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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

Infective L3 of T. brevior.(A) and A. abstrusus (B) detected in the mucus of H. aspersa snails at 25 days post-infection (scale bar = 50μm).
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pntd.0003722.g001: Infective L3 of T. brevior.(A) and A. abstrusus (B) detected in the mucus of H. aspersa snails at 25 days post-infection (scale bar = 50μm).

Mentions: Following the artificial digestion, all H. aspersa snails scored positive for metastrongyloid larvae. A total of 2858 A. abstrusus and 1390 T. brevior L3 were recovered and individual larval counts are reported in Table 2. The mean number of L3 was 127.8 (min 14–max 386) for A. abstrusus and 60.3 (min 10–max 170 L3) for T. brevior. Taking into account the original 500 L1 administered to each snail and the total number of larvae recovered, the proportion of L1 that had moulted to L3 was 25.6% for A. abstrusus and 12.1% for T. brevior (see statistical analysis paragraph). All nematodes detected were actively motile, and all specimens were morphologically identified as infective L3, since they had lost their outer sheaths and measured 442.7±17.8 μm (i.e., T. brevior and Fig 1A) and 548.6±30.3 μm (i.e., A. abstrusus and Fig 1B). This identification was confirmed by molecular amplification and sequencing of partial ITS-2 gene. Nucleotide sequences, examined by BLAST, displayed a 100% homology with those of A. abstrusus and T. brevior in GenBank (accession numbers KF751656 and KF751655).


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)

Infective L3 of T. brevior.(A) and A. abstrusus (B) detected in the mucus of H. aspersa snails at 25 days post-infection (scale bar = 50μm).
© Copyright Policy
Related In: Results  -  Collection

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

pntd.0003722.g001: Infective L3 of T. brevior.(A) and A. abstrusus (B) detected in the mucus of H. aspersa snails at 25 days post-infection (scale bar = 50μm).
Mentions: Following the artificial digestion, all H. aspersa snails scored positive for metastrongyloid larvae. A total of 2858 A. abstrusus and 1390 T. brevior L3 were recovered and individual larval counts are reported in Table 2. The mean number of L3 was 127.8 (min 14–max 386) for A. abstrusus and 60.3 (min 10–max 170 L3) for T. brevior. Taking into account the original 500 L1 administered to each snail and the total number of larvae recovered, the proportion of L1 that had moulted to L3 was 25.6% for A. abstrusus and 12.1% for T. brevior (see statistical analysis paragraph). All nematodes detected were actively motile, and all specimens were morphologically identified as infective L3, since they had lost their outer sheaths and measured 442.7±17.8 μm (i.e., T. brevior and Fig 1A) and 548.6±30.3 μm (i.e., A. abstrusus and Fig 1B). This identification was confirmed by molecular amplification and sequencing of partial ITS-2 gene. Nucleotide sequences, examined by BLAST, displayed a 100% homology with those of A. abstrusus and T. brevior in GenBank (accession numbers KF751656 and KF751655).

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