The present situation and towards the prevention and control of neurocysticercosis on the tropical island, Bali, Indonesia
- Toni Wandra†1,
- Kadek Swastika†2, 5, 6,
- Nyoman S Dharmawan†3,
- Ivan Elisabeth Purba1,
- I Made Sudarmaja2,
- Takahiko Yoshida4,
- Yasuhito Sako5,
- Munehiro Okamoto†6,
- Ni Luh Putu Eka Diarthini2,
- Dewa Ayu Agus Sri Laksemi2,
- Tetsuya Yanagida5, 7,
- Minoru Nakao5 and
- Akira Ito†5Email author
© Wandra et al.; licensee BioMed Central. 2015
Received: 9 December 2014
Accepted: 18 February 2015
Published: 7 March 2015
Neurocysticercosis (NCC), which is caused by accidental ingestion of eggs of the pork tapeworm, Taenia solium, was common in Bali, Indonesia until the early 1990s. However, improved education on hygiene and sanitation, a move to keeping pigs indoors, and improvement of economic and living conditions have substantially reduced the occurrence of NCC in Bali. Since 2011, T. solium tapeworm carriers (T. solium taeniasis) and heavily infected pigs and dogs have exclusively been detected from villages in mountainous regions of northeastern Bali where NCC and ocular cysticercosis (OCC) cases have also been identified. In response to this continued area of high infection, a one-day workshop was convened to discuss how to prevent and control this potentially lethal zoonotic parasitic infection in Bali. This review presents an overview of the current status of T. solium taeniasis and cysticercosis in Indonesia and proposes a strategy for the prevention and control of this zoonosis in Bali.
Taenia solium (also known as the pork tapeworm) and Taenia saginata (also known as the beef tapeworm) are human cestodes with a cosmopolitan distribution. These cestode infections result in both economic and public health impacts on affected communities [1-24]. Cysticercosis, which is caused by the larval stage of T. solium, is prevalent in humans and pigs mainly in many developing countries of the Americas, Africa and Asia but also in Europe as well [1-3,14,18,19,21,22,24]. Approximately 50 million people are suffering from neurocysticercosis (NCC) due to T. solium globally and more than 50,000 deaths per year are due to NCC [6,25]. Increased international travel and immigration are resulting in NCC being diagnosed and treated more frequently in non-endemic areas [5,26-33].
This review presents an overview of the current status of human taeniases caused by T. solium, T. saginata and Taenia asiatica and cysticercoses caused by T. solium (humans and livestock) and Taenia hydatigena (livestock) in Indonesia. A strategy for the prevention and control of this zoonosis in Bali is also proposed. Presented information is based on an ongoing joint project towards the control of human NCC in Indonesia which started in 1996 using several Japanese research funds. The topics addressed in this review are based on summaries from a one-day international workshop entitled “Strengthening of Prevention and Control of Taeniasis/Cysticercosis and Soil Transmitted Helminthiases in Bali, Indonesia” held at the Faculty of Medicine, University of Udayana, Bali on 22 September 2014.
Taeniases caused by three human Taenia species in Indonesia
In Thailand  and China  where T. saginata, T. asiatica, and T. solium are sympatrically distributed, hybrids or hybrid-derived tapeworms of T. saginata and T. asiatica have been confirmed by mitochondrial and nuclear DNA analyses [50-52]. Therefore, T. saginata and T. asiatica specimens collected in Indonesia should also be analyzed to determine whether or not hybridization is occurring.
Cysticercosis in Indonesia
Papua (Irian Jaya): T. solium taeniasis and NCC highly endemic
Bali: T. saginata and T. solium taeniases and NCC
No. of T. saginata taeniasis cases
No. of T. solium taeniasis cases
Seroprevalence of cysticercosis in humans (%)
Seroprevalence of cysticercosis in pigs (%)
Gianyar (Jan 2013)
Gianyar (Sept 2013)
Karangasem (urban area, 2006)
Karangasem (rural area, 2011)
Karangasem (Jan. 2013)
Karangasem (Sept. 2013)
No. of case
Gianyar/Sanglah Hosp. (2003)
1 (disseminated cysticercosis)
NCC (dual infection)
1 (with T. saginata taeniasis)
3 (with T. saginata taeniasis) (dual infection)
When tapeworm carriers in Gianyar were treated with praziquantel (PZQ) (15 mg/kg BW), one individual had an epileptic seizure within half a day of receiving the drug. This patient was later confirmed as having previously asymptomatic NCC, which became symptomatic after receiving PZQ [89,92]. This case was also confirmed serologically to be cysticercosis . If a lower dose of PZQ (5 mg/kg BW) which is sufficient for expulsion of tapeworms but not sufficient for damaging cysticerci was administered , this veiled asymptomatic NCC could not become symptomatic, and we could not find dual infections with T. saginata taeniasis and T. solium NCC. It is believed that T. saginata infections in people were due to consumption of undercooked beef “lawar” contaminated with cysticerci. In contrast, it is believed that the NCC case was due to accidental ingestion of T. solium eggs from a tapeworm carrier who had been infected in a T. solium endemic area of Bali.
Bali (eastern slope of Mt. Agung in Karangasem): T. solium tapeworm carriers and infected pigs
The weather on the eastern slope of Mt. Agung differs from other areas in Bali, with little grass available during the dry season (Figure 5). Since all climbing routes to Mt. Agung are located on the western side of the mountain, the endemic villages are almost completely isolated. However, residents of this area often go to the local capital city of Denpasar or other districts to find work, which has the potential to result in an outbreak of NCC in these non-endemic areas [85,97-100].
Modern tools for identification of taeniasis carriers, cysticercosis patients, and cysticercosis in pigs
Multiplex PCR was first used to identify parasites that were expelled after chemotherapeutic therapy, since the expelled tapeworms were often damaged and without a scolex, which is useful for the differentiation of T. solium with hooklets on the scolex from two other T. saginata-like species without hooklets. As eggs of Taenia spp. are impossible to be identified morphologically, molecular analysis using even a single egg in feces  is essential for the identification of the Taenia species. While multiplex PCR was useful for differentiation of adult worms [75,76,97-100], it was not optimal for the detection of DNA in stool samples. It is important to be able to detect parasite-specific DNA in stool samples to avoid inducing epileptic seizures in taeniasis cases that also have asymptomatic NCC [88,89]. Recently, loop mediated isothermal amplification (LAMP) and copro-LAMP have been utilized to obtain real-time identifications of Taenia species [102-104]. Molecular identification using a haplotype network of mitochondrial gene(s) is another useful tool for identifying the infecting species [105,106].
Cysticercoses in pigs and dogs
Pigs confirmed to be naturally infected with T. solium show antibody responses to antigens purified by preparative iso-electric focusing [69,70] and recombinant antigens [67,71,107,108]. Similar results are also achieved using a more simple and cheap, cathion-exchange chromatography . Antibody responses in pigs in endemic areas have been tested using an ELISA with tests read by looking for a colour change with the naked eye (Dharmawan et al. unpublished) [36,37]. The majority of pigs showing strong positive responses were confirmed to be infected with T. solium cysticerci, with the remainder infected with T. hydatigena. Pigs infected with T. hydatigena tended to have a much weaker positive test than pigs infected with T. solium (Dharmawan et al. unpublished). Cysticercoses in pigs co-infected with these two species should also be identified due to the risk of human NCC [70,109].
Available serology is also applicable to dogs in endemic areas . Residents of villages in Kubu are known to eat dog meat, with local dogs confirmed to be infected with T. solium. Therefore, studies are needed to evaluate the role of dogs in the T. solium life cycle. In addition, the role of dogs should also be included in local education programmes .
International meetings on NCC in Bali
NCC was discussed at two International meetings on “Recent Progress in Parasitology” (August 2007) and “Neurological Diseases” (November 2009) held in Denpasar. The meetings were aimed at both clinicians and medical researchers. These meetings were in addition to a symposium on cestode zoonoses in Asia which has been held almost every year since 2000 in Thailand, and in Japan (2006), and in Korea (2007) [39,60,64,68,72,73,76-78,89,98,99,110-112]. On 22 September 2014, a workshop focusing exclusively on the control of taeniasis and NCC was held at the University of Udayana. The meeting was aimed at personnel working in medicine, veterinary medicine, public health, meat inspection, and the local government.
Towards control of NCC
Since 2011, T. solium in Bali has been maintained in a small area on the eastern slope of Mt. Agung. However, the prevalence and distribution of NCC seems to be increasing through immigration of individuals from this endemic area to the Denpasar metropolitan area. As shown in Figure 5, during the dry season, villagers have difficulty in obtaining safe drinking water and feed for their pigs. Therefore, pigs are often left to roam and scavenge during the dry season. In addition, during the dry season, local inhabitants often go to Denpasar or other larger cities to find work, increasing the risk of bringing T. solium to currently non-endemic locations. This phenomenon has also been seen in refugee villages along the Thailand-Myanmar border , and in Tibetan communities in Sichuan Province, China .
Due to the stigma attached to being a tapeworm carrier, most people are not willing to submit a stool sample for evaluation. It is also difficult to change local food consumption behavior lawar, a traditional food made with uncooked beef or pork is commonly consumed in the endemic areas of Bali. In Gianyar district, while the majority of people stop eating lawar after being diagnosed with tapeworm(s), it is not uncommon for these same individuals to start eating lawar again 1–3 months later (Figure 2) . Based on questionnaires administered to residents of a T. solium endemic area in Karangasem district, 29% (18/62) of families have no sanitary facilities and people defecate in the garden, 83.9% (40/46) of pig owners keep their pigs in a fenced field, 10.9% (5/46) keep their pigs in an open common pasture, and 2.2% (1/46) allow their pigs to roam free . Based on direct observations, environmental sanitation and personal hygiene is also very poor in this region.
In Bali, infection with T. saginata is believed to be related to consumption of beef lawar. Quality control of beef and pork is difficult due to the presence of illegal slaughterhouses in addition to a limited number of official meat inspectors. In study conducted in 2002–2004, three of 56 identified tapeworm carriers were lawar sellers who acknowledged suffering from T. saginata taeniasis for 1–10 years. Several other taeniasis carriers indicated that they bought lawar from these sellers (Wandra, personal communication).
The health sector budget allocated by the central government for taeniasis control is very limited due to the presence of other important communicable diseases and the need for resources to be channeled into the country’s environmental health programme. There is also very little funding to pursue control measures at the provincial and district levels. Similarly, T. solium has a low priority for the agricultural sector and, therefore, receives little to no funding from this sector.
Approximately more or less than 3 million travelers visiting the island of Bali every year may be at risk for acquiring T. solium cysticercosis. Fortunately, the identified highly endemic areas are not commonly visited by tourists. Due to the limited geographic distribution of the parasite, it may be possible to control and eradicate T. solium from Bali given the appropriate resources. Successful control of T. solium transmission on Bali could then be used as a model for other islands in Indonesia and beyond.
Combine the prevention and control of taeniasis and NCC with the prevention and control of STHs. As STHs including Ascaris, Trichuris and hookworms etc. are more common than Taenia, detection of taeniasis carriers are one part of STH surveys. All STH carriers have been medicated through all taeniasis projects in Indonesia.
Review and strengthen the ‘legal aspects’ for the prevention and control of taeniasis and NCC at the provincial, district, and local level. This would include standardizing policies and methods for the distribution of guidelines for the prevention and control of taeniasis and NCC. It would also include better law enforcement to prevent the occurrence of illegal slaughterhouses.
Strengthen buy-in of policy makers, stake holders, professional organizations, universities, NGOs, and members of the private sector.
Intensify active and passive surveillance, with prompt treatment of identified tapeworm carriers.
Conduct periodic health inspection of lawar sellers and their family members.
Conduct health investigations of family members and neighbours of newly diagnosed NCC patients.
Improve public health education focusing on personal hygiene, environmental sanitation, and practices related to pig and cattle rearing, with an emphasis on primary school-aged children.
Develop and distribute IEC media on taeniasis and NCC prevention that has been translated into the local languages/dialects and edited to be socially and culturally appropriate.
Further invest in local health education programmes by training additional health workers and then having them participate in a train-the-trainer programme.
Strengthen the epidemiological surveillance of taeniasis and NCC in Bali by using validated diagnostic tools.
Provide additional funding for the prevention and control of taeniasis and NCC.
Improve the meat inspection system and conduct studies to determine the prevalence and distribution of infected animals.
Encourage political commitment and inter-sectoral collaboration at the local, national, and international levels.
Put in place a system to monitor and evaluate the taeniasis and NCC prevention and control programme in Bali.
Vaccination of pigs is an additional highly promising action plan [113-117]. Detection of pigs contaminated with cysticerci of T. solium by simple but reliable serology (Dharmawan et al. unpublished) [36,37,67,70], and simultaneous vaccinations of all pigs by oral treatment with oxfendazole (30 mg/kg) at the same time as the booster vaccination [116,117] may be the best. However, through sustainable education which almost succeeded in control of taeniasis and NCC in Bali over the past two decades, further sustainable education and improvement of living environment and treatment of T. solium taeniasis carriers, especially in endemic area, Karangasem, may be sufficient for successful control of taeniasis and NCC in Bali. If the budget for the control of NCC is big enough to introduce vaccination trials, it is the best.
In order to strengthen the NCC prevention and control programme in Bali, a Research Center at University of Udayana will be established. University of Udayana was selected due to its hospital’s clinical experience with the treatment of NCC as well at the presence of faculties of medicine and veterinary medicine. This new research center will complement the current work being conducted on the prevention and control of other neglected tropical diseases, i.e. rabies in Bali.
An overview of the current status of T. solium taeniasis and cysticercosis in Indonesia reveals the importance of a strategy for the prevention and control of this zoonosis in Bali.
This study in Indonesia has been supported by a Grant-in-Aid (A) (21256003, 24256002) to AI and (B) (21406009, 24406011) to MO, from the Japan Society for the Promotion of Science (JSPS) and was supported by JSPS-Asia/Africa Scientific Platform Fund (2006–2011) and by the Special Coordination Fund for Promoting Science and Technology from the Ministry of Education, Japan (2003–2005, 2010–2012) to AI. We sincerely thank Christine Budke for her amendment of this MS.
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