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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: Inflammatory response to A. abstrusus in the H. aspersa.Cell-poor granuloma formation with vacuolated amebocytes at 3dpi. (A); cell-rich granuloma formation at 9 dpi (B); small necrotic granuloma at 15 dpi (C); fibroblast-like reaction at 27 dpi (D) (scale bar = 50μm; H&E).
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pntd.0003722.g003: Histopathology: Inflammatory response to A. abstrusus in the H. aspersa.Cell-poor granuloma formation with vacuolated amebocytes at 3dpi. (A); cell-rich granuloma formation at 9 dpi (B); small necrotic granuloma at 15 dpi (C); fibroblast-like reaction at 27 dpi (D) (scale bar = 50μm; H&E).

Mentions: The tissue response to nematode larvae included: i) cell-poor (3 dpi; Fig 3A) and cell-rich (9 dpi; Fig 3B) granuloma-like formations, composed of non-vacuolated or vacuolated epithelioid amebocytes; ii) small necrotic granulomas (15 dpi; Fig 3C); iii) fibroblast-like encapsulations (27 dpi; Fig 3D). The severity of the inflammatory pattern ranged from mild reactions, featured by vessel dilatation, mild increase of the cellularity and small granulomas (Fig 4A), to strong focal reactivity. In the latter case, large necrotic granulomas were characterized by nodular aggregates of amebocytes in the periphery and their debrided remnants in the centre (Fig 4B). This last response was mainly observed in T. brevior infected snails, which were often featured by enlarged ventral surfaces of the foot and prominent vessel dilatation, along with few larval granulomas (Fig 4C). The occurrence of large amount of amebocytes was also seen in the kidney of T. brevior snails at 3 dpi (Fig 4D).


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: Inflammatory response to A. abstrusus in the H. aspersa.Cell-poor granuloma formation with vacuolated amebocytes at 3dpi. (A); cell-rich granuloma formation at 9 dpi (B); small necrotic granuloma at 15 dpi (C); fibroblast-like reaction at 27 dpi (D) (scale bar = 50μm; H&E).
© Copyright Policy
Related In: Results  -  Collection

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

pntd.0003722.g003: Histopathology: Inflammatory response to A. abstrusus in the H. aspersa.Cell-poor granuloma formation with vacuolated amebocytes at 3dpi. (A); cell-rich granuloma formation at 9 dpi (B); small necrotic granuloma at 15 dpi (C); fibroblast-like reaction at 27 dpi (D) (scale bar = 50μm; H&E).
Mentions: The tissue response to nematode larvae included: i) cell-poor (3 dpi; Fig 3A) and cell-rich (9 dpi; Fig 3B) granuloma-like formations, composed of non-vacuolated or vacuolated epithelioid amebocytes; ii) small necrotic granulomas (15 dpi; Fig 3C); iii) fibroblast-like encapsulations (27 dpi; Fig 3D). The severity of the inflammatory pattern ranged from mild reactions, featured by vessel dilatation, mild increase of the cellularity and small granulomas (Fig 4A), to strong focal reactivity. In the latter case, large necrotic granulomas were characterized by nodular aggregates of amebocytes in the periphery and their debrided remnants in the centre (Fig 4B). This last response was mainly observed in T. brevior infected snails, which were often featured by enlarged ventral surfaces of the foot and prominent vessel dilatation, along with few larval granulomas (Fig 4C). The occurrence of large amount of amebocytes was also seen in the kidney of T. brevior snails at 3 dpi (Fig 4D).

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