Implementation of Taenia solium control measures in Bali, Indonesia: Survey findings and a historical overview.

Historically, cysticercosis cases caused by infection with the larval stage of the Taenia solium tapeworm have occurred sporadically in Bali, with taeniasis carriers found primarily in villages located in the Kubu subdistrict of Karangasem. As Bali is a well-known tourist destination, living standards are relatively high on the island, except for an area located beneath the northeast slope of the active volcano Mt. Agung (Alt. 3031 m), which includes Kubu. Over the last 30 years, pigs originating from this area have been found with T. solium cysticerci, whereas pigs from other parts of the island have not been shown to be infected. Out of 108 individuals screened via fecal sample examination in Kubu during 2019, 3 cases of T. solium taeniasis (2.8%) were identified. There was no significant difference in taeniasis prevalence from surveys conducted in 2011-2016 (1.0%, 11/1089) (p = 0.123). Out of 110 humans and 140 pigs tested serologically in Kubu during 2019, no cases of cysticercosis were identified. This is in contrast to a seroprevalence of 4.1% (42/1025) in humans during 2011-2016 and a seroprevalence of 13.1% (43/329) in pigs during 2011-2013. Over the last decade, improved drinking water and sanitary systems have been employed in addition to health education targeting primary school children, including emphasis on washing hands before eating and after defecation. This review provides previously unpublished survey data and a historical overview of T. solium infection in Bali and offers guidance on best practices to ensure that remaining pockets of transmission are addressed.

Origin of the pork tapeworm Taenia solium in Bali and Papua, Indonesia.

Global distributions of zoonotic pathogens have been strongly affected by the history of human dispersal and domestication of livestock. The pork tapeworm Taenia solium is distributed worldwide as the cause of neurocysticercosis, one of the most serious neglected tropical diseases. T. solium has been reported in Indonesia but only endemic to restricted areas such as Bali and Papua. Previous studies indicated the distinctiveness of a mitochondrial haplotype confirmed in Papua, but only one isolate has been examined to date. In this study, genetic characterization of T. solium and pigs in Bali and Papua was conducted to clarify the distributional history of the parasite. Mitochondrial haplotype network analysis clearly showed that Indonesian T. solium comprises a unique haplogroup which was the first to diverge among Asian genotypes, indicating its single origin and the fact that it was not introduced in the recent past from other area in Asia in which it is endemic. Although phylogenetic analysis based on the mitochondrial D-loop revealed multiple origins of pigs in Bali and Papua, the majority of pigs belonged to the Pacific Clade, which is widely dispersed throughout the Island Southeast Asia (ISEA) and Oceania due to Neolithic human dispersal. Given the results of our network analysis, it is likely that the Pacific Clade pigs played a key role in the dispersal of T. solium. The data suggest that T. solium was introduced from mainland Asia into Western Indonesia, including Bali, by modern humans in the late Pleistocene, or in the early to middle Holocene along with the Pacific Clade pigs. Introduction into New Guinea most likely occurred in the late Holocene through the spread of Pacific Clade pigs. Over time, T. solium has been eradicated from most of Indonesia through the middle to modern ages owing to religious and cultural practices.

A seroepidemiological study of bovine cysticercosis in Bali and Nusa Tenggara, Indonesia.

BACKGROUND AND AIM: Taenia saginata hazardously affects human and animal health. The distribution of this disease is found almost all over the world. The study aimed to obtain epidemiological information concerning prevalence and the distribution of bovine cysticercosis in Bali and Nusa Tenggara, Indonesia. MATERIALS AND METHODS: A total of 267 community-owned Bali cattle serum samples from the provinces of Bali, West Nusa Tenggara, and East Nusa Tenggara were examined. The study was conducted by examining the serum of Bali cattle using enzyme-linked immunosorbent assay technique. Risk factors related to cysticercosis that analyzed were sex, breeding type, age, physical condition, source of drinking water, pen condition, and latrine availability. RESULTS: Seven of 91 Bali cattle sera from all regencies/cities in Bali showed a positive result. Those positive sera were originated from Buleleng (1), Gianyar (2), Denpasar (2), and Klungkung (2). Meanwhile, four of 92 Bali cattle sera from West Nusa Tenggara and seven of 84 from East Nusa Tenggara occurred antibodies against T. saginata. We identified that two risk factors that influence the incidence of T. saginata infection in Bali cattle in Bali were the sex and the cattle breeding type. CONCLUSION: Through this research can be made a map of bovine cysticercosis in Bali cattle in Bali and Nusa Tenggara region. By mapping the disease, it is recommended that the animal health officers should be more accurate when conducting postmortem examination, especially on cattle from a positive region.

Neurocysticercosis cases identified at Sanglah Hospital, Bali, Indonesia from 2014 to 2018.

Neurocysticercosis (NCC) was first reported in the province of Bali, Indonesia in 1975. Since this time, sporadic cases have been reported annually. This study reports information on 29 NCC cases (20 males and 9 females) admitted to a referral hospital in Denpasar, Bali from 2014 until 2018. Twenty-four cases were from Bali, 2 were from the province of East Nusa Tenggara, and 3 were from the Democratic Republic of Timor-Leste. Mean patient age was 37.2 years and 69.0% (20/29) were male. Epileptic seizures were the most common clinical manifestation (65.5%, 19/29). Serology (ELISA) was used in 14 cases (48.2%, 14/29), but only 6 cases, including one case with an inactive calcified lesion, were positive (42.9%, 6/14). Two cases underwent surgical resection after their lesions were initially misdiagnosed as brain tumors. These hospital-based findings are discussed along with the present status of NCC in Bali.

A preliminary study to assess the use of a "Snakes and Ladders" board game in improving the knowledge of elementary school children about taeniasis.

The Snakes and Ladders board game was modified so that it contained information on taeniasis. A quantitative approach was used to evaluate if elementary school children were able to answer correctly more questions about Taenia saginata and Taenia solium transmission and control after playing the game compared to before playing the game. In total, 78 children (9-12 years of age) from Dukuh elementary school in Karangasem District, Bali, Indonesia, were evaluated. The children were asked to complete a pre- and post-test assessment before and after playing the game a single time. Overall proportion of correct answers was 40.3% before playing the game and 58.8% after playing the game. There was a greater proportion of correct answers for questions pertaining to the transmission route for T. saginata (p < 0.001) and T. solium (p < 0.001), human infection type with T. solium (p = 0.035) and T. saginata (p < 0.001), and animal infection type with T. solium or T. saginata (p < 0.001) after playing the game compared to before playing the game. However, there was no significant difference for any question for the youngest grade level. Use of this popular board game appears to be a promising tool for teaching older (10 years of age and above) children about taeniasis in endemic areas.

Identification of a previously unidentified endemic region for taeniasis in North Sumatra, Indonesia.

In North Sumatra, Indonesia, taeniasis has previously been reported solely from Samosir Island located in Lake Toba. In 2014, however, three individuals were identified with taeniasis after voluntarily reporting for treatment, stimulating a subsequent investigation conducted in 2017. This investigation indicated that a previously unidentified endemic area exists in Simalungun District. Molecular analysis showed the worms to be hybrid-derived descendants of Taenia asiatica and Taenia saginata, which is consistent with specimens identified previously from Samosir Island.

Towards a cysticercosis-free tropical resort island: A historical overview of taeniasis/cysticercosis in Bali.

Taeniasis and cysticercosis are known to be endemic in several Indonesian islands, although relatively little recent epidemiological data are available. As most Indonesian people are Muslims, taeniasis/cysticercosis caused by the pork tapeworm, Taenia solium, has a restricted presence in non-Muslim societies and is endemic only among some Hindu communities on the island of Bali. Bali has long been known to be endemic for taeniasis/cysticercosis; almost a century ago levels of cysticercosis of 20-30% were described in cattle and 2-3% in pigs. Few studies of taeniasis/cysticercosis were undertaken in Bali prior to a series of research programs commenced since the 1990s. Both Taenia saginata and T. solium continue to be endemic in Bali. Molecular studies have revealed that all T. saginata-like tapeworms detected in Bali are T. saginata. No evidence has been found for the presence of Taenia asiatica in Bali. Economic, sanitary and education improvements across much of the island over the past decades have been associated with a decline in the amount of transmission of T. solium such that the parasite now seems to be restricted to the eastern part of the island, a small area on the northeastern slope of Mt. Agung, the highest mountain in Bali. The living environment including sanitation and hygiene condition in this endemic area remains relatively poor especially during the half-year dry season, and pigs continue to roam freely. In this review, historical records and ongoing projects towards elimination of taeniasis/cysticercosis in Bali are reviewed to provide a better understanding of the present situation of taeniasis/cysticercosis in Bali towards a future, cysticercosis-free tropical resort island.

Taeniasis caused by Taenia saginata in Gianyar town and Taenia solium in Karangasem villages of Bali, Indonesia, 2011-2016: How to detect tapeworm carriers, anamnesis or microscopy?

From January 2011 until September 2016, screening of taeniasis carriers was carried out in a town in Gianyar District (Taenia saginata) and in villages which consisted of several Banjars (the smallest community units) on the eastern slope of Mt. Agung, Karangasem District (Taenia solium) in Bali, Indonesia. Fecal samples from all community members who chose to participate were examined microscopically for detection of taeniid eggs each person completedwith a questionnaire to determine if they had seen whitish, noodle-like proglottids (anamnesis) in their feces. Members with egg positive feces, and those with anamnesis, were treated with niclosamide (Yomesan®, Bayer). A total of 39T. saginata tapeworm carriers were confirmed in Gianyar after deworming based on anamnesis (100%, 39/39). Only three of them (3/39, 7.7%) and 3/173 participants (1.7%) were identified by fecal microscopy. In contrast, 20T. solium carriers including one migrated to Gianyar were confirmed from 12 patients with eggs in their feces and from another 8 persons of 12 persons suspected to be infected due anamnesis only (8/12,66.7%) in Karangasem. The majority of carriers (12/20, 60.0%) identified by microscopy included 4 (33.3%) and 8 (66.7%) carriers confirmed microscopically with and without anamnesis, respectively. The prevalence rate was 12/1090 (1.10%) of participants. The results indicate that anamnesis is reliable for detection of T. saginata carriers, whereas it is not so reliable for detection of T. solium taeniasis (8/12, 66.7%) and that microscopy is more informative than anamnesis for T. solium. Eggs were detected more frequently in T. solium carriers (4/12, 33.3%) than in patients infected with T. saginata (3/39, 7.7%). T. solium carriers have so far been confirmed from nine of 13 Banjars examined in Karangasem. This study reveals that anamnesis is highly useful for screening of T. saginata carriers, whereas microscopy is a more valuable tool for detection of T. solium carriers.

Swine cysticercosis in the Karangasem district of Bali, Indonesia: An evaluation of serological screening methods.

A serological assessment was undertaken on pigs from the Kubu and Abang sub-districts of Karangasem on the island of Bali, Indonesia, where earlier studies had detected patients with cysticercosis. Antigens purified from Taenia solium cyst fluid by cation-exchange chromatography were used to evaluate antibody responses in the pigs and the serological tests were also evaluated using sera from pigs experimentally infected with T. solium eggs. A total of 392 serum samples from naturally exposed pigs were tested using an ELISA that could be read based on both a colour change perceptible by the naked eye and an ELISA based on absorbance values. Twenty six (6.6%) pigs were found seropositive by the naked-eye ELISA and were categorized into three groups: strongly positive (absorbance values >0.8, n=6), moderately positive (absorbance values between 0.2 and 0.8, n=7), and weakly positive (absorbance values <0.2, n=13). Necropsies performed on 11 strongly and moderately positive pigs revealed that six strongly positive pigs were infected either solely with T. solium cysticerci (n=3), or co-infected with both T. solium and Taenia hydatigena (n=3). Four moderately positive pigs were infected solely with T. hydatigena. No cysticerci were found in one pig that was moderately positive by the naked-eye ELISA. Two experimentally infected pigs became antibody positive by 6 weeks post-infection, whereas eight control pigs remained negative. An additional 60 pigs slaughtered at authorized abattoirs on Bali were tested using the same ELISA. All 60 pigs were seronegative with no evidence of Taenia infection at necropsy. The results confirm the presence of porcine cysticercosis on Bali and, while the serological responses seen in T. solium infected animals were much stronger than those infected with T. hydatigena, the diagnostic antigens are clearly not species specific. Further studies are necessary to confirm if it is possible to draw a cut off line for differentiation of pig infected with T. solium from those infected with T. hydatigena.

The present situation and towards the prevention and control of neurocysticercosis on the tropical island, Bali, Indonesia.

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.

Taeniases and cysticercosis in Indonesia: past and present situations.

The main aim of this study is to overview the past and present situations of human taeniases and cysticercosis in Indonesia and including future perspectives. Through joint projects from 1996, we have confirmed the occurrence of Taenia saginata (beef tapeworm) in Bali, of Taenia solium (pork tapeworm) mainly in Papua and sporadically in Bali, and of Taenia asiatica in North Sumatra. These taeniases were caused through eating uncooked pork and pig viscera for T. solium and T. asiatica, respectively, and beef for T. saginata. The distribution of these tapeworms in Indonesia is basically highly restricted by the traditional cultural and religious backgrounds in each island. T. saginata is relatively common in Bali although people consume pork 'lawar' more than beef 'lawar'. Taeniases due to T. saginata or T. asiatica and T. solium and cysticercosis due to T. solium have also been sporadically reported in some other islands. Among these species, T. solium is exceptional since humans can be infected not only by larval stages (cysticerci) in pork but also by eggs released from human tapeworm carriers. Cysticercosis has been confirmed in Indonesia in humans, pigs and even dogs.

An ocular cysticercosis in Bali, Indonesia caused by Taenia solium Asian genotype.

An ocular cysticercosis case of a nine-year-old Balinese girl in Indonesia is reported. She presented with redness and pain in the left eye and showed a cysticercus in the anterior chamber in December 2010. Morphological feature of the cysticercus removed from the anterior chamber indicated that it was an immature cysticercus of Taenia species with no hooklets. However, mitochondrial DNA analysis using a piece of histopathological specimen revealed it a cysticercus of Taenia solium Asian genotype. Serology by immunoblot and ELISA highly specific to cysticercosis was negative.

The first workshop towards the control of cestode zoonoses in Asia and Africa.

The first workshop towards the control of cestode zoonoses in Asia and Africa was held in Asahikawa Medical University, Japan on 15 and 16 Feb 2011. This meeting was fully supported by the Asian Science and Technology Strategic Cooperation Promotion Programs sponsored by the Special Coordination Funds for Promoting Science and Technology, the Ministry of Education Japan (MEXT) for 3 years from 2010 to Akira Ito. A total of 24 researchers from 9 countries joined together and discussed the present situation and problems towards the control of cestode zoonoses. As the meeting was simultaneously for the establishment of joint international, either bilateral or multilateral collaboration projects, the main purposes were directed to 1) how to detect taeniasis/cysticercosis infected patients, 2) how to differentiate Taenia solium from two other human Taenia species, T. saginata and T. asiatica, 3) how to evaluate T. asiatica based on the evidence of hybrid and hybrid-derived adult tapeworms from Thailand and China, 4) how to evaluate T. solium and T. hyaenae and other Taenia species from the wild animals in Ethiopia, and 5) how to detect echinococcosis patients and 6) how to differentiate Echinococcus species worldwide. Such important topics are summarized in this meeting report.