at school. A high
123
illiteracy of 6l.3Vo was found and only 9.7o/omales
have ever attended the senior high school.
The source of drinking water and the use of
water for daily use are important indicators for
socio-economic conditions, which are basic in the
perpetuation ofthe disease. A very high percentage
(92.1o/o) of the respondents were using open wells
as a source for drinking water; for the rest drinking
water sources were the river and the rain. Although
70.7o/o admitted that they took a bath once daily,
25.3 and 4.0%o took a bath once weekly and once
monthly respectively, it should be known that
almost no sanitary facilities exist and the few
toilets of houses in main roads, built financed by
the government were not being used by the local
people.
The respondents (95.0%) were defecating in
garden or bushes, in the river (2.7%) and in the
garden/river (1.3%). As was reported by
Simanjuntak et al. [1], infection may be due to the
habit of the people to consume sweet potatoes,
directly after harvesting the potatoes. Sometimes
without washing hands, without washing the
potatoes, the potatoes are consumed raw. At this
time transmission occur considering the possibility
of soil contamination with T. solium eggs, €ls
people are defecating promiscuously on the soil.
Although the transmission of cysticercosis is
considered mainly by eggs in the soil to man, eggs
of T. solium on parts ofthe body, such as around
the anus, on the hands, beneath the nails can cause
autoinfection or hetero-infection to other people.
Swasono and her group [48] identified four
main factors causing people at risk towards
diseases in the area of Kurulu, Papua. There is a
relationship between cultural behavior (adat) and
diseases i.e. the practice of traditional customs
124 Taeniasis and Cysticercosis in Indonesia

(adat), dwelling patterns and interactions within
the dwelling place, contact of man to man and man
to animal. Christians were spreading the religion in
this region using different strategies.
5. Diagnosis
hyalinized fibrous tissue with a minimum amount
of mononuclear infiltrate was observed. There was
a distinct inner lining of flattened endothelium.
The tissue reaction consisted of epitheloid cells,
some showing mitosis and giant cell formation.
The second layer consisted of foamy cells, plasma
cells, lymphocytes and eosinophils, whereas

5. 1. Parasitic diagnosis fibrous connective tissue formed the outer layer

In Bali the whole adult worms or segments t47l
obtained after treatment were identified after using Fan (1991) reported on comparative
the WHO criteria described by Gemmell and morphological studies of T. saginata asiatica. Six
others [38,49]. L-SEM pigs became infected 6l-195 days after
In Papua an abundant number of cysticercus cysts each was feed with 30,000 T. saginata asiatica
were found at autopsy on the surface and in the eggs from Indonesia. The recovered cysticerci
brains of a 35 years old male, who suffered form from the livers were mostly degenerated or
epileptic seizures. It wts microscopically calcified (99.9%). However, in 3 SEM pigs 78%o
diagnosed as cysticercus cellulosae of T. soliurn of the cysticerci were mature and only 22oh were
[50]. Recently, in a woman from Bali, suffering degenerated or calcified 45-76 days after feeding
from skin and brain cysticercosis, several nodules each 3,000 eggs. The diameter of the protoscolex
were excised from the forehead, near the right side was 566 pm and the cysticercus had two rows of
of the lips, temporal side of the face, neck and hooklets. The hooklets of the outer row were
shoulders, measuring 1.5 to 2 cm. The specimens numerous. The mean (and range) of the number
consisting of skin tissue, striated muscle and and the length of the inner-row hooklets were 2 (1-
connective tissue, which were infiltrated by 40) and ll pm (3-20 pm), respectively [52].
chronic inflammatory cells and a few
multinucleated giant cells. Cystic structures with 5.2. Stool Samples
thick collageneous walls with inside the cysts'a Besides the conventional stool examinations, such
scolex with hooklets, suckers and spiral canals was as the direct smear, the concentration technique of
observed, which was diagnosed as cysticercus Z. Ritchie and Kato-Katz smear technique, copro-
solium f5l). antigen tests were used for detecting antigens shed
The microscopical study in Surabaya, East Java by adult Taenia worTns and found in stools of
covered an evaluation of 9 positive specimens taeniasis patients. This method was described by
among 80,000 examined tissue specimens. The Allan et al. [53], and later reported again by the
cysts, measuring between 0.6 and l.l cm, were group of Sutisna [38]. The method was used for
spherical in shape. Microscopically, the scolex surveys in Bali during the last ten years.
showed head with suckers and a rostellum with Copro-antigen tests were used for 33 stool
hooklets. A distinct bladder wall, consisting of samples collected in the village of Kama,

Jayawijaya, Papua. Among them, 5 (l5.2Vo) were
found positive and after drug administration
adult L solium were expelled.
5. 3. S ero lo g ical examin ations
It is important to establish reliable
methods for cysticercosis in humans and pigs for
the surveillance, control and prevention of
taeniasis and cysticercosis. Several serological
methods have also been used for surveys in
Indonesia [30,54].
Immunodiagnosis of cysticercosis
conducted using several methods including gel
precipitation, complement fixation, indirect
hemagglutination, indirect immunofluorescence,
and counter- and immuno-electrophoresis tests
tssl.
The ELISA was implemented by Diwan and
others [56] and Coker-Vann and others [5] using a
pork muscle antigen control for the cysticercus test
antigen, which somewhat improved the serological
distinction between infected and uninfected
subjects. The examined serum samples were from
3l symptomatic, hospitalized patients with
cysticercosis in Enarotali, Paniai District, Irian
Jaya (Papua), collected in 1974 and 1977. Serum
antibody to cysticercus was detected in 61% o?the
patients, with higher rates when subcutaneous
were present than with NCC alone. The combined
l:770. This test
Geometric mean titer (GMT) was
showed cross-reactivity with some patients
suffering from schistosomiasis, echinococcosis and
possibly angiostrongyliasis, diseases not known
existing in humans in Papua. With the
ELISA, of clinical and typical NCC patients
79o/o
from Mexico were found positive with serum
antibody to cysticercus. The patients from Mexico
S. S. Margono et al. 125
previously showed titers of >1:8 with spinal fluid
5 complement-fixation test [56]. Among another 120
samples from the asymptomatic general population
of Obano, a village in the endemic area of the
Wissel Lakes, l6olo was seropositive. Negative
serological results were found in 345 residents of 3 villages
adjacent to the endemic region, east of the Wissel
Lakes. Only 2 samples were positive in Asmat
urmong 301 residents of 6 villages in the Asmat and
Citak communities in the southem lowlands and of
4 villages of the Mek group in the Eipomek Valley
has been of the central highlands [5]. It was suggested that
positive samples outside endemic areas might have
become infected during travel to endemic areas or
might be due to antigen other than cysticerci of Z.
solium such as Echinococcus and Schistosoma.
This ELISA technique had a heterogeneous
nature of cystic antigens [56]. Coker-Vann and
others t5l found also ELISA antibodies to
cysticerci of T. solium in sera samples from three
other islands of Indonesia: Samosir (3/106), Nias
(8/191) and Bali (11/53), which is 3o/o, 4%o, and
2lo/o, respectively. At that time, the highest sero-
positive prevalence rate was found in Tenganan, a
village in Bali, an area known to be endemic for
taeniasis/cysticercosis.
Further studies with serodiagnostic techniques
in Bali used by Coker-Van and others [5] seemed
relatively to be not so sensitive and specific.
During the study in the village of Ketewel, District
Gianyar Bali, serum samples were frozen in -20
oC
using the immunoblot technique, described by
Rodrigues-Canul and others [58], before examined
same by Sutisna et al. [38] in the Bioscience Research
Institute, Salford University, United Kingdom.
Antigen extract of metacestodes Z. solium was
prepared by homogenization process with PBS
solution, pH 7.2, followed by centrifuging at
14,000 x g for 60 minutes at temperature of 4oC.
The antigen extract was run on sodium dodecyl
sulfate polyacrylamide gel electrophoresis (SDS-
PAGE, gel\ and transferred to a cellulose
12o/o
membrane. The membranes were cut in small
strips and mixed with the serum of the sample
during t hour. The serum sample was diluted into
l:100 in phosphate-buffered saline (PBS)
containing Tween 20 and a 5olo solution of skim
milk. After washing, the cellulose strip was
incubated in
anti-human immunoglobulin G
conjugated with horseradish peroxide during I
hour, in a buffer substrate of 3,3-diaminobenzidine.
The emergence of one or more antigens at 8-kDa
and/or 28-kDa band showed the presence of
antibodies against cysticercus T. solium with a
sensitivity of 100% [58]. Recently, in Papu4
serum samples were examined using antigen of Z.
solium cysticerci fractioned by a single step
isoelectric focusing. Using immunoblot and
ELISA techniques, glycoprotein (GP) components
of the antigen showed to be highly specific and
sensitive for the diagnosis of cysticercosis [6].
The purification is basically a single step and the
purity of the GPs is different from lectin affinity
purified GPs [59]. The examination methods #erg
also used for human as well as for pig and dog
serum samples. In the village of Kama, 37/65
(56.9%) human, 12/13 (92.3%) pig and 5fi2
(41.7%) dog samples were positive by immunoblot.
Seropositive human serum surmples were found in
four other villages: Piramid 9ll7 (52.9%), Woma
18132 (56.3yo), Kimbim l4l2t (66.7%) and
Araboda 9116 (56.3%). These data showed the
highest sero-positive prevalences in humans
against T. solium antigen compared to other parts
of the world.
Ito and others showed that serological
t6]
methods such as immunoblot and ELISA using
new GP antigen were also useful for the detection
of cysticercosis in pigs compared with human
cysticercosis. ln 1999, a total of 8 serum samples
from pigs, including one from Indonesi4 harboring
multiple cysticerci, showed similar antibody
responses with ELISA compared with human
cysticercosis [7]. The ELISA optical density (OD)
values were between 0.567 and 2.500 (maximum
OD), compared with OD for 4 uninfected pigs with
values between 0.014 and 0.076. The cut-off value
in human cysticercosis was 0.150 [6].
6. Treatment
Westhoff [l7] treated a child of 8- months with
good result, suffering from taeniasis saginat4 with
lz g of extract of Filicis maris. A report mentioned
that in several regions of Indonesia seeds of
Cucurbita maschata,locally known as labu meralt,
were used for treating taeniasis 1601. No
information was available on the active component
of the seeds. Also it was not known if all varieties
of the seeds were effective for tapeworms. The
seeds were administered before breakfast and
about 3 hours later a laxative such as a solution of
magnesium sulfate was given. Van Veen and
Colliers [60] concentrated 60-100 g of the seeds
into 5-10 g dry material, which was solved and
emulsified in 50-100 cc boiled water before used
for treatment. Seeds of Semen cucurbitae were
used in the community in a dose of 180 g
 S. S. Margono et al.
containing about 1,000 seeds, according to a recipe
of Vermande cited by Hadidjaja [19].
Oleum chenopodii was a common drug used for
several intestinal worm infections. A European
patient, sufTering since eight years from taeniasis
solium was treated by this drug in a dose of 2 cc
during two months, which resulted in the expulsion
of a number of proglottids, however without a
scolex [61]. Afterwards the patient died after five
days after taking the whole bottle of 10 cc oleum
chenopodii, which should be used for several
courses. One day after taken the drug, he had
heavy headache and was deaf. On the second day,
he did not recognize the nurses and had then
hallucinations. Three days after the intake of the l0
cc oleum chenopodii, he suffered from muscular
spasms and the temperature increased till 39.6oC.
He was comatose the day before his death.
Another drug used for taeniasis was atebrine
(quinaquine hydrochloride), which was given in a
single dose, 15 mg per kg/body weight and the
highest dose was I g. The cure rate was 85% [19].
The adult worns, yellow colored by the drug were
expelled as a whole with or without a scolex. In a
Chinese woman multiple subcutaneous cysts were
excised for cosmetic reasons [20].
Kosin and others [41] treated taeniasis in North'
Sumatra with bithionol (2,2, thio, 4,6,
dichlorophenol), l0 tablets (2.0 g), single dose, in
65 patients. On the same day, 23 patients expelled
wofins, whereas the others were expelling the
worTns during the next day. Bithionol was also
used in Bali, single dose, and 20 g per kg/body
weight, which was increased to 40 mg per kg/body
weight. The result was a cure rate of 90.3%o.
In the year 1987, Koesharjono and others [62]
treated 24 patients in Simanindo, North Tapanuli,
127
North Sumatra and 54 cases in Badung, Bali with
praziquantel. In Sumatra the cure rate was 8750%
(21 cases), whereas in Bali 70.37% (38 cases).
Side effects were found in 1 patient from North
Sumatr4 who complained of headache and was
feeling weak. Six persons from Bali had headache
and nausea" whereas 4 persons complained of
headache only. Side effects disappeared quickly.
Sutisna et al. [38] treated patients, with copro-
antigen positive results or/and with
eggs/proglottids in their stool, with 2 g of
niclosamide, followed by magnesium sulfate
solution as a laxative. The total fecal mass was
collected during 48 hours to search for adult
worrns and its segments. However this drug is
difficult to obtain on the market.
Praziquantel (biltricide) is the most recent drug,
which is effective in treating taeniasis. During
hospitalization, a female from Bali, detected in
Jakarta, suffering from multiple cysts of T. solium
in skin and brain, was given symptomatic
treatment for her headache and seizures with
methampyrone, 3 times a day and phenytoin, 3
times a day. Intra-muscular injection with
dexamethasone was given at the same time, 3
times a day, tapering to one ampulla. A single dose
of 1,050 mg praziquantel (20 mg per kg body
weight), followed by purging with 30 g of
magnesium sulphate solution was administered for
intestinal taeniasis. Two days later, 800 mg
albendazole, as a single dose was given during l0
days for the multiple cysts. At the same time, a
single dose of methyl prednisolone 750 mg was
injected intravenously. Later on carbamazepine,
one tablet b.i.d. was given daily.
Hamid et al. I29l treated 72 individuals
diagnosed as suspected NCC with albendazole or
128 Taeniasis and Cysticercosis in Indonesia

were treated with

praziquantel. Thirty-five
albendazole and 37 cases with praziquantel,
however treatment with albendazole was not
completed in 3 cases and in 7 praziqtantel
due to side effects. After one year, only 9 among
the 32 cases treated with albendazole and l0
among 30 praziquantel cases could be followed up.
The diagnosis was determined as suspected NCC
by history of illness, physical and neurological
well as serological examinations by immunoblot
schedule. Patients without any symptoms of
taeniasis/cysticercosisA.,lCC were given vitamins
and symptomatic treatment such as antipyretics,
cases antacids and antibiotics, or treatment for other
diseases. Praziquantel 600 mg (2 tablets), once a
day for one day was administered to suspected
taeniasis patients, followed by a laxative of 30-60
g magnesium sulfate as a suspension after 2 hours.
as In the case of cysticercosis, albendazole, 400 mg, 3
tablets once daily for l0 days was the drug given

described by Ito et al. [7]. to the patient, whereas in NCC besides the

No electroencephalogram (EEG) or schedule used for cysticercosis, predonison 5 mg, 4

neuroimaging could be done in patients in this area. tablets, once daily was used for 5 days and dilantin
Sero-positivity was found among the 9 cases 100 mg, 2 capsules once a day for 10 days. The
treated with albendazole (Tables 4 and 5) [291. local health providers adopted the standard
Dharmawan [40] obtained proglottids from Z. schedule.

saginata for his experimental infection in 2 cows, It appea$ that only the present drugs,
by treating a patient, 65 years old with 2 g of albendazole and praziquantel are useful in treating
niclosamide. A solution of magnesium sulfate, a taeniasis as well as cysticercosis. During the last
dose of 30 g, was given two and a half hours after years praziquantel is used in cysticercosis and
the administration of niclosamide. NCC, considering the practical, single dose. If not
Since the year 2000, during our surveys in available, albendazole should be used for eight
Jayawijaya District, patients visiting the health days or longer for cysticercosis and NCC.
units or in the field were treated with a standard Albendazole is easier to find on the market, as it is

Table 4. Results of therapy with albendazole before and after one year in patients of Jayawtjaya Papua.

No. ,-1g:^.
Sex (Years) ",.Hl'""r"
Srffi ffi inyears

IM l8-+
2M32 3+8
3M39+
4M48
5M 30
+
+
-+3+
-+2+
-+3+
+
.l':'l I
6M +2
7M 2+6
8M60+- -+ I
9M28+- ++ 7

SZ, Seizure; Sn, Subcutaneous nodule; Hd, Headache; IB, immunoblot. Source: Hamid et al. [29].
 S. S. Margono et al. t29

Table 5. Results of therapy with praziquantel before and alter one year in patients of Jayawij aya, Papua.
Signs and symptoms Duration
Age
No. Sex
(years) Before therapy After therapy seizures
in years
Sz IB Sz Sn Hd IB
1M 54 + + 2+ 2+ 6

2F l9 + + 3+ 3+ 2

3M 40 + + 3+ 2+ 7

4M 48 + + 2+ + l8
5M 30 + + + J

6M 40 + Jf 4

7M 38 + + 5

8M 50 + + 2+ 12

9M 30 + + 3+ 3+ 7

10M50-++ + l0
SZ, Seizure; Sn, Subcutaneous nodule; Hd, Headache; IB, immunoblot

Source: Hamid et al. [29].

module did not significantly increase their

also used for soil-transmitted helminthiasis and it
is also cheaper.
7. Controlprogram
One of the most important aspects of
programs is health education, which was not much
given attention except possible in some extent in
Bali. Since around the 1970, information on
taeniasis/cysticercosis wurs given ,Bugh
knowledge.
The control program should be conducted
systematic and sustainable as to have an effective
impact on the community. However, because of
low priority, limited funds and manpower, control
control On this disease could not be maintained. Also,
checking school children for early detection, early
treatment should be part of the implementation of a
sustainable program.
An intemational collaboration project on an

broadcasting for years, however this topic is ?rt
present not available anymore. An effort to obtain
better results has been done in a control program.
Widjana [63] gave health education on the disease
in Pamesan, Ketewel, Sukawati, sub-district
Gianyar, using lectures, module or combination to
120 heads of households, with at least primary
school education.It was found that lectures were
the most effective way of increasing the
knowledge of the participants; adding the use of a
epidemiological study of taeniasis/cysticercosis in
Indonesia has been carried out in Jayawijaya
District, Papua since 1996. The first step consisted
of sero-epidemiological analysis of local persons,
followed by the second step, which is the detection
of pigs infected with Z. solium serologically.
During the third step, the copro-antigen test for
detection oftaeniasis worrn carriers was
introduced and DNA analysis was performed.
Eggs prepared from gravid segments were also
used for experimental infection in NOD-scld mice.
130 Taeniasis and Cysticercosis in Indonesia

The forth step was to check local dogs, since both intensive epidemiological studies are urgently
dogs and pigs are roaming free with access to needed, especially covering the eastern part of
human feces. In Papu4 community-based health Indonesia, to ensure a sustainable system for the
education was conducted through primary and control ofthe disease.
junior high schools. From 1996, several funds
from Japan were available through Gifu University 9. Addendum
and Asahikawa Medical College. WHO has funded
for training and education of local health workers A short but timely review on human taeniasis and
and school children in Wamena in 2001 and,2002. cysticercosis in Asia including the historical
Technical transfer has been carried out several findings of Taenia asiatica has just been published
times in Gifu University and Asahikawa Medical by Ito et al. [63]. Another monograph entitled pig
College, Japan. Furthermore, Asahikawa Medical husbandry in New Guinea: a literature review and
College has been supporting to establish the bibliography by Hide [64] has been published.
laboratory reference center in Indonesia. Indonesian work in Irian Jaya and other islands are
well referred.
8. Conclusions
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