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Review Human Toxocariasis Review Human toxocariasis Guangxu Ma, Celia V Holland, Tao Wang, Andreas Hofmann, Chia-Kwung Fan, Rick M Maizels, Peter J Hotez, Robin B Gasser Parasitic nematodes of the genus Toxocara are socioeconomically important zoonotic pathogens. These parasites are Lancet Infect Dis 2018; usually directly transmitted to the human host via the faecal–oral route and can cause toxocariasis and associated 18: e14–24 complications, including allergic and neurological disorders. Although tens of millions of people are estimated to be Published Online exposed to or infected with Toxocara spp, global epidemiological information on the relationship between seropositivity August 3, 2017 http://dx.doi.org/10.1016/ and toxocariasis is limited. Recent findings suggest that the effect of toxocariasis on human health is increasing in S1473-3099(17)30331-6 some countries. Here we review the salient background on Toxocara and biology, summarise key aspects of the Department of Veterinary pathogenesis, diagnosis, and treatment of toxocariasis, describe what is known about its geographic distribution and Biosciences, Melbourne prevalence, and make some recommendations for future research towards the prevention and control of this Veterinary School, The important disease. University of Melbourne, Parkville, VIC, Australia (G Ma MVSc, T Wang PhD, Introduction with contaminated food, water, soil, or utensils. In the Prof R B Gasser DVSc); The first diagnosis of human toxocariasis was the small intestine, the larvae are released from the eggs, Department of Zoology, School detection of Toxocara larvae in enucleated eyes from penetrate the intestinal wall, and travel via the circulatory of Natural Sciences, Trinity College, Dublin, Ireland children with suspected retinoblastoma more than system to various organs, including the lungs, liver, (Prof C V Holland PhD); Griffith 60 years ago.1,2 Histological examination of the retinas of muscles, and CNS. Except in the definitive canid host, Institute for Drug Discovery, these diseased eyes revealed granulomatous lesions that third-stage larvae do not mature but can arrest in Griffith University, Nathan, likely contained Toxocara canis larvae.2 Since then, various development within tissues for many years. Tissue QLD, Australia (A Hofmann Dr rer nat); clinical forms of human toxocariasis have been recognised: infection evokes an inflammatory immune response in Department of Molecular ocular larva migrans, visceral larva migrans, covert or the body that can lead to (usually non-specific) symptoms Parasitology and Tropical common toxocariasis, and neurotoxocariasis.3–5 Despite of disease, such as fever, headaches, coughing, and Diseases, School of Medicine & 3,8,32 Research Center of the clinical recognition of these syndromes and the rising pains. Infective eggs ingested by paratenic or transport International Tropical awareness that human toxocariasis is causing an hosts (eg, mice, rats, rabbits, pigs, cattle, or chickens, and Medicine, College of Medicine, increasing burden to public health, particularly in earthworms or other invertebrates) undergo a similar Taipei Medical University, 33 Taipei, Taiwan subtropical and tropical regions and in disadvantaged fate, with third-stage larvae arresting in tissues. 6–11 (Prof C-K Fan PhD); Wellcome communities in some countries, there are still major Although larvae never develop to adult worms in the Centre for Molecular 7,12–19 gaps in the understanding of this disease. Indeed, intestine of human beings or other paratenic hosts, Parasitology, Institute for evidence from recent investigations suggests that human larvae-infected tissues from paratenic hosts can serve as Infection, Immunity and toxocariasis is seriously neglected because limited food for human beings and definitive hosts, leading to Inflammation, University of Glasgow, Glasgow, UK attention has been paid to its prevention, treatment, and infection or disease. For instance, the consumption of (Prof R M Maizels PhD); Texas 20–22 surveillance and because it is a non-notifiable disease. undercooked or raw liver from infected animals has been Children’s Hospital Center for A major challenge in preventing toxocariasis is the implicated in toxocariasis.34,35 Vaccine Development complexity of infection sources of Toxocara spp and routes Although eliminating or reducing intestinal infections in (Prof P J Hotez PhD); and Department of Pediatrics of transmission, about which still relatively little is known. definitive hosts (dogs and cats) by chemotherapy is probably (Prof P J Hotez) and Department Adult worms of Toxocara spp live in the small intestines of the most efficient way of decreasing environmental of Molecular Virology & various wild or domestic definitive hosts (figure 1). For contamination and subsequent transmission to human Microbiology (Prof P J Hotez), instance, T canis infects canid hosts, including coyotes, beings and other paratenic hosts, the high prevalence of National School of Tropical Medicine, Baylor College of dogs, foxes, and wolves, and Toxocara cati (previously anti-T canis serum antibodies in human beings in many Medicine, Houston, TX, USA Toxocara mystax) and Toxocara malaysiensis infect regions of the world, particularly disadvantaged Correspondence to: 9,23–25 20,22 felids. Related species, such as Toxocara vitulorum, communities, indicates that this approach is not being Prof Robin B Gasser, Department Toxascaris leonina, and Baylisascaris procyonis, infect adequately implemented. In this Review, we introduce of Veterinary Biosciences, various carnivorous or ruminant hosts.9 Human salient aspects of human toxocariasis and Toxocara Melbourne Veterinary School, The University of Melbourne, toxocariasis acquired from cats and Toxoplasma gondii co- infections, emphasise key knowledge gaps, and discuss Parkville, VIC, Australia infection might be more common than previously future prospects and research areas to improve insights [email protected] thought.24,26 Infected definitive hosts, such as dogs and into what is still a neglected parasitic disease of major cats, excrete eggs in the faeces, which then contaminate public health importance. the environment under suitable conditions (humidity and temperature)27–29 where they can remain infective for many Clinical manifestations and disease months or even years. T canis larvae can also undergo In human beings, Toxocara larvae penetrate the intestinal arrested development in the tissues of female canids and mucosa and migrate to liver, lungs, and other organ reactivate during pregnancy to infect pups through both systems (eg, skeletal muscle, heart, brain, and eyes) transplacental and transmammary routes.30,31 by mechanical means and protease digestion.4,5,34 Eggs containing infective third-stage larvae are Migrating larvae are attacked by host immune accidentally ingested by human beings through contact responses, resulting in local inflammation associated www.thelancet.com/infection Vol 18 January 2018 e14 Review impairment associates with migrating or dead larvae and Larvae migrate through resultant immune reactivity against the worm in the eye.5 liver and lung as well as brain, eye, and muscles Blindness can result from severe vitritis, cystoid macular oedema, or tractional retinal detachment.5,38 I Neurotoxocariasis is rare and occurs mainly in middle- aged people.4,39 This syndrome relates to the migration of E J* T canis larvae in CNS and subsequent induction F K of meningitis, encephalitis, cerebral vasculitis, or Transplacental and transmammary myelitis, usually associated with relatively non-specific transmission to puppies; larval A* C 4,39,40 D migration and development; clinical symptoms (eg, fever and headache). C adult male and female worms Possible associations between cerebral toxocariasis and G* mate and reproduce neurodegenerative disorders (eg, seizure, schizophrenia, H cognitive deficits, idiopathic Parkinson’s disease, B J* dementia) have also been discussed in the scientific Environment literature.4,15,16 Cognitive or developmental delays among Figure 1: The life cycle of Toxocara canis, the most common species of Toxocara infecting human beings socioeconomically disadvantaged children who become 41 The life cycle of T canis involves canids (including coyotes, dogs, foxes, wolves) as definitive hosts. infected is of particular concern. Peripheral nervous (A) Eggs of this parasite are released in the faeces of the canid host. (B) Eggs embryonate in the environment and system involvement (radiculitis or inflammation of become infective. (C) After ingestion by this host, infective (third-stage) larvae hatch from the eggs, and larvae cranial nerves or skeletal muscles) is, however, rarely penetrate the intestinal wall. (D) In young dogs (usually <12 weeks), larvae migrate through the liver and lungs to 4 the airways and then get swallowed and make their way to the small intestine, where fourth-stage larvae develop to seen in human beings. adult worms (female and male), mate, and reproduce. (E) In some dogs (usually >12 weeks), oral infection can occur, Covert toxocariasis in children and common but larvae tend to encyst in tissues, where they undergo arrested development. (F) In female dogs, encysted larvae toxocariasis in adults are challenging syndromes to are activated, usually in the last trimester of pregnancy, and undergo transplacental (about 99%) transmission to 3 diagnose clinically because of non-specific symptoms. pups in utero and transmammary transmission (about 1%) to newborn pups. (G) Adult
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