- Open Access
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
- Taenia saginata
- Taenia asiatica
- Parasitic zoonosis
- Soil transmitted helminthiases
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.
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.
- Pawlowski Z, Schultz MG. Taeniasis and cysticercosis (Taenia saginata). Adv Parasitol. 1972;10:269–343.PubMedGoogle Scholar
- Flisser A, Willms K, Laclette JP, Larralde C, Ridaura C, Beltran F. Cysticercosis: present state of knowledge and perspectives. New York: Academic Press; 1982. p. 1–700.Google Scholar
- Gemmell M, Matyas Z, Pawlowski Z, Soulsby EJL. Guidelines for surveillance, prevention and control of Taeniasis/Cysticercosis. Geneva: VPH/83.49, WHO; 1983. p. 1–207.Google Scholar
- Richards Jr F, Schantz PM. Cysticercosis and taeniasis. N Engl J Med. 1985;312:787–8.PubMedGoogle Scholar
- Schantz PM, Moore AC, Munoz JL, Hartman BJ, Schaefer JA, Aron AM, et al. Neurocysticercosis in an Orthodox Jewish community in New York City. N Engl J Med. 1992;327:692–5.PubMedGoogle Scholar
- Schantz PM, Cruz M, Sarti E, Pawlowski Z. Potential eradicability of taeniasis and cysticercosis. Bull Pan Am Health Organ. 1993;27:397–403.PubMedGoogle Scholar
- White Jr AC. Neurocysticercosis: a major cause of neurological disease worldwide. Clin Infect Dis. 1997;24:101–13.PubMedGoogle Scholar
- Schantz PM, Wilkins PP, Tsang VCW. Immigrants, imaging, and immunoblots: the emergence of neurocysticercosis as a significant public health problem. In: Scheld WM, Craig WA, Hughes JM, editors. Emerging infections 2. Washington: ASM Press; 1998. p. 213–42.Google Scholar
- Craig PS, Pawlowski Z. Cestode zoonoses: echinococcosis and cysticercosis. NATO Sci Series I: Life and Behavioural Sciences. Amsterdam: IOS Press; 2002. p. 1–395.Google Scholar
- Carpio A. Neurocysticercosis: an update. Lancet Infect Dis. 2002;2:751–62.PubMedGoogle Scholar
- Schantz PM. Taenia solium cysticercosis: an overview of global distribution and transmission. In: Signh G, Prabhakar S, editors. Taenia solium Cysticercosis. From basic to clinical science. Oxon: CABI Publishing; 2002. p. 63–73.Google Scholar
- Garcia HH, Gonzalez AE, Evans CAW, Gilman RH, for the Cysticercosis Working Group in Peru. Taenia solium cysticercosis. Lancet. 2003;361:547–56.Google Scholar
- Ito A, Nakao M, Wandra T. Rapid Review: Human taeniasis and cysticercosis in Asia. Lancet. 2003;362:1918–20.PubMedGoogle Scholar
- Murrell KD. International action planning workshop on Taenia solium cysticercosis/taeniosis with special focus on Eastern and Southern Africa. Acta Trop. 2003;87:1–191.Google Scholar
- Murrell KD. WHO/FAO/OIE Guidelines for the surveillance, prevention and control of taeniosis/cysticercosis. Paris: OIE; 2005. p. 1–139.Google Scholar
- Garcia HH, Del Brutto OH, for the Cysticercosis Working Group in Peru. Neurocysticercosis: updated concepts about an old disease. Lancet Neurol. 2005;4:653–61.PubMedGoogle Scholar
- Ito A, Craig PS, Schantz PM. Taeniasis/cysticercosis and echinococcosis with focus on Asia and the Pacific. Parasitol Int. 2006;55:s1–311.Google Scholar
- Ito A, Zhou XN, Craig PS, Giraudoux P. Control of cestode zoonoses in Asia: role of basic and applied science. Parasitology. 2013;140:1547–700.PubMedGoogle Scholar
- Robertson LJ, van der Giessen JWB, Batz MB, Kojima M, Cahill S. Have food borne parasites finally become a global concern? Trends Parasitol. 2013;29:101–3.PubMedGoogle Scholar
- Robertson LJ, Sprong H, Ortega YR, van der Giessen JWB, Fayer R. Impacts of globalisation on foodborne parasites. Trends Parasitol. 2014;30:37–52.PubMedGoogle Scholar
- Torgerson PR, de Silva NR, Fevre EM, Kasuga F, Rokni MB, Zhou XN, et al. The global burden of foodborne parasitic disease: an update. Trends Parasitol. 2014;30:20–6.PubMedGoogle Scholar
- Ito A, Budke CM. Culinary delights and travel? A review of zoonotic cestodiases and metacestodiases. Trav Med Infect Dis. 2014;12:582–91.Google Scholar
- Dorny P, Praet N, Deckers N, Gabriel S. Emerging food-borne parasites. Vet Parasitol. 2009;163:196–206.PubMedGoogle Scholar
- Willingham AL, Wu HW, Conlan J, Satrija F. Combating Taenia solium cysticercosis in Southeast Asia: an opportunity for improving human health and livestock production. Adv Parasitol. 2010;72:235–66.PubMedGoogle Scholar
- Del Brutto OH, Rajashekhar V, White Jr AC, Tsang VC, Nash TE, Takayanagui OM, et al. Proposed diagnostic criteria for neurocysticercosis. Neurology. 2001;57:177–83.PubMed CentralPubMedGoogle Scholar
- Sorvillo FJ, Waterman SH, Richerds FO, Schantz PM. Cysticercosis surveillance: locally acquired and travel-related infections and detection of intestinal tapeworm carriers in Los Angeles County. Am J Trop Med Hyg. 1992;47:365–71.PubMedGoogle Scholar
- Sorvillo FJ, DeGiorgio C, Waterman SH. Deaths from cysticercosis, United States. Emerg Infect Dis. 2007;13:230–5.PubMed CentralPubMedGoogle Scholar
- Sorvillo F, Wilkins P, Shafir S, Ebenhard M. Public health implications of cysticercosis acquired in the United States. Emerg Infect Dis. 2011;17:1–6.PubMed CentralPubMedGoogle Scholar
- Hira PR, Francis I, Abdella NA, Gupta R, Al-Ali FM, Grover S, et al. Imported and autochthonous infections in Kuwait. Trans R Soc Trop Med Hyg. 2004;98:233–9.PubMedGoogle Scholar
- Leshem E, Kliers I, Bakon M, Gomori M, Karplus R, Schwartz E. Neurocysticercosis in travelers: a nation-wide study in Israel. J Travel Med. 2010;18:191–7.Google Scholar
- Cantey PT, Coyle CM, Sorvillo FJ, Wilkins PP, Starr MC, Nash TE. Neglected parasitic infections in the United States: cysticercosis. Am J Trop Med Hyg. 2014;90:805–9.PubMed CentralPubMedGoogle Scholar
- Yanagida T, Sako Y, Nakao M, Nakaya K, Ito A. Mini Review: Taeniasis and cysticercosis due to Taenia solium in Japan. Parasit Vectors. 2012;5:18.PubMed CentralPubMedGoogle Scholar
- Kobayashi K, Nakamura-Uchiyama F, Nishiguchi T, Isoda K, Kokubo Y, Ando K, et al. Rare case of disseminated cysticercosis and taeniasis in a Japanese traveler after returning from India. Am J Trop Med Hyg. 2013;89:58–62.PubMed CentralPubMedGoogle Scholar
- Ito A, Putra MI, Subahar R, Sato MO, Okamoto M, Sako Y, et al. Dogs as alternative intermediate hosts of Taenia solium in Papua (Irian Jaya), Indonesia confirmed by highly specific ELISA and immunoblot using native and recombinant antigens and mitochondrial DNA analysis. J Helminthol. 2002;76:311–4.PubMedGoogle Scholar
- Hoberg E, Alkire NL, de Queiroz A, Jones A. Out of Africa: origin of the Taenia tapeworms in humans. Proc Biol Sci. 2001;268:781–7.PubMed CentralPubMedGoogle Scholar
- Ito A. Basic and applied problems in developmental biology and immunobiology of cestode infections. Parasite Immunol. 2015;37:53–69.PubMedGoogle Scholar
- Ito A. Nothing is perfect! Trouble-shooting in immunological and molecular studies of cestode infections. Parasitology. 2013;140:1551–65.PubMedGoogle Scholar
- Simanjuntak GM, Margono SS, Okamoto M, Ito A. Taeniasis/cysticercosis in Indonesia as an emerging disease. Parasitol Today. 1997;13:321–3.Google Scholar
- Wandra T, Margono SS, Gafar MS, Saragih JM, Sutisna P, Sudewi AAR, et al. Current situation of taeniasis/cysticercosis in Indonesia. Trop Med Health. 2007;35:323–8.Google Scholar
- Margono SS, Ito A, Sato MO, Okamoto M, Subahar R, Yamasaki H, et al. Taenia solium taeniasis/cysticercosis in Papua, Indonesia in 2001: detection of human worm carriers. J Helminthol. 2003;77:39–42.PubMedGoogle Scholar
- Ito A, Wandra T, Yamasaki H, Nakao M, Sako Y, Nakaya K, et al. Review article: Cysticercosis/taeniasis in Asia and the Pacific. Vector-Borne Zoonotic Dis. 2004;4:96–107.Google Scholar
- Suroso T, Margono SS, Wandra T, Ito A. Challenges for control of taeniasis/cysticercosis in Indonesia. Parasitol Int. 2006;55:s161–5.PubMedGoogle Scholar
- Wandra T, Ito A, Swastika K, Dharmawan NS, Sako Y, Okamoto M. The past and present situation of taeniasis and cysticercosis in Indonesia. Parasitology. 2013;140:1608–16.PubMedGoogle Scholar
- Kosin E, Depary AAS, Djohansjah A. Taeniasis di pulau Samosir. Maj Kedok Univ Sumatera Utara Medan. 1972;3:5–11 (in Indonesian).Google Scholar
- Fan PC, Kosman ML, Kosin E, Depary AA, Napitupulu T. Indonesia Taenia and taeniasis. Yonsei Rep Trop Med. 1990;21:33–7.Google Scholar
- Wandra T, Sutisna P, Dharmawan NS, Margono SS, Sudewi R, Suroso T, et al. High prevalence of Taenia saginata taeniasis and status of Taenia solium cysticercosis in Bali, Indonesia, 2002–2004. Trans R Soc Trop Med Hyg. 2006;100:346–53.PubMedGoogle Scholar
- Wandra T, Depary AA, Sutisna P, Margono SS, Suroso T, Okamoto M, et al. Taeniasis and cysticercosis in Bali and north Sumatra, Indonesia. Parasitol Int. 2006;55:s155–60.PubMedGoogle Scholar
- Anantaphruti MT, Yamasaki H, Waikagul H, Wattanakulpanich D, Nuamtanong S, Maipanich W, et al. Sympatric occurrence of Taenia asiatica, Taenia saginata and Taenia solium in Kanchanaburi Province, western Thailand. Emerg Infect Dis. 2007;13:1413–6.PubMed CentralPubMedGoogle Scholar
- Li T, Craig PS, Ito A, Chen X, Qiu D, Qiu J, et al. Taeniasis/cysticercosis in a Tibetan population in Sichuan Province, China. Acta Trop. 2006;100:223–31.PubMedGoogle Scholar
- Okamoto M, Nakao M, Blair D, Anantaphruti MT, Waikagul J, Ito A. Evidence of hybridization between Taenia saginata and Taenia asiatica. Parasitol Int. 2010;59:70–4.PubMedGoogle Scholar
- Yamane K, Suzuki Y, Tachi E, Li TY, Chen XW, Nakao M, et al. Recent hybridization between Taenia asiatica and Taenia saginata. Parasitol Int. 2012;61:351–5.PubMedGoogle Scholar
- Yamane K, Yanagida T, Li T, Chen X, Dekumyoy P, Waikagul J, et al. Complicated relationships between Taenia saginata and Taenia asiatica and their hybrids. Parasitology. 2013;140:1595–601.PubMedGoogle Scholar
- Tumada LR, Margono SS. Cysticercosis in the area of the Wissel Lakes, West Irian. Southeast Asian J Trop Med Public Health. 1973;4:371–6.PubMedGoogle Scholar
- Desowitz RS, Margono SS, Sutjahyo, Simanjuntak G. Observations on the application of counterimmunoelectrophoresis for the seroepidemiology of human cysticercosis. Southeast Asian J Trop Med Public Health. 1977;8:303–7.Google Scholar
- Subianto DB, Tumada LR, Margono SS. Burns and epileptic fits associated with cysticercosis in mountain people of Irian Jaya. Trop Geogr Med. 1978;30:275–8.PubMedGoogle Scholar
- Coker-Vann MR, Subianto DB, Brown P, Diwan AR, Desowitz R, Garruto RM, et al. ELISA antibodies to cysticerci of Taenia solium in human populations in new Guinea, Oceania and Southeast Asia. Southeast Asian J Trop Med Public Health. 1981;12:499–505.PubMedGoogle Scholar
- Handali S, Liying H, Lusikoy C, Senis J, Sihombing D. A survey report—July 1993: Cysticercosis in the Grand Dali valley, Jayawijaya district, Irian Jaya province, Indonesia. Southeast Asian J Trop Med Public Health. 1997;28:22–5.PubMedGoogle Scholar
- Wandra T, Subahar R, Simanjuntak GM, Margono SS, Suroso T, Okamoto M, et al. Resurgence of cases of epileptic seizures and burns associated with cysticercosis in Assologaima, Jayawijaya, Irian Jaya, Indonesia, 1991–95. Trans R Soc Trop Med Hyg. 2000;94:46–50.PubMedGoogle Scholar
- Margono SS, Ito A, Suroso T. The problem of taeniasis and cysticercosis in Irian Jaya, Indonesia. Med J Indonesia. 2001;10:110–4.Google Scholar
- Margono SS, Subahar R, Hamid A, Wandra T, Sudewi SS, Sutisna P, et al. Cysticercosis in Indonesia: epidemiological aspects. Southeast Asian J Trop Med Public Health. 2001;32 Suppl 2:79–84.PubMedGoogle Scholar
- Subahar R, Hamid A, Purba W, Wandra T, Karma C, Sako Y, et al. Taenia solium infection in Irian Jaya (West Papua), Indonesia: a pilot serological survey of human and porcine cysticercosis in Jayawijaya District. Trans R Soc Trop Med Hyg. 2001;95:388–90.PubMedGoogle Scholar
- Margono SS, Ito A, Suroso T. The problem of taeniasis and cysticercosis in Irian Jaya (Papua), Indonesia. In: Chen ER, Yamaguchi T, Chung WC, editors. Parasitic Zoonoses in Asian-Pacific Regions 2000. Taipei: The Organizing Committee Asian-Pacific Congress for Parasitic Zoonoses Taipei; 2000. p. 55–64.Google Scholar
- Wandra T, Ito A, Yamasaki H, Suroso T, Margono SS. Taenia solium in Irian Jaya, Indonesia. Emerg Infect Dis. 2003;9:884–5.PubMed CentralPubMedGoogle Scholar
- Simanjuntak GM, Widarso HS. The current Taenia solium taeniasis/cysticercosis situation in Indonesia. Southeast Asian J Trop Med Public Health. 2004;35 Suppl 1:240–6.Google Scholar
- Margono SS, Wandra T, Swarsono MF, Murni S, Craig PS, Ito A. Taeniasis/cysticercosis in Papua (Irian Jaya), Indonesia. Parasitol Int. 2006;55:s143–8.PubMedGoogle Scholar
- Salim L, Ang A, Handali S, Cysticercosis Working Group in Papua, Tsang VC. Seroepidemiologic survey of cysticercosis-taeniasis in four central highland districts of Papua, Indonesia. Am J Trop Med Hyg. 2009;80:384–8.PubMedGoogle Scholar
- Sako Y, Itoh S, Okamoto M, Nakaya K, Ito A. Simple and reliable preparation of immunodiagnostic antigens for Taenia solium cysticercosis. Parasitology. 2013;140:1589–94.PubMedGoogle Scholar
- Wandra T, Margono SS, Suroso T, Wibisono H, Ito A. Taeniasis/cysticercosis in Indonesia. Southeast Asian J Trop Med Public Health. 2007;38 Suppl 1:140–3.Google Scholar
- Ito A, Plancarte A, Ma L, Kong Y, Flisser A, Cho YS, et al. Novel antigens for neurocysticercosis: simple method for preparation and evaluation for serodiagnosis. Am J Trop Med Hyg. 1998;59:291–4.PubMedGoogle Scholar
- Ito A, Plancarte A, Nakao M, Nakaya K, Ikejima T, Piao ZX, et al. ELISA and immunoblot using purified glycoproteins for serodiagnosis of cysticercosis in pigs naturally infected with Taenia solium. J Helminthol. 1999;73:363–5.PubMedGoogle Scholar
- Sako Y, Nakao M, Ikejima T, Piao XZ, Nakaya K, Ito A. Molecular characterization and diagnostic value of Taenia solium low-molecular-weight antigen genes. J Clin Microbiol. 2000;38:4439–44.PubMed CentralPubMedGoogle Scholar
- Ito A, Nakao M, Sako Y, Nakaya K. Neurocysticercosis and echinococcosis in Asia: Recent advances in the establishment of highly reliable differential serodiagnosis for international collaboration. Southeast Asian J Trop Med Public Health. 2000;31 Suppl 1:16–20.PubMedGoogle Scholar
- Ito A, Wandra T, Subahar R, Hamid A, Yamasaki H, Sako Y, et al. Recent advances in basic and applied science for the control of taeniasis/cysticercosis in Asia. Southeast Asian J Trop Med Public Health. 2002;33 Suppl 3:79–82.PubMedGoogle Scholar
- Sato MO, Yamasaki H, Sako Y, Nakao M, Nakaya K, Plancarte A, et al. Evaluation of tongue inspection and serology for diagnosis of Taenia solium cysticercosis in swine: usefulness of ELISA using purified glycoproteins and recombinant antigen. Vet Parasitol. 2003;111:309–22.PubMedGoogle Scholar
- Sato MO, Sako Y, Nakao M, Yamasaki H, Nakaya K, Ito A. Evaluation of purified Taenia solium glycoprotein and recombinant antigens in the serologic detection of human and swine cysticercosis. J Infect Dis. 2006;194:1783–90.PubMedGoogle Scholar
- Ito A, Takayanagui MO, Sako Y, Sato MO, Odashima NS, Yamasaki H, et al. Review: Neurocysticercosis: the usefulness of highly specific serology and molecular confirmation of histopathologic specimens. Southeast Asian J Trop Med Public Health. 2006;37 Suppl 3:74–81.PubMedGoogle Scholar
- Sato MO, Sako Y, Nakao M, Wandra T, Yamasaki H, Nakaya K, et al. Usefulness of immunological and molecular tools: programs towards control and eradication of cysticercosis in endemic areas. Southeast Asian J Trop Med Public Health. 2007;38 Suppl 1:159–65.Google Scholar
- Ito A, Sako Y, Nakao M, Nakaya K, Okamoto M, Wandra T, et al. Molecular and immunological diagnosis of taeniasis and cysticercosis in Asia and the Pacific. Southeast Asian J Trop Med Public Health. 2008;39 Suppl 1:37–47.Google Scholar
- Ngoerah IGNG. Cysticercosis of the central nervous system. Maj Ilmiah Univ Ud. 1975;2:31–8. in Indonesian.Google Scholar
- Sutisna P. Parasitic infections in humans in Bali: a review. Bull Penelitian Kesehatan. 1989;17:276–83.Google Scholar
- Sutisna P. The problem of taeniasis in Banjar Kelod, Renon, Denpasar. Medika. 1990;7:543–9.Google Scholar
- Sutisna P. Sistiserkosis di Bali: laporan 6 kasus. Maj Ilmiah Univ Ud. 1994;41:5–9 (in Indonesian).Google Scholar
- Suweta IG. The situation of cysticercosis/taeniasis in animal/man in Bali. Southeast Asian J Trop Med Public Health. 1991;22(Suppl):236–8.PubMedGoogle Scholar
- Dharmawan NS, Siregar EAA, He S, Hsibuan KM. Cysticercosis padababi di Bali. Hemera Zoa. 1992;75:25–37 (in Indonesian).Google Scholar
- Theis JH, Goldsmith RS, Flisser A, Koss J, Chionino C, Plancarte A, et al. Detection by immunoblot assay of antibodies to Taenia solium cysticerci in sera from residents of rural communities and from epileptic patients in Bali, Indonesia. Southeast Asian J Trop Med Public Health. 1994;25:464–8.PubMedGoogle Scholar
- Sutisna P, Kapti IN, Allan JC, Rodrigues-Canul R, Craig PS. Prevalence of taeniasis and cysticercosis in Banjar Pamesan, Ketewel village, Gianyar, Bali. Maj Kedok Ud. 2000;31:226–34.Google Scholar
- Margono SS, Himawan S, Purnama TA, Subahar R, Hamid A, Ito A. Multiple cysticercus nodules in skin and brain in a Balinese woman: a case report. Med J Indonesia. 2002;11:169–73.Google Scholar
- Sudewi AAR, Wandra T, Artha A, Nkouawa A, Ito A. Taenia solium cysticercosis, Bali, Indonesia, with serology and mitochondrial DNA. Trans R Soc Trop Med Hyg. 2008;102:96–8.PubMedGoogle Scholar
- Wandra T, Sudewi RAA, Swastika IK, Sutisna P, Dharmawan NS, Yulfi H, et al. Taeniasis/cysticercosis in Bali, Indonesia. Southeast Asian J Trop Med Public Health. 2011;42:793–802.PubMedGoogle Scholar
- Swastika K, Dewiyani CI, Yanagida T, Sako Y, Sudamaja M, Sutisna P, et al. An ocular cysticercosis in Bali, Indonesia caused by Taenia solium Asian genotype. Parasitol Int. 2012;61:378–80.PubMedGoogle Scholar
- Raka Sudewi AA, Nuartha AABN. Gambaran CT scan beberapa kasus neurosistiserkosis di Rumah Sakit Umum Pusat Denpasar. Conference and Yearly Scientific Meeting, Indonesian Neurologist Association, Malang, Indonesia, 1998 (in Indonesian).Google Scholar
- Sarti E, Schantz PM, Avila G, Ambrosio J, Medina-Santilan R, Flisser A. Mass treatment against human taeniasis for the control of cysticercosis: a population-based intervention study. Trans R Soc Trop Med Hyg. 2000;94:85–9.PubMedGoogle Scholar
- Ito A, Okamoto M, Li T, Wandra T, Dharmawan NS, Swastika KI, et al. The first workshop on towards the control of cestode zoonoses in Asia and Africa. Parasite Vectors. 2011;4:114.Google Scholar
- Sarti E, Schantz PM, Plancarte A, Wilson M, Gutierrez IO, Lopez AS, et al. Prevalence and risk factors for Taenia solium taeniasis and cysticercosis in humans and pigs in a village in Morelos, Mexico. Am J Trop Med Hyg. 1992;46:677–85.PubMedGoogle Scholar
- Sarti E, Schantz PM, Plancarte A, Wilson M, Gutierrez OI, Aguilera J, et al. Epidemiological investigation of Taenia solium taeniasis and cysticercosis in a rural village of Michoacan state, Mexico. Trans R Soc Trop Med Hyg. 1994;88:49–52.PubMedGoogle Scholar
- Gilman RH, Gonzalez AE, Llanos-Zavalaga FL, Tsang VCW, Garcia HH, for the Cysticercosis Working Group in Peru. Prevention and control of Taenia solium taeniasis/cysticercosis in Peru. Pathog Glob Health. 2012;106:312–8.PubMed CentralPubMedGoogle Scholar
- Yamasaki H, Matsunaga S, Yamamura K, Chang CC, Kawamura S, Sako Y, et al. Solitary neurocysticercosis caused by Asian genotype of Taenia solium confirmed by mitochondrial DNA analysis. J Clin Microbiol. 2004;42:3891–3.PubMed CentralPubMedGoogle Scholar
- Yamasaki H, Nakao M, Sako Y, Nakaya K, Ito A. Molecular identification of Taenia solium cysticercus genotype in the histopathological specimens. Southeast Asian J Trop Med Public Health. 2005;36 Suppl 4:131–4.PubMedGoogle Scholar
- Ito A, Yamasaki H, Nakao M, Sako Y, Nakaya K, Mamuti W, et al. Review: Echinococcosis and cysticercosis in Asia: evaluation of the modern technology for epidemiological study. Southeast Asian J Trop Med Public Health. 2003;34 Suppl 2:103–7.PubMedGoogle Scholar
- Yamasaki H, Allan JC, Sato MO, Nakao M, Sako Y, Nakaya K, et al. DNA differential diagnosis of taeniasis/cysticercosis by multiplex PCR. J Clin Microbiol. 2004;42:548–53.PubMed CentralPubMedGoogle Scholar
- Hüttner M, Nakao M, Wassermann T, Siefert L, Boomker JDF, Dinkel A, et al. Genetic characterization and phylogenetic position of Echinococcus felidis (Cestoda: Taeniidae) from the African lion. Int J Parasitol. 2008;38:861–8.PubMedGoogle Scholar
- Nkouawa A, Sako Y, Nakao M, Nakaya K, Ito A. Loop-mediated isothermal amplification method for differentiation and rapid detection of Taenia species. J Clin Microbiol. 2009;47:168–74.PubMed CentralPubMedGoogle Scholar
- Nkouawa A, Sako Y, Li T, Chen X, Wandra T, Swastika K, et al. Evaluation of loop-mediated isothermal amplification method using fecal specimens for differential detection of Taenia species. J Clin Microbiol. 2010;48:3350–2.PubMed CentralPubMedGoogle Scholar
- Nkouawa A, Sako Y, Li T, Chen X, Nakao M, Yanagida T, et al. Loop-mediated isothermal amplification method for a differential identification of Taenia tapeworms from human: application to a field survey. Parasitol Int. 2012;61:723–5.PubMedGoogle Scholar
- Yanagida T, Yuzawa I, Joshi DD, Sako Y, Nakao M, Nakaya K, et al. Neurocysticercosis: assessing where the infection was acquired? J Travel Med. 2010;17:206–8.PubMedGoogle Scholar
- Jongwietiwes U, Yanagida T, Ito A, Kline S. Isolated intradural-extramedullary spinal cysticercosis: a case report. J Travel Med. 2011;18:284–7.Google Scholar
- Sako Y, Ito A. Recent advances in serodiagnosis for cysticercosis. Southeast Asian J Trop Med Public Health. 2001;32 Suppl 2:98–104.PubMedGoogle Scholar
- Sako Y, Nakao M, Nakaya K, Yamasaki H, Ito A. Recombinant antigens for serodiagnosis of cysticercosis and echinococcosis. Parasitol Int. 2006;55:s69–73.PubMedGoogle Scholar
- Ito A, Li TY, Chen XW, Long CP, Yanagida T, Nakao M, et al. Mini review on chemotherapy of taeniasis and cysticercosis due to Taenia solium in Asia, and a case report with 20 tapeworms. Trop Biomed. 2013;30:164–73.PubMedGoogle Scholar
- Ito A, Okamoto M, Wandra T, Wibisono H, Anataphruti MT, Waikagul J, et al. Review: Taeniasis and cysticercosis in Asia and the Pacific: present state of knowledge and perspectives. Southeast Asian J Trop Med Public Health. 2005;36 Suppl 4:123–30.PubMedGoogle Scholar
- Ito A, Wandra T, Sato MO, Mamuti W, Xiao N, Sako Y, et al. Review: Towards the international collaboration for detection, surveillance and control of taeniasis/cysticercosis and echinococcosis in Asia and the Pacific. Southeast Asian J Trop Med Public Health. 2006;37 Suppl 3:82–90.PubMedGoogle Scholar
- Ito A, Okamoto M, Wandra T, Wibisono H, Anataphruti MT, Waikagul J, et al. Review: The present situation of taeniasis and cysticercosis in Asia and the Pacific. Southeast Asian J Trop Med Public Health. 2007;38 Suppl 1:119–24.Google Scholar
- Johnson KS, Harrison GB, Lightowlers MW, O’Hoy KL, Cougle WG, Dempster RP, et al. Vaccination against ovine cysticercosis using a defined recombinant antigen. Nature. 1989;338:585–7.PubMedGoogle Scholar
- Lightowlers MW. Eradication of Taenia solium cysticercosis: a role for vaccination of pigs. Int J Parasitol. 2010;40:1183–92.PubMedGoogle Scholar
- Jayashi CM, Gonzalez AE, Neyra RC, Kyngdon CT, Gauci CG, Lightowlers MW. Characterisation of antibody responses in pigs induced by recombinant oncosphere antigens from Taenia solium. Vaccine. 2012;30:7475–80.PubMedGoogle Scholar
- Lightowlers MW. Control of Taenia solium taeniasis/cysticercosis: past practices and new possibilities. Parasitology. 2013;140:1566–77.PubMedGoogle Scholar
- Gonzalez AE, Gauci CG, Barber D, Gilman RH, Tsang VC, Garcia HH, et al. Vaccination of pigs to control human neurocysticercosis. Am J Trop Med Hyg. 2005;72:837–9.PubMedGoogle Scholar
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