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Release of lungworm larvae from snails in the environment: potential for alternative transmission pathways.

Giannelli A, Colella V, Abramo F, do Nascimento Ramos RA, Falsone L, Brianti E, Varcasia A, Dantas-Torres F, Knaus M, Fox MT, Otranto D - PLoS Negl Trop Dis (2015)

Bottom Line: The number of snail sections positive for A. abstrusus was higher than those for T. brevior.Results 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.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Veterinary Medicine, University of Bari, Valenzano, Bari, Italy.

ABSTRACT

Background: Gastropod-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 findings: Twenty-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.

Conclusions: Results 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.

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Related in: MedlinePlus

Histopathology: Free larvae of A. abstrusus (21 dpi) in snail foot observed in transverse (hash) and oblique sections (star) in the fibro-muscular tissues.(A); oblique larval section of T. brevior (9 dpi) the subpallial tissue (arrow) (B) (scale bar = 50μm; H&E).
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pntd.0003722.g002: Histopathology: Free larvae of A. abstrusus (21 dpi) in snail foot observed in transverse (hash) and oblique sections (star) in the fibro-muscular tissues.(A); oblique larval section of T. brevior (9 dpi) the subpallial tissue (arrow) (B) (scale bar = 50μm; H&E).

Mentions: During the histological examination, larvae of metastrongyloids were found at different time points, starting from 1 dpi and 9 dpi for A. abstrusus and T. brevior, respectively. Larval transverse sections were recognized as belonging to A. abstrusus or T. brevior according to their mean diameter, detected on round bodies, measuring ~25 and 20 μm, respectively. The number of snail sections positive for A. abstrusus (n = 103) was higher than that for T. brevior (n = 16), with a mean number of 6.4 for the former and 1.0 for the latter species. For both metastrongyloids, larvae were mainly observed in the anterior and posterior parts of fibro-muscular tissue (Fig 2A) of the foot and in the skirt, close to the pedal and oesophageal glands. Larvae were randomly detected in other organs, such as the kidney parenchyma, the wall of the pallial cavity and the connective sub-epithelial layer of the intestine (Fig 2B). Nonetheless, free larvae were rarely found in infected snails at different time points (i.e., at 1, 12 and 21 dpi for A. abstrusus and at 9 dpi for T. brevior). Specimens were localized in the fibro-muscular tissue of the foot, with some of them near vessels, and one specimen in the coelom. All individuals were separated from the surrounding tissue by a thin optically empty space.


Release of lungworm larvae from snails in the environment: potential for alternative transmission pathways.

Giannelli A, Colella V, Abramo F, do Nascimento Ramos RA, Falsone L, Brianti E, Varcasia A, Dantas-Torres F, Knaus M, Fox MT, Otranto D - PLoS Negl Trop Dis (2015)

Histopathology: Free larvae of A. abstrusus (21 dpi) in snail foot observed in transverse (hash) and oblique sections (star) in the fibro-muscular tissues.(A); oblique larval section of T. brevior (9 dpi) the subpallial tissue (arrow) (B) (scale bar = 50μm; H&E).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4401693&req=5

pntd.0003722.g002: Histopathology: Free larvae of A. abstrusus (21 dpi) in snail foot observed in transverse (hash) and oblique sections (star) in the fibro-muscular tissues.(A); oblique larval section of T. brevior (9 dpi) the subpallial tissue (arrow) (B) (scale bar = 50μm; H&E).
Mentions: During the histological examination, larvae of metastrongyloids were found at different time points, starting from 1 dpi and 9 dpi for A. abstrusus and T. brevior, respectively. Larval transverse sections were recognized as belonging to A. abstrusus or T. brevior according to their mean diameter, detected on round bodies, measuring ~25 and 20 μm, respectively. The number of snail sections positive for A. abstrusus (n = 103) was higher than that for T. brevior (n = 16), with a mean number of 6.4 for the former and 1.0 for the latter species. For both metastrongyloids, larvae were mainly observed in the anterior and posterior parts of fibro-muscular tissue (Fig 2A) of the foot and in the skirt, close to the pedal and oesophageal glands. Larvae were randomly detected in other organs, such as the kidney parenchyma, the wall of the pallial cavity and the connective sub-epithelial layer of the intestine (Fig 2B). Nonetheless, free larvae were rarely found in infected snails at different time points (i.e., at 1, 12 and 21 dpi for A. abstrusus and at 9 dpi for T. brevior). Specimens were localized in the fibro-muscular tissue of the foot, with some of them near vessels, and one specimen in the coelom. All individuals were separated from the surrounding tissue by a thin optically empty space.

Bottom Line: The number of snail sections positive for A. abstrusus was higher than those for T. brevior.Results 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.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Veterinary Medicine, University of Bari, Valenzano, Bari, Italy.

ABSTRACT

Background: Gastropod-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 findings: Twenty-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.

Conclusions: Results 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.

Show MeSH
Related in: MedlinePlus