taeniasis and cysticercosis in bali and north sumatra, indonesia
TRANSCRIPT
sevier.com/locate/parint
Parasitology International 5
Taeniasis and cysticercosis in Bali and North Sumatra, Indonesia
Toni Wandra a,g,*,1, A.A. Depary b, Putu Sutisna c, Sri S. Margono d, Thomas Suroso a,
Munehiro Okamoto e, Philip S. Craig f, Akira Ito g,1
a Directorate General, Communicable Disease Control and Environmental Health, Ministry of Health, Indonesiab Department of Parasitology, University of Sumatra Utara, North Sumatra, Indonesia
c Department of Parasitology, University of Udayana, Bali, Indonesiad Department Research and Community Service, University of Indonesia, Indonesia
e University of Tottori, Tottori, Japanf University of Salford, Greater Manchester, UKg Asahikawa Medical College, Asahikawa, Japan
Available online 20 December 2005
Abstract
It has been reported that three human Taenia species are distributed in Indonesia: Taenia solium, Taenia asiatica and Taenia saginata. T.
asiatica is well known in North Sumatra, especially on Samosir island in Lake Toba. T. solium and T. saginata are known from Bali. T. solium is
most serious public health issue in Papua (former Irian Jaya). In this report, we briefly review the present situation of these three human Taenia
species mainly in Bali and North Sumatra. For community based epidemiological survey, we have adopted and applied questionnaire, microscopic
observation of eggs, coproantigen tests, coproDNA tests, mitochondrial DNA analysis and morphology for isolated specimens, serology for
cysticercosis and taeniasis. For detection of taeniasis cases of both T. saginata and T. asiatica, questionnaire by expert doctors is perfect to detect
worm carriers. Corpoantigen test developed for detection of taeniasis of T. solium is also highly reliable to detect taeniasis carriers in the
community. Epidemiological data from these two islands 2002–2005 are reviewed with backgrounds of historical culture, religions and customs.
D 2005 Elsevier Ireland Ltd. All rights reserved.
Keywords: Taeniasis; Cysticercosis; Taenia saginata; Taenia solium; Taenia asiatica; Serology; Mitochondrial DNA; Corpoantigen; Copro-DNA; Bali; North
Sumatra; Indonesia
1. Introduction
In Indonesia, there are three endemic provinces for taeniasis/
cysticercosis: Bali, Papua (former Irian Jaya) and North
Sumatra. Data on taeniasis/cysticercosis from other provinces
are scarce or unavailable.
Taeniasis either due to Taenia saginata or T. solium was
distributed in all nine districts of Bali (see Fig. 1). Prevalence
rates were reported to ranged from 0.4% to 23% [1–5] (Widjana
et al., unpublished data; Bakta et al., unpublished data). The
current survey performed in three districts in southern part of
Bali indicates that T. saginata taeniasis has increased dramat-
ically in number of cases, while T. solium taeniasis and
1383-5769/$ - see front matter D 2005 Elsevier Ireland Ltd. All rights reserved.
doi:10.1016/j.parint.2005.11.024
* Corresponding author. Tel./fax: +62 21 4202856.
E-mail address: [email protected] (T. Wandra).1 Both authors contributed equally.
cysticercosis is now rather rare compared to 10–20 years ago.
There was no Taenia asiatica case in human found in Bali [6].
The present situation of cysticercosis in Papua appears to be
one of the worst in the world [8,9]. Epidemiological surveys in
2000 and 2001 in Jayawijaya District of Papua showed that
8.6% (5/58) local people, who were found taeniasis by
coproantigen test and later confirmed by mitochondrial DNA
analysis, harbored adult worm of T. solium, whereas 45.8% (44/
96) of people, 70.4% (50/71) of pigs, and 10.9% (7/64) of local
dogs were seropositives for cysticercosis by ELISA and
immunoblot with later molecular confirmation [8,10–12].
Taenia asiatica has been found in Samosir island in Lake
Toba, North Sumatra [9,13–15]. The prevalence rates of
taeniasis were reported to be ranged from 1.9% to 20.7%
[13,16,17,32]. Repeated epidemiological surveys in 2003 and
2005 on 240 local people revealed that 2.5% (6/240) to be
infected with T. asiatica (Wandra et al., unpublished data).
5 (2006) S155 – S160
www.el
Table 2
Summarized data of seroprevalence of cysticercosis in Bali, 1981–2005
Area surveyed
(year)
Population
sampled
Seroprevalence
rates (%)
Methods Reference
Bali 5.2 up to 21.0 [25]
Bali 927 5.3 (49/927) ELISA Breguet
and Ney,
unpublisheda
Bali 746 12.6 (94/746) Immunoblot [26]
Gianyar 115 5.2 (6/115) Immunoblot [27]
Gianyar
(2002)
125 0.8 (1/125) ELISA and
immunoblot
[6]
Gianyar
(2004)
46 0 (0/46) ELISA [6]
Badung 91 0.0 (0/91) ELISA [6]
Denpasar 49 0.0 (0/49) ELISA [6]
a Quoted from Ref. [3].
T. Wandra et al. / Parasitology International 55 (2006) S155–S160S156
This brief review summarizes epidemiological data of
taeniasis and cysticercosis from Bali and Samosir islands
2002–2005 with backgrounds of historical culture, religions
and customs.
2. Taeniasis and cysticercosis in Bali
2.1. T. solium cysticercosis
Bali, one of the 32 provinces of Indonesia consisting of 9
districts, has an area of 5561 km2. According to National
Socio-Economic Survey (2003), Bali’s population has grown to
over 3 millions, with population density of 585 people per km2.
The majority of the population of Bali Island is Hindu (93.4%).
Most people live in the south, and the capital city of this
province is Denpasar with a population of over 370,000.
The first report of T. solium infection in pigs in Bali was
published more than 75 yeas ago [18]. Thereafter there are two
human cases of subcutaneous cysticercosis (SCC) found in
Bali. They were a Balinese woman and a Chinese woman [19].
Summarized data on T. solium taeniasis, epileptic seizures,
SCC, neurocysticercosis (NCC) and seroprevalence of cysti-
cercosis in Bali 1960–2005 are shown in Tables 1 and 2.
During 1977–1993, a total of six tapeworm carriers of T.
solium taeniasis were detected [1,3,20] (Bakta et al., unpub-
lished data) (Table 1). Epileptic seizures cases in the
community ranged from 1.1–8.0% in three districts of Bali
(Badung: 03 in Fig. 1, Gianyar: 04 in Fig. 1, and Bangli: 06 in
Fig. 1) [1], whereas from hospitals 68 and 368 new cases in
1980 and 1984 (Wangaya Hospital, Denpasar), and 74 cases in
1991 within 3 months (Sanglah Hospital, Denpasar) were
reported, respectively [20,21]. Margono and others [22]
reported that 10 of 74 (13.5%) patients with epileptic histories
in Bali were diagnosed to be due to NCC based on ELISA.
Both SCC and NCC were found in Bali during 1960–2003
Table 1
Summarized data of T. solium taeniasis, epileptic seizures, subcutaneous cysticercosis (SCC) and neurocysticercosis (NCC) in Bali, 1960–2003
Area surveyed/hospital (year) Symptom/diagnosed No. of case/% Reference
Bali T. solium taeniasis 2 cases [1]
Denpasar T. solium taeniasis 1 case Bakta et al., unpublisheda
Renon, Denpasar T. solium taeniasis 1 case [3]
Denpasar (1991–1993) T. solium taeniasis (with nodul SC) 2 cases [20]
Trunyan, Bangli District Epileptic seizures 8% [1]
Sukawati, Gianyar District Epileptic seizures 3% [1]
Padangsambian, Badung District Epileptic seizures 1.1% [1]
Wangaya Hospital, Denpasar (1980) Epileptic seizures 68 new cases [21]
Wangaya Hospital, Denpasar (1984) Epileptic seizures 368 new cases [21]
Sanglah Hospital, Denpasar (1991, within 3 month) Epileptic seizures 74 cases [20]
Bali SCC 2 cases [19]
Bali (found in Jakarta) SCC 4 cases [23]
Udayana University, Bali SCC 6 cases Susanti, unpublishedb
Wangaya Hospital, Denpasar NCC 4 cases [24]
Denpasar (1991–1993) NCC 3 cases [20]
NCC (with nodul SC) 1 case [20]
Sanglah Hospital, Denpasar (1995–1997) NCC 25 cases Sudewi and Nuartha, unpublished
Sanglah Hospital, Denpasar (2003) NCC 1 case Sudewi et al., unpublishedc
a Quoted from Ref. [3].b Quoted from Ref. [21].c Quoted from Ref. [5].
[19,20,23,24] (Susanti, unpublished data; Sudewi and Nuartha,
unpublished data; Sudewi et al., unpublished data) (Table 1).
Seroprevalence of cysticercosis in humans in Bali was ranged
from 5.2% up to 21% since more than 20 years ago [25–27]
(Breguet and Ney, unpublished data) (Table 2).
The current survey in 2002–2004, from 398 population
sampled in three villages in three districts of southern part of Bali
(Gianyar: 04 in Fig. 1, Badung: 03 in Fig. 1, and Denpasar: 01 in
Fig. 1), there were no individuals with indication of T. solium
cysticercosis including history of epileptic seizures, presence of
subcutaneous nodules, except one seropositive in Ketewel
village, Gianyar District in 2002. In this village, serological
examination of 125 serum samples revealed that 0.8% (1/125) of
sera was seropositive [6] (Table 2).
The significant decrease in infection of T. solium in Bali is
probably due to improvement in sanitation and pig husbandry
at least in the surveyed areas. In these districts, 56 tapeworm
carriers detected during 2002–2004 and 192 people of 192
c
1000km
N
Bali
01
02
03
04
05
06
07
0809
Fig. 1. Geographic maps of Indonesia (upper) and Bali (lower). There are 9 districts in Bali. They are Denpasar (01), Tabanan (02), Badung (03), Gianyar (04),
Klungkung (05), Bangli (06), Karang Asem (07), Buleleng (08), and Jembrana (09) Districts. Denpasar is the capital city of Bali Province.
T. Wandra et al. / Parasitology International 55 (2006) S155–S160 S157
families interviewed said that none of them defecated in the
backyard (teba). Almost all families (96.9%) had sanitary
facilities. All pig owners (56 of 192 families) kept their pigs
indoors [6]. By contrast, only 64.1% of families had sanitary
facilities, while 42.4% of taeniasis carriers and 12.6% of
families defecated in the backyard, and pigs were allowed to
roam free in 1990 [3,28].
2.2. T. saginata taeniasis
Taeniasis (either due to T. saginata or T. solium) was
distributed in all nine districts of Bali island. Summarized
data of taeniasis in the island are shown in Table 3. During
1977–1999 prevalence rates of taeniasis were reported to be
ranged from 0.4% to 23% [1–5] (Widjana et al., unpub-
lished data; Bakta et al., unpublished data). In three villages
in three districts (Gianyar, Badung and Denpasar Districts)
of Bali in 2002 and 2004, a total prevalence of 14.1% (56/
398) T. saginata taeniasis was detected to be ranged from
1.1% to 27.5%. The prevalence rates had increased
dramatically in Ketewel village, Gianyar District in 2002
(26.5%, 32/125) and in 2004 (27.5%, 14/51) [6] compared
with previously surveys in 1977 (2.1%, 4/189) [1] and 1999
(1.3%, 2/156) [5].
A total of 60 persons among 398 local people in these areas
were suspected to be taeniasis by anamnesis (questionnaire
method) and 56 taeniasis cases were confirmed after treatment
with praziquantel. The history of expulsion of proglottids from
four suspected persons was that they expelled proglottids 1 or 2
years before, and fecal samples from these four persons were
negatives by direct smears. A total of 82 fecal samples were
available for coproantigen, included seven (8.54%) coproanti-
gen positives (but negatives by direct smear) and four direct
smear positives (were not applied to re-confirmation by
Table 3
Summarized data of taeniasis by districta in Bali, 1977–2005
District Area surveyed
(year)
Population
sampled
Prevalence
rates (%)
Reference
Gianyar Sukawati 189 2.1 (4/189) [1]
Sukawati (1999) 156 1.3 (2/156) [5]
Sukawati (2002) 125 25.6 (32/125) [6]
Sukawati (2004) 51 27.5 (14/51) [6]
Badung Padangsambian 216 3.3 (7/216) [1]
Jagapati 9.4 Widjana et al.,
unpublishedb
Jagapati (2004) 94 1.1 (1/94) [6]
Denpasar Penatih 94 23 (22/94) Bakta et al.,
unpublishedb
Renon 515 7.1 (37/515) [3]
Penatih (2004) 128 7.0 (9/128) [6]
Jembrana 1.0 [2]
Buleleng 0.4 [6]
Bangli Trunyan 133 0.8 (1/133) [1]
Karang
Asem
1.0 [2]
a Bali consisting of 9 districts. However data from two other districts
(Tabanan and Klungkung) are scarce or unavailable. In Tabanan District,
mentioned treatment of taeniasis in 17 patients in December, followed by 12,
24, and 36 patients in January, February and March, respectively by the
Tabanan District Health Office Services in 1985 [7]: Quoted from Ref. [28].b Quoted from Ref. [3].
Table 4
Summarized data of prevalence rates of taniasis/cysticercosis in Samosir Island
North Sumatra, 1972–2005
Area surveyed
(year)
Population
sampled
Prevalence
rates (%)
Seroprevalence
of cysticercosis
(%)
Reference
Ambarita 285 9.5 (27/285) [13]
314 1.9 (6/314) [16]
94 11.7 (11/94) [17]
Ambarita 135 20.7 (28/135) [32]a
Ambarita
(2003)
58 3.4 (2/58) 0.0 (0/58) Wandra et al.
unpublished
Ambarita
(2005)
182 2.2 (4/182) 0.0 (0/105) Wandra et al.
unpublished
a Quoted from Ref. [15].
T. Wandra et al. / Parasitology International 55 (2006) S155–S160S158
coproantigen). All (71) other samples from direct smear
negatives were confirmed to be coproantigen negatives.
All proglottid samples from 56 tapeworm carriers were
analyzed by mitochondrial DNA analysis and all were
confirmed to be T. saginata [6,29–31]. There is no evidence
of the distribution of T. asiatica in human in Bali [6]. Local
people in Bali like uncooked meat (with blood) as a traditional
local dish (pork lawar), but they do not like uncooked viscera.
This might be one of the reasons why we could not find any T.
asiatica [6].
The source of infection with T. saginata was related to
consumption of local raw beef dish (beef lawar), under
inadequate meat and food (lawar) inspections [6]. According
to Bali Provincial Livestock Office Services (2004), many
cattle/pigs from many places in Bali were also slaughtered in
illegitimate slaughterhouses, and then distributed to the
markets. Quality control of beef/pork in these illegitimate
slaughterhouse as well as meat hygiene in the markets is rather
difficult due to the limited number of inspectors. In addition,
during 2002–2004, three of 56 tapeworm carriers were lawar
sellers, and had suffered from T. saginata taeniasis for 1–10
years. Several other taeniasis carriers interviewed bought lawar
from these sellers [6].
3. Taeniasis in North Sumatra
The prevalence rates of taeniasis in Ambarita village,
Simanindo Sub-District, Samosir island in Lake Toba, North
Sumatra during 1972–1990 were reported to ranged from 1.9%
to 20.7% [13,16,17,32] (Table 4). Through repeated epidemi-
ological surveys in 2003 and 2005 in this area on 240 local
people revealed that 6 of 240 (2.5%) to be infected of T.
asiatica, included 2 of 58 (3.4%) in 2003 and 4 of 182 (2.2%)
in 2005 (Wandra et al., unpublished data).
Among these 240 local people, 8 persons (2 persons in 2003
and 6 person in 2005) were suspected to be taeniasis cases by
questionnaire method and a total of six persons (2 persons in
2003 and 4 persons 2005) expelled tapeworms after treatment
with praziquantel. Two suspected persons in 2005 through
questionnaire expelled proglottids 1 or 3 years before. So, these
persons were expected to have had taeniid worms but lost them
more than 1 year before. Fecal samples from these two persons
were also negatives by both direct smears and coproantigen
test. All fecal samples from 240 persons examined in 2003 and
2005 were negatives by direct smear (Wandra et al., unpub-
lished data). A total of 182 fecal samples in 2005 re-confirmed
by coproantigen test revealed that four fecal samples (from four
tapeworm carriers) were positives (Craig and Ito, unpublished
data). In Asahikawa Medical College, a new serology for
detection of taeniasis was applied for serum samples from Bali
and Samosir island. However, the sensitivity is still not so high
(Nakao, unpublished data). However, simultaneous serological
tests for screening of both taeniasis and/or cysticercosis
patients may become feasible near future. All six proglottid
samples from six tapeworm carriers detected during 2003 and
2005 were confirmed to be T. asiatica by mitochondrial DNA
analysis [30] (Okamoto et al., unpublished data; Wandra et al.,
unpublished data).
In 2003–2005, there was no person with indication of T.
solium cysticercosis including presence of subcutaneous
nodules. Similar observation and repeated investigations results
were reported by Depary [33] during 1986–1988. The results
of serological examination (ELISA and immunoblot) of 163
serum samples collected in 2003 and 2005 were all negatives
(Table 4).
On Samosir island, the majority of population is Christians
and the people have very rare or never eat beef [13]. In 2003–
2005, all 240 people interviewed were Christians. The number
of people consuming beef was only 2.5% (6/240). Most of
people consumed pork (86.3%, 207/240) and dog meat 8.3%
(20/240), chicken 3.3% (8/240) and sheep 0.8% (2/240). Five
of six taeniasis patients found in 2003–2005 reported that they
usually consumed pork, and one person consumed both pork
and beef. The people on Samosir island like sang-sang (call:
,
,
,
T. Wandra et al. / Parasitology International 55 (2006) S155–S160 S159
sak-sang) as traditional dish with minced pork, viscera and
blood. However, the main risk factor of taeniasis to the people
is due to preparation of sang-sang at home and local restaurants
and also through the traditional or religious celebrations. When
they cut pork into small pieces, sometime they try to eat
uncooked viscera (liver). This is completely different from the
Bali people who do not like the taste of uncooked viscera
(liver).
4. Conclusion
The present survey performed in three districts in southern
part of Bali indicates that T. solium taeniasis and cysticercosis
is now rather rare compared to 10–20 years ago and it is
probably due to improvement in sanitation and pig husbandry,
while T. saginata taeniasis has been increased in number of
cases related to consumption of local raw beef dish (lawar),
under inadequate meat and food (lawar) inspections. There
was no T. asiatica case in human found in Bali [6].
On Samosir island, North Sumatra where T. asiatica
taeniasis is still common, it was related to consumption of
uncooked viscera of local pig (domesticated wild boar).
However the prevalence rates were decreased compared to
previous repots in 1972–1990, due to sustainable health
education for boiling meat and viscera.
For detection of tapeworm carries of T. saginata and T.
asiatica in order to provide active and passive case finding and
surveillance, distribution of questionnaire is simple method for
doctor (health worker) especially in local health centers.
Corpoantigen test developed for detection of taeniasis of T.
solium is also highly reliable to detect taeniasis carriers in the
community.
Considering the differences in cultures, religions, education
and socio-economic levels, etc., control programs should be
adapted to the local situations [34]. Following strategies appear
to have priorities in Bali and Samosir islands, North Sumatra:
1) Active case finding (active surveillance) and treat the
tapeworm carriers, and 2) Sustainable public health education
through treatment. In addition in Bali: Check beef lawar
hygiene including lawar sellers’ health, periodically; establish
a system to check the quality of beef/pork; and look for
distribution of infected animals are needed.
Acknowledgements
This work was supported by Japan Society for Promotion of
Science (JSPS) to A.I. (142560001; 17256002). T.W. is a
Ronpaku researcher getting the JSPS scholarship from 2003.
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