Release of Lungworm Larvae from Snails in the Environment: Potential for Alternative Transmission Pathways

Abstract

BackgroundGastropod-borne parasites may cause debilitating clinical conditions in animals and humans following the consumption of infected intermediate or paratenic hosts. However, the ingestion of fresh vegetables contaminated by snail mucus and/or water has also been proposed as a source of the infection for some zoonotic metastrongyloids (e.g., Angiostrongylus cantonensis). In the meantime, the feline lungworms Aelurostrongylus abstrusus and Troglostrongylus brevior are increasingly spreading among cat populations, along with their gastropod intermediate hosts. The aim of this study was to assess the potential of alternative transmission pathways for A. abstrusus and T. brevior L3 via the mucus of infected Helix aspersa snails and the water where gastropods died. In addition, the histological examination of snail specimens provided information on the larval localization and inflammatory reactions in the intermediate host.Methodology/Principal FindingsTwenty-four specimens of H. aspersa received ~500 L1 of A. abstrusus and T. brevior, and were assigned to six study groups. Snails were subjected to different mechanical and chemical stimuli throughout 20 days in order to elicit the production of mucus. At the end of the study, gastropods were submerged in tap water and the sediment was observed for lungworm larvae for three consecutive days. Finally, snails were artificially digested and recovered larvae were counted and morphologically and molecularly identified. The anatomical localization of A. abstrusus and T. brevior larvae within snail tissues was investigated by histology. L3 were detected in the snail mucus (i.e., 37 A. abstrusus and 19 T. brevior) and in the sediment of submerged specimens (172 A. abstrusus and 39 T. brevior). Following the artificial digestion of H. aspersa snails, a mean number of 127.8 A. abstrusus and 60.3 T. brevior larvae were recovered. The number of snail sections positive for A. abstrusus was higher than those for T. brevior.ConclusionsResults of this study indicate that A. abstrusus and T. brevior infective L3 are shed in the mucus of H. aspersa or in water where infected gastropods had died submerged. Both elimination pathways may represent alternative route(s) of environmental contamination and source of the infection for these nematodes under field conditions and may significantly affect the epidemiology of feline lungworms. Considering that snails may act as intermediate hosts for other metastrongyloid species, the environmental contamination by mucus-released larvae is discussed in a broader context.

Larval development of the cat lungworm Aelurostrongylus abstrusus in the tropical freshwater snail Biomphalaria glabrata

“…This might additionally suggest that in the most suitable intermediate hosts larvae may survive as long as the snails live. On the other hand, we cannot rule out the possibility that the absence of larvae at 28 wpe in B. glabrata Table 1 was due to spontaneous departure of L3 from the snails, as it has been demonstrated for the same snail species infected with Angiostrongylus vasorum, another metastrongyloid nematode (Barcante et al 2003), or in H. aspersa infected with A. abstrusus (Giannelli et al 2015). Due to its high fertility and easy maintenance, Biomphalaria glabrata is not only a naturally occurring intermediate host but also a perfect experimental intermediate host for S. mansoni (DeJong et al 2001;Pointier et al 2005), and proved its suitability for experimental infections also with other metastrongylid parasites such as A. vasorum (Ash, 1970;Barcante et al 2012).…”

The effect of host age and inoculation dose on infection dynamics of Angiostrongylus vasorum in red foxes (Vulpes vulpes)

“…Lastly, we need to emphasize that other means of infection than intake of snails cannot be ruled out. Spontaneous shedding of L3 in mucus from snails was recently demonstrated for several metastrongyloid parasites, including A. vasorum [46, 47]. Such L3 may remain viable for some time in the environment depending on temperature and humidity.…”

Achatina fulica na zona urbana de Maringá-PR: na perspectiva da análise ambiental (Achatina fulica in the urban area of Maringá-PR: from the perspective of environmental analysis)

“…Além da falta de proteção ao manusear a espécie exótica em estudo, há também outros meios de contaminação dos seres humanos pelo Angiostrongylus, por exemplo: a ingestão do animal cru ou mal cozido e também por verduras, legumes e frutas que não foram bem higienizadas, pois o caracol gigante africano libera em seu muco os patógenos (Kramer, Posner e Gosnell, 2018;Waugh et al, 2016;Giannelli et al, 2015).…”