taeniasis and cysticercosis in bali and north sumatra, indonesia

6
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, Indonesia b Department of Parasitology, University of Sumatra Utara, North Sumatra, Indonesia c Department of Parasitology, University of Udayana, Bali, Indonesia d Department Research and Community Service, University of Indonesia, Indonesia e University of Tottori, Tottori, Japan f University of Salford, Greater Manchester, UK g 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 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). 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. Parasitology International 55 (2006) S155 – S160 www.elsevier.com/locate/parint

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Page 1: Taeniasis and cysticercosis in Bali and North Sumatra, Indonesia

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

Page 2: Taeniasis and cysticercosis in Bali and North Sumatra, Indonesia

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

Page 3: Taeniasis and cysticercosis in Bali and North Sumatra, Indonesia

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

Page 4: Taeniasis and cysticercosis in Bali and North Sumatra, Indonesia

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:

,

,

,

Page 5: Taeniasis and cysticercosis in Bali and North Sumatra, Indonesia

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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