Abstract

Snails are essential to complete the life cycle of the metastrongylid nematode Angiostrongylus cantonensis, the causative agent of infections in domestic and wild animals, mainly rodents, and also of neural angiostrongyliasis or eosinophilic meningitis in humans. There are many reports of mollusks that can act as intermediate hosts of this parasite, especially freshwater snails and the African giant Achatina fulica. The terrestrial gastropod Bulimulus tenuissimus is widely distributed in Brazil and other species of the same genus occur in Brazil and other countries, overlapping regions in which there are reports of the occurrence of A. cantonensis and angiostrongyliasis. In spite of this, there are no records in the literature of this species performing the role of intermediate host to A. cantonensis. The present study analyzed the experimental infection with first-stage larvae of A. cantonensis, under laboratory conditions, of B. tenuissimus, by using histology and electron microscopy techniques. Three weeks after exposure to L1 larvae, it was possible to recover L3 larvae in small numbers from the infected snails. Developing larvae were observed in the cephalopedal mass (foot), ovotestis, and mantle tissues, being located inside a granulomatous structure composed of hemocyte infiltration, but there was no calcium or collagen deposition in these structures in significant amounts. In the third week post exposure, it was possible observe a sheath around the developing larvae. The infected snails presented reduction in the fibrous muscular tissue in the foot region, loss of the acinar organization in the digestive gland, with increase of amorphous material inside the acini and loss of epithelial pattern of nuclear organization in the acinar cells. However, the ovotestis seemed unaffected by the infection, since there was a large number of developing oocytes and spermatozoa in different stages of formation. The digestion of infected snails allows us the third-stage recovery rate of 17.25%, at 14 days post exposure to the L1. These L3 recovered from B. tenuissimus were used to infect rats experimentally, and 43 days post infection first-stage (L1) larvae of A. cantonensis were recovered from fresh feces. The results presented constituted the first report of the role of B. tenuissimus as an experimental intermediate host to A. cantonensis and shed some light on a possible problem, since the overlapping distribution of B. tenuissimus and A. cantonensis in Brazil and other countries where different species of Bulimulus occur enables the establishment and maintenance of the life cycle of this parasite in nature, with wild rodents as reservoirs, acting as a source of infection to humans, causing neural angiostrongyliasis.

Highlights

  • Angiostrongyliasis has been recorded in many countries since the main species indicated as causative agents of human disease, Angiostrongylus cantonensis (Chen, 1935) and Angiostrongylus costaricensis Morera and Céspedes (1971) were described. Nomura and Lin (1945) first recorded a case of human eosinophilic meningitis in Taiwan, in a 15-year-old boy who had 10 A. cantonensis worms in his cerebrospinal fluid (CSF) and died because of the infection

  • The L3 larvae recovery rate three weeks after exposure was 17.25%, in relation to the initial number of 1,200 L1 larvae used to infect the snails, but the recovery of L3 larvae showed that A. cantonensis is able to infect B. tenuissimus and complete its life cycle from L1 until L3, the infective stage to the vertebrate definitive host

  • The results obtained in the present study represent the first report of B. tenuissimus as an experimental intermediate host of A. cantonensis

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Summary

Introduction

Angiostrongyliasis has been recorded in many countries since the main species indicated as causative agents of human disease, Angiostrongylus cantonensis (Chen, 1935) and Angiostrongylus costaricensis Morera and Céspedes (1971) were described. Nomura and Lin (1945) first recorded a case of human eosinophilic meningitis in Taiwan, in a 15-year-old boy who had 10 A. cantonensis worms in his cerebrospinal fluid (CSF) and died because of the infection. Angiostrongyliasis has been recorded in many countries since the main species indicated as causative agents of human disease, Angiostrongylus cantonensis (Chen, 1935) and Angiostrongylus costaricensis Morera and Céspedes (1971) were described. Nomura and Lin (1945) first recorded a case of human eosinophilic meningitis in Taiwan, in a 15-year-old boy who had 10 A. cantonensis worms in his cerebrospinal fluid (CSF) and died because of the infection. Reports can be found of the parasite infecting humans and other mammals in 19 countries (Thailand, China (including Taiwan and Hong Kong), Tahiti, French Polynesia, United States, Cuba, New Caledonia, Japan, Australia, Vanuatu, India, Vietnam, Malaysia, Mayotte, Réunion Island-France, Sri Lanka, Cambodia, Samoa, Fiji, Germany, Jamaica, Costa Rica, Indonesia, Belgium, Italy, Côte d’Ivoire, New Zealand, Papua New Guinea, Switzerland, and United Kingdom (Puthiyakunnon and Chen, 2015; Prociv et al, 2000). Reports can be found of the parasite infecting humans and other mammals in 19 countries (Thailand, China (including Taiwan and Hong Kong), Tahiti, French Polynesia, United States, Cuba, New Caledonia, Japan, Australia, Vanuatu, India, Vietnam, Malaysia, Mayotte, Réunion Island-France, Sri Lanka, Cambodia, Samoa, Fiji, Germany, Jamaica, Costa Rica, Indonesia, Belgium, Italy, Côte d’Ivoire, New Zealand, Papua New Guinea, Switzerland, and United Kingdom (Puthiyakunnon and Chen, 2015; Prociv et al, 2000). Flerlage et al (2017) reported a case of A. cantonensis-meningoencephalitis in a 12-month-old boy in Tennessee, USA, who had not traveled outside of southwestern Tennessee or northwestern Mississippi, showing the existence and maintenance of the parasite’s life cycle in loco. Puthiyakunnon and Chen (2015) reported that until 2012, there were about 3,161 cases of human angiostrongyliasis documented globally, but this number is certainly underestimated, because many cases go unreported due to lack of awareness of this parasite within the medical community. Morassutti et al (2014) drew attention to neural angiostrongyliasis in Brazil as an emerging disease, which requires more careful investigation by researchers and health professionals

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