REVIEW Neglected zoonotic helminths: Hymenolepis nana, Echinococcus canadensis and Ancylostoma ceylanicum R. C. A. Thompson School of Veterinary and Life Sciences, Murdoch University, Murdoch, WA, Australia Abstract The majority of helminth parasites that are considered by WHO to be the cause of ‘neglected diseases’ are zoonotic. In terms of their impact on human health, the role of animal reservoirs and polyparasitism are both emerging issues in understanding the epidemiology of a number of these zoonoses. As such, Hymenolepis (Rodentolepis) nana, Echinococcus canadensis and Ancylostoma ceylanicum all qualify for consideration. They have been neglected and there is increasing evidence that all three parasite infections deserve more attention in terms of their impact on public health as well as their control. Clinical Microbiology and Infection © 2015 European Society of Clinical Microbiology and Infectious Diseases. Published by Elsevier Ltd. All rights reserved. Keywords: Ancylostoma ceylanicum, Echinococcus canadensis, Hymenolepis(Rodentolepis) nana, neglected diseases, zoonoses Article published online: 14 January 2015 the small intestine of humans, attaching to the mucosal surface R. C. A. Thompson, Parasitology, School of Veterinary and Life Sci- between the villi. As the worm matures sexually, the terminal ences, Murdoch University, Murdoch, WA, 6150, Australia E-mail: [email protected] proglottids (‘segments’) become gravid, detach and disintegrate in the gut releasing the eggs, which are passed in the faeces. The eggs are immediately infective but can survive in the environ- ment for up to 2 weeks [2]. As with most cestodes, the life Introduction cycle includes a metacestode, the larval cysticercoid, but atyp- ically an intermediate host is not an obligatory requirement in Helminth parasites feature prominently in WHO’s list of the life cycle. If humans ingest the eggs, they hatch in the small neglected diseases (http://www.who.int/neglected_diseases/ intestine releasing a motile embryo, the oncosphere, which diseases/en/). Most are zoonotic with animal reservoirs play- invades a villus and develops into the larval cysticercoid in ing a role in their epidemiology and are a major impediment to approximately 4 days. The cysticercoid then ruptures, control (Table 1). In this article, I have chosen three zoonotic completely destroying the villus it occupies, attaches to the helminth infections that, as well as falling under the ‘neglected’ mucosal surface and develops into the adult tapeworm, which umbrella, require re-evaluation in view of emerging issues reaches patency in 4 weeks [1]. Humans can therefore be both relating to the epidemiology and impact on public health of the definitive and intermediate hosts (Fig. 2). infections they cause. A true indirect cycle involving an arthropod, usually small beetles such as Tribolium that commonly contaminate flour or cereal, also occurs [1,2]. The beetles become infected by Hymenolepis nana ingesting eggs from the environment, and cysticercoids subse- quently develop in their body cavity. The accidental ingestion of Hymenolepis (Rodentolepis) nana is the most common cestode of infected beetles by humans, usually with contaminated food, will humans, particularly in young children [1–3]. It is often referred lead to the development of the adult tapeworm. The frequency to as the ‘dwarf tapeworm’ due to its small size, 2–4 cm long of food-borne transmission is not known but is likely to vary and only 1 mm wide [1] (Fig. 1). The adult tapeworm parasitizes between endemic foci. A recent report considered that the Clin Microbiol Infect 2015; 21: 426–432 Clinical Microbiology and Infection © 2015 European Society of Clinical Microbiology and Infectious Diseases. Published by Elsevier Ltd. All rightsreserved http://dx.doi.org/10.1016/j.cmi.2015.01.004 CMI Thompson Neglected zoonotic helminths 427 TABLE 1. Neglected zoonotic helminths Disease Causative agent Life cycle Definitive hosts Intermediate hosts/ Geographical distribution/no. of cases Risk factors vectors Cysticercosis/ Taenia spp. Indirect Humans Cattle, pigs, (Humans Global but most prevalent in South Communities with free-roaming Taeniasis for T. solium) America, Asia, South-East Asia, Africa/ pigs, poor sanitation and highly variable; prevalence up to 20% in unregulated animal slaughter some endemic areas Dracunculiasis Dracunculus Indirect Humans, occ. Copepod crustaceans Now restricted to a few countries in Communities with poor water medinensis other mammals Africa quality especially dogs Food-borne Clonorchis*, Indirect Humans and other Snails (and freshwater Focal—South-East Asia, China, former Eating uncooked fish and other trematodiases Opisthorchis*, mammals fish*) Soviet Union, Middle East, western aquatic products Paragonimus*, Europe, Africa/2–35 million Fasciola Hydatid disease/ Echinococcus spp. Indirect Carnivores Non-carnivorous Global/~ 1 million Ingestion of infective stages echinococcosis mammals and from the environment or humans contact with definitive hosts Lymphatic Brugia spp. Indirect Humans, cats Mosquitoes South and South-East Asia/> 10 million Exposure to mosquito vectors filariasis Schistosomiasis Schistosoma spp. Indirect Humans and other Snails Africa, Middle East, Caribbean, South Children exposed to mammals America, China, South-East Asia/ contaminated freshwater > 200 million Soil-transmitted Ancylostoma Direct Dogs, cats, N/A Asia, South-East Asia, Australia, South Poor sanitation, promiscuous helminthiases ceylanicum humans Africa/5–40% in endemic communities defecation Hymenolepiasis Hymenolepis nana Direct and Humans and Beetles Young children living in areas indirect rodents with poor hygiene and sanitation Trichinellosis Trichinella spp. Direct Mammals N/A Global Eating meat that has not been including inspected by regulatory humans authorities, e.g. hunting *Only Clonorchis, Opisthorchis and Paragonimus include freshwater fish in their life cycles. Information from references [4,24,29,33,34,40,49] and WHO (http://www.who.int/neglected_diseases/diseases/en/). proportion of cases attributable to food-borne infection is transmission may be greater in poor, high-density urban envi- negligible [4], although no data are available to support this ronments and four recent reports found mice and rats in urban view. In addition to humans, mice can also be definitive hosts of environments of Rio de Janeiro, Brazil, Uttarakhand in India, H. nana and so act as reservoir hosts. northern England and Kuala Lumpur, Malaysia, to be commonly Epidemiological evidence suggests that direct human-to- infected with H. nana [10–13]. Molecular evidence is equivocal, human transmission is the most common route of infection suggesting that there may be two strains of H. nana that are with H. nana, particularly in environments where the frequency maintained in zoonotic and non-zoonotic cycles but this re- of such transmission is likely to be high due to poor hygiene and mains to be determined. Macnish et al. [5] suggested that iso- inadequate sanitation [2,5–7]. However, it is still considered a lates of H. nana in Australia actually exist as two cryptic or zoonosis because infected commensal/synanthropic rodents, sibling (morphologically identical, but genetically different) such as mice and rats, and arthropod intermediate hosts species, based on a sequence divergence of 5% in the represent a reservoir of infection that may vary in importance in different environments [2,5,8,9]. The risk of zoonotic FIG. 2. Illustration showing direct development of adult Hymenolepis nana following ingestion of cysticercoid or indirect with mucosal FIG. 1. Adult tapeworm of Hymenolepis nana. development of cysticercoid following ingestion of egg. Clinical Microbiology and Infection © 2015 European Society of Clinical Microbiology and Infectious Diseases. Published by Elsevier Ltd. All rights reserved, CMI, 21,426–432 428 Clinical Microbiology and Infection, Volume 21 Number 5, May 2015 CMI mitochondrial cytochrome c oxidase 1 gene. Hymenolepis nana TABLE 2. Currently recognized species of Echinococcus has also been shown to infect lower primates and in such cases, Main Known humans appear to be the source of infection in a ‘reverse intermediate definitive Infectivity Species hosts hosts to humans zoonosis’ scenario [14]. Infections in humans with H. nana are ubiquitous, particularly Echinococcus granulosus Sheep, camels, Dog, fox, dingo, Yes macropod jackal and hyena in children in developing countries [15–20]. Mono-infections marsupials Echinococcus equinus Horses Dog Probably not are rare and in published surveys H. nana is usually reported Echinococcus ortleppi Cattle Dog Yes Echinococcus canadensis Cervids Wolves, dog Yes as co-occurring with a number of other enteric parasites, Echinococcus intermedius Camels, pigs, Dog Yes sheep particularly in community situations where the frequency of Echinococcus felidis Warthog Lion ? – Echinococcus multilocularis Rodents Fox, dog, cat, Yes faecal oral transmission is likely to be high [21,22]. Giardia, wolf, racoon-dog, coyote Entamoeba coli, Blastocystis, Chilomastix as well as species of Echinococcus shiquicus Pika Tibetan fox ? gastrointestinal/soil-transmitted helminth, are the most com- Echinococcus vogeli Rodents Bush dog Yes Echinococcus oligarthrus Rodents Wild felids Yes mon co-habiting parasites in such polyparasitic infections Data from reference [30]. [21–27]. Chronic G. duodenalis infection is well recognized as contributing to poor growth and development (‘failure