Fatal neural angiostrongyliasis in the Bolivian squirrel monkey (Saimiri boliviensis boliviensis) leading to defining Angiostrongylus cantonensis risk map at a zoo in Australia

Phoebe Rivory; Kresen Pillay; Rogan Lee; David Taylor; Michael P Ward; Jan Šlapeta

doi:10.1016/j.onehlt.2023.100628

Fatal neural angiostrongyliasis in the Bolivian squirrel monkey (Saimiri boliviensis boliviensis) leading to defining Angiostrongylus cantonensis risk map at a zoo in Australia

One Health. 2023 Sep 15:17:100628. doi: 10.1016/j.onehlt.2023.100628. eCollection 2023 Dec.

Authors

Phoebe Rivory¹, Kresen Pillay², Rogan Lee³, David Taylor⁴, Michael P Ward¹, Jan Šlapeta^{1

5}

Affiliations

¹ Sydney School of Veterinary Science, Faculty of Science, The University of Sydney, New South Wales 2006, Australia.
² Sydney Zoo, Bungarribee, New South Wales 2767, Australia.
³ NSW Health Pathology, Centre for Infectious Diseases and Microbiology Lab Services, Level 3 ICPMR, Westmead Hospital, Westmead, New South Wales 2145, Australia.
⁴ Vetnostics, North Ryde, New South Wales 2113, Australia.
⁵ The University of Sydney Institute for Infectious Diseases, New South Wales 2006, Australia.

Abstract

Neural angiostrongyliasis (NA) is a parasitic disease caused by Angiostrongylus cantonensis (rat lungworm). This study presents a case of NA in a captive Bolivian squirrel monkey from a zoo in western Sydney, Australia. The objective was to identify the A. cantonensis cox1 haplotype responsible for the infection and compare its mitochondrial DNA (mtDNA) to known Australian mtDNA. An epidemiological investigation was conducted to assess the risk of infection, focusing on the resident rat population in the zoo. Methods involved trapping rats and collecting rat faeces for Angiostrongylus detection, speciation, and cox1 haplotype confirmation. Various techniques were employed, including necropsy, morphological examination, and molecular methods such as ITS-2 qPCR, cox1 sequencing, and ITS-2 metabarcoding. Cluster analysis of rat faeces distribution and Angiostrongylus detection utilised an equal sampling effort (ESE) approach. Gastropods were collected throughout the study for Angiostrongylus surveillance using a hypersensitive qPCR assay. Results revealed significant clustering of rat faeces near exhibits with fresh food provision and absence of predators. Angiostrongylus-positive faeces were uniformly distributed across the zoo property. Mitochondrial DNA analysis confirmed the presence of the Ac13 haplotype of A. cantonensis in the monkey. Morphology, ITS-2 metabarcoding and partial cox1 sequencing detected only A. cantonensis, with the Ac13 cox1 haplotype predominating. A high prevalence of infection (64%, 9/14) was found in brown rats, with quantification of larvae indicating high shedding rates. Co-infections with both Ac13 and local SYD.1 A. cantonensis cox1 haplotypes were observed. Only three gastropods (all of which were Angiostrongylus-negative) were found in the survey. To minimise the risk of exposure for susceptible species, targeted rodent control was implemented in areas with higher exposure risk. A potential strategy (which requires further exploration) to consider for future zoo design was suggested. This study provides insights into the epidemiology and genetic diversity of A. cantonensis in Australia, emphasising the importance of control measures to prevent future outbreaks.

Keywords: Angiostrongylus cantonensis; Captive primates; Neural angiostrongyliasis; Rat lungworm; cox1; mtDNA.