Taeniasis and cysticercosis in Asia: A review with emphasis on molecular approaches and local lifestyles

Acta Tropica 198 (2019) 105075

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Taeniasis and cysticercosis in Asia: A review with emphasis on molecular approaches and local lifestyles

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Akira Itoa, ,1, Tiaoying Lib, Toni Wandrac, Paron Dekumyoyd, Tetsuya Yanagidae, Munehiro Okamotof, Christine M Budkeg,1 a

Department of Parasitology and Laboratory of NTDs, Asahikawa Medical University, Asahikawa, Japan Institute of Parasitic Diseases, Sichuan Centers for Disease Control and Prevention, Chengdu, People’s Republic of China c Directorate of Postgraduate, Sari Mutiara Indonesia University, Medan, Indonesia d Department of Helminthology, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand e Laboratory of Veterinary Parasitology, Joint Faculty of Veterinary Medicine, Yamaguchi University, Yamaguchi, Japan f Center for Human Evolution Modeling Research, Primate Research Institute, Kyoto University, Inuyama, Japan g Department of Veterinary Integrative Biosciences, College of Veterinary Medicine & Biomedical Sciences, Texas A & M University, College Station, Texas, USA b

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Keywords: Taeniasis Cysticercosis Taenia solium Taenia asiatica Taenia saginata Asia

Taeniasis is an important parasitic condition in Asia, especially since all three human-infecting Taenia spp., Taenia solium, Taenia saginata, and Taenia asiatica are found in this region. These three species are believed to be sympatrically distributed, with the largest disease burden found in remote and rural areas where people raise pigs and cattle in a traditional manner. Recent studies revealed that T. asiatica and T. saginata are geneticallyrelated sister species that are not completely reproductively isolated from each other. Current evidence indicates that most T. asiatica adult worms are hybrid-derived descendants. Moving forward, nuclear DNA analysis will be critical in further assessing the species circulating locally. Lifestyle choices, such as the consumption of undercooked meat, are important in maintaining the life cycles of these parasites. In addition, poor hygiene and sanitation, in highly endemic areas, make disease control difficult, resulting in the need for sustainable education programs. An overview of the present situation of taeniasis and cysticercosis in Asia is provided, followed by a discussion of molecular approaches to species assessment and the impact of human lifestyles on parasite transmission.

1. Introduction Taeniasis is an important parasitic condition in Asia, with all three human-infecting Taenia spp., Taenia solium, Taenia saginata, and Taenia asiatica circulating in this region (Ito et al., 2003a). These three species are believed to be sympatrically distributed, with the largest disease burden found in remote areas where the local inhabitants raise pigs and cattle in a traditional manner (Aung and Spelman, 2016; Braae et al., 2018; Flisser et al., 2011; Ito and Budke, 2014; Ito et al., 2003a, 2004, 2014, 2016; Murrell, 2005; Rajshekhar et al., 2003; Singh et al., 2002; Wandra et al., 2015; Willingham et al., 2010; Wu et al., 2017). Recent studies revealed that T. asiatica and T. saginata are genetically-related sister species that are not completely reproductively isolated from each other (Yamane et al., 2013). Current evidence indicates that most T. asiatica adult worms are hybrid-derived descendants. Thus far, only T. solium has been shown to cause cysticercosis in humans (Ito et al.,

2016). Nuclear DNA (nDNA) analysis will be critical in further assessing the species and genetic diversity of T. solium circulating globally (Nakao et al., 2002; Yanagida et al., 2014). Lifestyle choices, such as the consumption of raw or undercooked meat, are important in maintaining the life cycles of these parasites. In addition, poor hygiene and sanitation, in highly endemic areas, make disease control difficult, resulting in the need for sustainable education programs (Sutisna et al., 2019). This review provides a summary of taeniasis and cysticercosis in Asia, followed by a discussion of molecular approaches to Taenia species assessment and the impact of human lifestyles on parasite transmission. 2. An update on Taenia spp. in Asia

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There have been a number of reviews on Taenia spp. in Asia

Corresponding author at: Asahikawa Medical University, Midorigaoka Higashi 2-1-1-1, Asahikawa, 078-8510, Japan. E-mail address: [email protected] (A. Ito). 1 These authors contributed equally for preparation of the MS. https://doi.org/10.1016/j.actatropica.2019.105075 Received 1 March 2019; Received in revised form 14 May 2019; Accepted 5 July 2019 Available online 08 July 2019 0001-706X/ © 2019 Elsevier B.V. All rights reserved.

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Fig. 1. Updated map showing T. solium endemic countries and areas in Asia and the Pacific (modified from Davaasuren et al., 2017). Countries and provinces in red are considered endemic. Areas in bolded red are considered highly endemic. Countries and provinces in orange are expected to be endemic, but data are lacking. No data are available from North Korea, although the country is believed to be endemic (Shen et al., 2007).

rural areas, such as Sichuan and Yunnan provinces (BLSCP website http://boulder-tibet.org/; Li et al., 2006, 2012, 2013, 2019; Meng and Liu, 2016; Openshaw et al., 2018; Raoul et al., 2013), Inner Mongolia (Ikejima et al., 2005), and some areas of eastern China (Liu et al., 2018) (Fig. 1). Infection with T. asiatica appears to be more focally distributed, which may be associated with the high-risk practice of eating uncooked/undercooked pork viscera. Since T. asiatica and T. saginata are morphologically similar, it is important to confirm a diagnosis with either of these species. In recent studies conducted in Muli County, located in Sichuan Province, up to 16% of primary school students were infected with adult worms of up to three Taenia species (T. solium, T. asiatica, and T. saginata) (Li et al., 2019; Openshaw et al., 2018; Li et al., in prep.). Openshaw et al. (2018) hypothesized that the children were likely acquiring taeniasis at home through consumption of raw or undercooked meat, but that the highest risk for acquiring cysticercosis was at school due to poor hygiene practices. Li et al. (in prep.) analyzed the mitochondrial DNA (mtDNA) and nDNA of more than 60 tapeworms obtained in Muli County and confirmed that all of the T. asiatica specimens were hybrid-derived descendants (32/32) and 33% (9/27) of the T. saginata specimens were hybrid-derived descendants. It is hypothesized that T. asiatica and T. saginata were historically maintained in a small closed human and livestock population in Muli, allowing such

published in the last twenty years (Aung and Spelman, 2016; Braae et al., 2018; Ito and Budke, 2014; Ito et al., 2003a, 2004, 2005, 2006a, 2006b, 2014, 2016; Murrell, 2005; Rajshekhar et al., 2003; Singh et al., 2002; Wandra et al., 2015; Willingham et al., 2010; Wu et al., 2017), including three special issues on the topic (Ito et al., 2005, 2006a, 2006b, 2013a). Among the three human Taenia species, T. solium is the only species known to cause cysticercosis in humans. T. solium is believed to be endemic in areas where pigs are free-roaming, meat inspection is insufficient, and sanitation is not optimal (Ahmad et al., 2017; Brizzi et al., 2016; Sah et al., 2017). Fig. 1 shows the present situation of T. solium transmission in Asia. 2.1. China Pork is frequently consumed in China and infection with T. solium has been common historically (Chen et al., 2005; Davaasuren et al., 2017; Ito et al., 2013a; Li et al., 2006, 2012, 2013; Singh et al., 2002; Willingham et al., 2010; Wu et al., 2012; Wu et al., 2017). Due to higher consumption of pork compared to beef, infection with T. solium is more frequent compared to infection with T. saginata or T. asiatica. However, nowadays, infection with T. solium is not nearly as widespread (Chung et al., 2005; Davaasuren et al., 2017; Song et al., 2017; Yang et al., 2014; Xiao et al., 2013) and is only considered endemic in remote and 2

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T. solium cysticercosis is highly endemic in Papua, Indonesia (Margono et al., 2006; Salim et al., 2009). Recent studies comparing antibody responses to T. solium antigens by ELISA in Papua and Bali reinforce this belief (Swastika et al., unpublished). Sustainable education programs aimed at eating well-cooked pork, improving hygiene and latrine use, and rearing pigs in pens, should be strengthened or implemented. Lessons learned in Bali concerning the control of T. solium will likely be valuable for Papua.

hybridization to occur. Due to improved hygiene and food preparation practices, taeniasis is now rare in urban and semi-urban areas of China. However, there is always the risk that individuals from rural areas who are harboring T. solium tapeworms may move to larger cities for employment and, therefore, pose a risk to the local inhabitants. Due to the established history of taeniasis in China, traditional medicines, such as pumpkin seeds and areca nut extract, have long been used as a more natural way to purge intestinal infections. Since these compounds don’t kill the parasites, there is no risk of inducing seizures in an individual who may also have asymptomatic neurocysticercosis (NCC) in addition to taeniasis (Chung and Ko, 1976; Li et al., 2012, 2019; Potemkina, 1966).

2.3.2. North Sumatra T. asiatica taeniasis was historically common on Samosir Island, which is located in Lake Toba in the northern part of Sumatra, Indonesia (Kosin et al., 1971; Suroso et al., 2006; Sutisna et al., 2019; Wandra et al., 2013, 2015). No new cases were identified from 2006 until 2016 (Wandra et al., 2013). However, in 2017, cases were identified in an area used for palm farming between Lake Toba and the capital city of Medan (Zein et al., 2019). During 2017, Zein and his colleagues confirmed 171 Taenia carriers out of 180 suspected carriers. Collected worms were identified as T. asiatica, and were later confirmed to be hybrid-derived descendants of T. asiatica and T. saginata (Yamane et al., 2013). Thus far, all human Taenia tapeworms in North Sumatra appear to be hybrid derived descendants.

2.2. Mongolia In Mongolia, all taeniasis cases confirmed over the past two decades have been due to T. saginata (Davaasuren et al., 2014; Myadagsuren et al., 2007). As of yet, no nDNA analysis has been conducted to determine if T. saginata parasites circulating in Mongolia are pure or hybrids of T. saginata and T. asiatica. However, since T. asiatica has not been identified in Mongolia, it is presumed that the parasites are pure. It has been hypothesized that T. saginata originating in Mongolia may have led to the current circulation of T. saginata in reindeer (Rangifer tarandus) in northern Russia (Konyaev et al., 2017). Studies in the reindeer-rearing Tsaatan ethnic group, located in the Sayan Mountain range, are needed to better understand the historical and current epidemiology in this region. In Mongolia, pork is not as popular as in neighboring China. Most of the country’s pig farms are located in the northern province of Selenge, where pigs are often allowed to roam freely. Only a single imported case of NCC has been reported in Mongolia (see below 4.3). (Davaasuren et al., 2017).

2.4. India, Nepal, and Bhutan In India, more than 70% of the population is vegetarian (Devi et al., 2014). For those that do consume meat, chicken is most commonly eaten followed by goat meat and pork. NCC cases without disseminated cysticercosis (DCC) are common in India (Rajshekhar and Chandy, 2000) and there are several updated reviews on this topic (Ahmad et al., 2017; Singh et al., 2017; Singhi and Suthar, 2015). The risk of NCC is believed to be largely due to consumption of vegetables contaminated with T. solium eggs. However, there are reports of DCC cases (Dev and Abbas, 2019), including in foreign travelers who ate pork while in India (Davaasuren et al., 2017; Kobayashi et al., 2013). T. asiatica, identified by mtDNA analysis, has also been reported in India (Singh et al., 2016) and Nepal (Devleesschauwer et al., 2012). NCC cases occur in Nepal (Amatya and Kimula, 1999; Poudel et al., 2019; Rao et al., 2017; Sah et al., 2017; Yanagida et al., 2010), where the favorite meat source animals are pigs followed by chickens, buffaloes, and goats. DCC cases are believed to be more common than in India, since the local population commonly eats pork (reviews by Ansari et al., 2003; Devleesschauwer et al., 2013; Joshi et al., 2004; Rajshekhar et al., 2003; Singh et al., 2002). There are only a few studies related to NCC conducted in Bhutan or in travelers from Bhutan (Brizzi et al., 2016; O’Neal et al., 2012a, 2012b).

2.3. Indonesia, the Philippines, and Malaysia All three human Taenia spp. are known to be distributed in Indonesia (Aung and Spelman, 2016; Suroso et al., 2006; Wandra et al., 2006a, 2006b, 2013) and the Philippines (Arambulo et al., 1976; Aung and Spelman, 2016; Cruz 1992; de Leon, 2005; Wu et al., 2017). However, there have been few recent studies conducted in the Philippines (Xu et al., 2010). In Malaysia, T. solium data are rare except for from the Orang Asli indigenous communities of the Malay Peninsula and from the state of Sabah in eastern Malaysia, Malaysian Borneo, where the local population is non-Muslim (Chua et al., 2017; Sahu et al., 2016, 2017). All other reports of NCC have been linked to immigration from or travel to other known endemic countries. 2.3.1. Bali and Papua, Indonesia Sutisna et al. (2019) provided a historical overview of Taenia spp. research in Bali. In general, T. saginata taeniasis is still common throughout the island (Sutisna et al., 2019; Wandra et al., 2006a, 2015), whereas T. solium taeniasis is focally distributed in villages positioned along the northeastern slope of Mt. Agung in the Kubu Subdistrict of Karangasem. In this region, pigs roam freely, especially during the dry season, and home slaughter is prevalent (Sudewi et al., 2008; Sutisna et al., 2019; Suweta, 1991; Swastika et al., 2012, 2016, 2017; Wandra et al., 2015). Consumption of uncooked or undercooked pork is also a common practice locally. Thus far, confirmed T. solium tapeworm carriers have been found exclusively from this area (Wandra et al., 2006a, 2013, 2015), indicating the need for a sustainable education program. Pilot programs aimed at children are currently under evaluation (Wulanyani et al., 2019). During the eruption of Mt. Agung in late 2017, most pigs in this region were sold. Studies are needed to determine if the pigs used to repopulate local herds are infected with T. solium and if this rapid sell-off impacted parasite transmission (Sutisna et al., 2019).

2.5. Thailand, Lao PDR, Vietnam, Cambodia, and Myanmar Several studies conducted in Kanchanaburi, Thailand, which is close to the Myanmar border, have revealed that T. solium and T. asiatica are both common in this region (Anantaphruti et al., 2007, 2010). Additional studies conducted in Tak, Thailand, which also borders Myanmar, have shown that T. solium is also circulating in this part of the country (Chaisiri et al., 2017, 2018; McCleery et al., 2015). While studies in Myanmar are lacking, research conducted in refugee villages on the Thai side of the border, indicate that both parasites are likely circulating in eastern Myanmar, including in members of the Karen ethnic group (Chaisiri et al., 2018; McCleery et al., 2015; O’Neal et al., 2012a, 2012b). There are additional endemic areas, especially where Thailand borders Cambodia and Lao PDR (Anantaphruti et al., 2013). A limited number of studies have been conducted in Lao PDR (Ash et al., 2017; Jeon et al., 2013; Okello et al., 2018; Sato et al., 2018), Vietnam (Ng-Nguyen et al., 2018a, 2018b, 2018c; Somers et al., 2006; Van De et al., 2014), and Cambodia (Adenuga et al., 2017). 3

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1989a, 1989b, 1990), and Thailand (Anantaphruti et al., 2007, 2010). Starting in the mid-1980s, several studies were published calling for the Asian Taenia to be considered a new species since, although morphologically similar to T. saginata, these parasites were suspected of having a different intermediate host and different organ tropism (Fan, 1988, 1991; Fan et al., 1988, 1990). However, there was less than a 5% difference found in the mtDNA cytochrome c oxidase subunit 1 gene of T. saginata and the Asian Taenia, making the parasitology community cautious of declaring the existence of a new species (Bowles and McManus, 1994; Zarlenga et al., 1991; reviewed by Simanjuntak et al., 1997). After much debate, T. asiatica is now considered a unique species based on morphological characteristics (Eom and Rim, 1993). Mayr (1996) defined a species as a group of interbreeding natural populations that are reproductively isolated from other such groups. Okamoto et al. (2010) was the first to demonstrate discordance between mtDNA and nDNA profiles in worms collected from Thailand and proposed that this was due to historical hybridization between T. saginata and T. asiatica. Yamane et al. (2012) confirmed that these hybridderived descendants were not only distributed in Thailand, but also in China. Additional studies evaluating nDNA, using the pold gene, revealed that all examined T. asiatica collected in Thailand, China, Indonesia, Lao PDR, and Korea were hybrid-derived descendants of T. saginata and T. asiatica (Sato et al., 2018; Yamane et al., 2013). Based on examination of the pold gene, pure T. asiatica has only been found in the Philippines and Taiwan (Yamane et al., 2013). Hybridization of Taenia in the human intestine is believed to be rare and occurs when there is infection with multiple tapeworm species. Although species identification of human Taenia tapeworms has conventionally relied on mtDNA analysis, it is now becoming apparent that mtDNA alone is not enough to differentiate T. saginata, T. asiatica, and their hybrid-derived descendants. This knowledge will also impact how these parasites’ life cycles are evaluated since intermediate hosts for parasites confirmed as T. saginata by mtDNA analysis may not necessarily be cattle (and buffalo and reindeer) and intermediate hosts for parasites confirmed as T. asiatica by mtDNA analysis may not always be pigs.

2.6. Japan, South Korea, and Taiwan There are several recent reviews on taeniasis and cysticercosis in Japan (Tsuboi et al., 2018; Yamasaki, 2013; Yanagida et al., 2012). Okinawa was endemic for T. solium until the end of World War II (see above 1.6) (Eguchi and Nishiyama, 1930). However, T. solium taeniasis has been rare in Japan other than in Okinawa. Historically, T. solium cysticercosis cases, other than those in Okinawa, represented individuals returning from China after World War II (Nishiyama and Araki, 1999; Okabe, 1972). In the 21 st century, there have been NCC cases confirmed in Japan, with no history of travel to a foreign country (Matsunaga et al., 2002; Yamasaki, 2013). It has been speculated that, at least some of these cases, may have occurred through interaction with a T. solium carrier who acquired the infection elsewhere. Recent outbreaks of T. asiatica taeniasis in Tokyo and the surrounding suburbs are believed to be a combination of autochthonous (Yamasaki et al., 2011; Taniyama et al., 2019; Tsuboi et al., 2018) and imported cases (Namikawa et al., 2018). Eom et al. (2009) reported that two cases in Japan kept in formalin from 1968 and 1996 were identified as T. asiatica. However, no travel history or nationality information was available for either of these cases. Since 2010, approximately 40 T. asiatica taeniasis cases have been confirmed in Tokyo and its suburbs. These cases are believed to have been caused by interaction with foreign T. asiatica carriers employed at pig farms located in the Tokyo suburbs. Addition molecular studies would assist with better characterizing the origin of these infections (Jongwutiwes et al., 2011; Yanagida et al., 2010). Unfortunately, only limited nDNA analysis has been conducted in Japan (Taniyama et al., 2019; Okamoto et al., 2007, 2010; Yamane et al., 2012, 2013) or South Korea (Eom et al., 2009). In South Korea, Cheju island was known to be endemic for T. solium until the 1960s (Chai, 2013). However, local transmission is not believed to be currently occurring. In Taiwan, there are no reports of locally-acquired NCC cases, with all cases suspected to be in immigrants from endemic countries. 3. Molecular approaches on Taenia spp. in Asia The majority of platyhelminths, including cestodes and trematodes, are hermaphrodites. In cestodes, self-fertilization (selfing) occurs when a host is infected with a single worm. This is important when considering population genetics and evolution of tapeworms. Infection with more than one species of tapeworm has also been documented, leading to questions regarding the evolution of currently circulating worms. An example is the Asian Taenia, now recognized as T. asiatica (Eom, 2006; Eom and Rim, 1993). This species resembles, and is difficult to differentiate morphologically from, T. saginata. However, recent studies have shown phylogenetic discordance between mtDNA and nDNA, indicating historical hybridization between T. asiatica and T. saginata (Okamoto et al., 2007, 2010; Yamane et al., 2012, 2013). Therefore, T. asiatica is likely not completely reproductively isolated from T. saginata. Fig. 2 depicts the most recent phylogenetic trees for Taenia spp. based on DNA profiles of nuclear genes for DNA polymerase delta (pold) and phosphoenolpyruvate carboxykinase (pepck) (Terefe et al., 2014).

3.2. Organ tropism in pigs and cattle

3.1. T. asiatica vs T. saginata: Are they independent species or subspecies?

As pigs are the intermediate hosts for both T. asiatica and T. solium, it was initially hypothesized that T. asiatica might cause cysticercosis in humans (Ito, 1992). However, this hypothesis was later discarded after molecular confirmation that T. asiatica and T. saginata are sister species (Hoberg et al., 2000; Ito et al., 2003a). Thus far, all T. asiatica isolates have been found in areas where T. saginata is also circulating. In contrast, T. saginata is often found in areas without T. asiatica (Okamoto et al., 2007, 2010; Sato et al., 2018; Yamane et al., 2012, 2013). To the authors’ knowledge, there have been no confirmed cases of cysticercosis in humans caused by T. asiatica or T. saginata. However, future studies may want to consider evaluating antibody responses to T. asiatica

A study conducting experimental infection of two breeds of pigs and a Holstein calf (susceptible control) with T. saginata (Poland strain) eggs provided information on organ tropism (Fan et al., 1992). Although the calf harbored mature T. saginata cysticerci throughout its body, the pigs developed predominately immature cysticerci exclusively in the liver. Therefore, eggs of both T. asiatica and T. saginata have the ability to produce cysticerci in the liver of pigs. In terms of other species, Fall et al. (1995) experimentally infected baboons (Papio hamadryas) with T. asiatica eggs. However, no cysticerci developed and it was concluded that T. asiatica most likely does not cause cysticercosis in primates, including humans. Additional molecular studies are needed to confirm which Taenia spp. are infecting both livestock and humans in highly endemic areas. 3.3. Does T. asiatica cause cysticercosis?

A long-standing mystery has been that adult taeniid tapeworms expelled from individuals in parts of Asia appeared to be T. saginata, the beef tapeworm, even though the local population ate primarily pork. This phenomenon was noticed in Taiwan (Hsieh, 1960; Huang, 1967; Huang et al., 1966; Oi, 1915; Yokogawa, 1935; Yokogawa and Kobayashi, 1928; reviewed by Fan, 1988, 1991; Fan et al., 1990; Ito et al., 2003a; Simanjuntak et al., 1997), the Philippines (Arambulo et al., 1976; Crutz, 1992; de Leon, 2005), North Sumatra, Indonesia (Kosin et al., 1971), Cheju, Korea (Cho et al., 1967; Fan et al., 1988, 4

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Fig. 2. Nuclear gene-based phylogenetic trees of Taenia spp. (modified from Terefe et al., 2014).

with T. asiatica have not been found. Pigs experimentally infected with T. asiatica produced smaller cysticerci than pigs infected with T. saginata, while cysts in pigs infected with T. asiatica remained viable for a shorter time than cysts due to T. solium (Fan, 1988; Fan et al., 1990). It has been suggested that infections with large numbers (e.g., more than 10) of adult T. asiatica may be rare, while heavy infections with T. solium may be much more common (Anantaphruti, 2013; Ito et al., 2013b; Kusolsuk et al., 2013; Li et al., 2019). Infection with numerous worms suggests that these taeniasis carriers became infected through ingesting pork with large numbers of cysts.

cysticercus antigens in T. asiatica tapeworm carriers. 3.4. Two geographic genotypes of T. solium T. solium has been differentiated into two geographic genotypes, the Asian genotype and the Afro/American genotype (Ito et al., 2002, 2003b; Nakao et al., 2002; Sato et al., 2006, 2011), and mtDNA haplotype network analysis can be used to help determine the origin of infection (Davaasuren et al., 2017; Jongwutiwes et al., 2011; Kobayashi et al., 2013; Yanagida et al., 2010). Michelet et al. (2010) examined 12 T. solium specimens collected from 11 different areas in Madagascar and identified the Asian genotype from 10 areas and the Afro-American genotype from the southwest part of the country. Later, Yanagida et al. (2014) analyzed 109 specimens from the same regions and confirmed that 1) the two mtDNA genotypes were sympatrically distributed in 4 areas, and 2) the mtDNA haplotypes of the Asian genotype were closely related to haplotypes obtained from the Indian subcontinent as shown by Michelet et al. (2010). This study also reported nuclear-mitochondrial discordance in single tapeworms, indicating cross-fertilization between the two genetic lineages of T. solium. It has been hypothesized that both genotypes may be circulating in eastern Africa or beyond due to human migration (Ito et al., 2003b, 2016). Further molecular studies on human Taenia spp. will help shed light on how these parasites historically moved with human and livestock populations (MartinezHernandez et al., 2009; Michelet and Dauga, 2012; Yanagida et al., 2014).

4.2. Infection in rodent models Experimental infection of severe combined immunodeficiency, scid mice via intraperitoneal or subcutaneous injection with in vitro hatched T. asiatica oncospheres obtained from North Sumatra, Indonesia, produced cysticerci of similar size to those produced via injection of T. saginata eggs (Fig. 3) (Chang et al., 2005; Fan et al., 2001; Ito and Ito, 1999; Ito et al., 1997a, 1997b; Nakaya et al., 2006; Wang et al., 1999, 2000). Similar work using immunocompetent C3H/HeN female mice produced fully developed T. asiatica cysticerci that were larger than cysts recovered from pigs (Peng et al., 2009). This study was carried out using parasites from Taiwan that were believed to be pure T. asiatica. The C3H/HeN mice were also infected with eggs orally, indicating that rodents may have the potential of acting as natural intermediate hosts for T. asiatica (Wang et al., 1999). The historical consumption of large rodents in Asia provides an interesting background for this conversation.

4. Intermediate host infection and the impact of lifestyle on human Taenia transmission

4.3. The estimated life spans of the human Taenia species 4.1. Infection in intermediate hosts There have been T. saginata specimens known to survive for over 40 years (Anantaphruti, 2013; Pawlowski and Schultz, 1972; Fan, 1991). There is also experimental evidence that T. asiatica can live for at least 11 years (K. Eom, personal communication). Residents of North Sumatra, Indonesia have anecdotally reported passing gravid proglottids, presumably due to the same infection, for over 40 years (Zein et al.,

Infection of cattle with T. saginata usually produces few cysticerci, which may be due to the propensity of cattle to avoid grazing in areas heavily contaminated with feces (Lawson and Gemmell, 1983). In contrast, infection of swine with T. solium typically results in a large number of cysticerci. To the authors’ knowledge, pigs naturally infected 5

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China in October 2012, and India from July 2014 until March 2015 (see 2.2). After returning from India, he was diagnosed with taeniasis and NCC with DCC. Based on haplotype network analysis, it was determined that he was infected with the Indian haplotype of T. solium. In this case, his infection was also believed to be less than three years in duration (Davaasuren et al., 2017). Only 5%–40% of cases with DCC have active T. solium taeniasis at the time of diagnosis (Davaasuren et al., 2017; Kobayashi et al., 2013; Schantz and Kramer, 1995; Schantz et al., 1998). This is also evidence of the short T. solium life span. T. solium taeniasis cases often report that they realized they were infected when an entire worm or worms were discharged in the feces, with no history of earlier release of individual proglottids. By the time many carriers seek medical attention, they no longer are harboring adult worms. Another approach to evaluating the life span of the three human Taenia spp. may be from evaluating the age distribution of cases in areas where more than one Taenia species is circulating. An example of such a location is southwest Sichuan Province, which makes up part of the Tibetan Plateau (Li et al., 2019; Openshaw et al., 2018). In one study, the research group visited villages and collected stool samples for microscopic examination of Taenia eggs. In an elementary school, 44 Taenia-egg positive students were treated with pumpkin seeds and areca nut extract 8 months after initial diagnosis. Of the 44 original cases, 34 expelled T. solium, T. asiatica or T. saginata tapeworms. No tapeworms were expelled by ten individuals, indicating that they may have cleared their worms within the previous 8 months. Identification of the infecting species by copro-DNA analysis (Nkouawa et al., 2010, 2012) will provide additional data on which species were lost during the 8 months between diagnosis and treatment. In another study, all eight Taenia-egg positive cases expelled T. solium tapeworms following treatment within 3 months after stool collection (Li et al., 2019). Further studies are needed to evaluate not only the infecting species, but also the age of the host. Most tapeworm carriers appear to harbor worms of a similar size even when living in an area with a constant infection pressure. Assessment of the carrier’s age may help with determination of the parasite’s longevity. Factors affecting tapeworm survival, including premunition, concomitant immunity, and the effect of crowding are not well understood. 4.4. The role of lifestyle and culture In many Asian countries where both pork and beef are consumed without religious barriers, pork tends to be the more commonly eaten meat. Pigs are popular livestock to raise due to their high fecundity and the relatively low cost of feeding (Haddon, 1996; Nelson, 1998). Figs. 4a and b illustrate the meaning of the word “house” written using modern Chinese characters, which depicts a pig under a roof. In addition, the word for “bride” or “daughter-in-law” in Chinese (Figs. 4-c) refers to taking care of “the house”, which can be interpreted as also taking care of the family’s pigs. Figs. 4-e and f show a poem using the former Chinese character for the word “house”. The importance of pigs to daily village life is not restricted to Asia, as illustrated by the 1939 picture from Papua New Guinea shown in Fig. 4-g and a more recent photograph from Brazil showing a Guajá woman breastfeeding a pig (Leles et al., 2012). Rearing pigs has been common practice in Asian countries for over 2500 years, with domestication of wild boars occurring in China 9000 years ago (Carr, 2017). The colloquial term “pig toilet” (Fig. 4-d) refers to a relatively simple human latrine located either inside or outside of a house. These types of toilet are still common in rural areas in many Asian countries (Carr, 2017; Ruddle and Zhang, 1988). Traditional practices, such as open defecation (Carr, 2017; Rajshekhar and Chandy, 2000; Ruddle and Zhang, 1988; Singh et al., 2002) and the use of fishpond toilets (a latrine overhanging a fishpond where the human waste is used to provide nutrients for the pond), are still found in some parts of Asia (Ruddle and Zhang, 1988). These defecation styles are

Fig. 3. T. saginata (a), T. asiatica (b) and T. solium (c) cysticerci in NOD/Shi-scid female mice 19 weeks after inoculation with in vitro hatched oncospheres (modified from Nakaya et al., 2006). Cysticerci of T. solium differ from those of T. saginata or T. asiatica, since the invaginated scolex in the intact cyst immediately evaginates (Margono et al., 2003).

2019). The life span of T. solium is believed to be less than 3 years. However, only one experimental study has been conducted to evaluate this parasite’s life span (Yoshino, 1934). Due to the risk of secondary cysticercosis (Lescano et al., 2019; Pray et al., 2017; Sarti et al., 1988, 1992; Schantz et al., 1998), experimental infection with T. solium is dangerous and not recommended. Information about the T. solium life span may be obtainable through evaluation of cases with both taeniasis and cysticercosis. As an example, a Japanese man was diagnosed with taeniasis and NCC with DCC after returning from India. Serology was antibody positive for cysticercosis and microscopy revealed the presence of Taenia eggs. Based on the patient’s date of presentation, it was estimated that the infection was less than three years in duration (Kobayashi et al., 2013). A similar scenario was seen in a Mongolian traveler who visited Inner Mongolia, 6

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Fig. 4. Humans and pigs living together. Typical house in rural Southeast Asia (a). Chinese hieroglyphic characters for the words “house” (depicting a pig under a roof) (b) and “bride” (depicting a woman carrying a house on her back) (c). Funeral statue of a pig toilet (=toilet with pigsty) (China, Eastern Han dynasty 25–220 AD) (from Wikipedia) (Carr, 2017) (d). Former character of “house” showing a pig under the floor of a house (e, f). Photograph of a Chimbu woman from the Eastern Highlands of Papua New Guinea, photographed in 1939 suckling a pig; from The Ian Skinner Collection (g).

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risky for T. solium transmission, since open defecation encourages the presence of free-roaming pigs. Fishpond toilets contaminate water that is often used for washing vegetables, resulting in another potential route for T. solium transmission. The use of fishpond toilets has been hypothesized to be the main reason why NCC cases occur in India where the majority of the population is vegetarian (Rajshekhar and Chandy, 2000).

Some of the work presented in this review was supported by Grantin-Aid for research (1994–2014, B: from 1994 to 1998, A: from 1999 to 2014), Asia-Africa Scientific Platform funds (2006–2008, 2009–2011) from the Japan Society for the Promotion of Science (JSPS), and the Special Coordination Fund for Promoting Science and Technology (2003–2005, 2010–2012), Hokkaido Translational Research Project for Advanced Medicine (2007–2011) to A. Ito from the Ministry of Education, Culture, Sports, Science & Technology in Japan.

5. Perspectives

References

Taeniasis/cysticercosis is considered a Neglected Tropic Disease (NTD) in Asia and elsewhere. These parasites disproportionately impact poor communities and there is a great need for sustainable education programs aimed at these communities. These programs should stress both improved sanitation and food preparation and handling practices. While the distribution of taeniasis is often focally endemic in rural areas, through globalization, there is the opportunity for taeniasis and cysticercosis to occur in areas not considered endemic, including predominately Jewish and Muslim communities (Earnest et al., 1987; Hira et al., 2004; Ito and Budke, 2014; O’Neal and Flecker, 2015; O’Neal et al., 2011; Schantz et al., 1992; Sorvillo et al., 1992; Yanagida et al., 2010, 2012). High-risk populations, for the more severe DCC, include tapeworm carriers, family members, and others who may have more intimate contact with the carriers (Lescano et al., 2019; Pray et al., 2017; Sarti et al., 1988, 1992; Schantz et al., 1993, 1998). Often the first indication that something is wrong is sudden onset of seizures, which may occur even with a solitary NCC lesion (Rajshekhar and Chandy, 2000; Schantz et al., 1992). Moving forward, molecular evaluation of the human Taenia spp. will continue to be critical. As an example, molecular studies can further explore the signals and switches that result in T. solium causing human cysticercosis, while at the same time preventing this outcome in T. saginata and T. asiatica (Olson et al., 2018). The human Taenia spp. continue to have a substantial impact on Asian countries and additional research is needed to better understand their history, epidemiology, and socioeconomic impact.

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