Changes in the reproductive biology of Biomphalaria glabrata experimentally infected with the nematode Angiostrongylus cantonensis

Tunholi-Alves, Vinícius Menezes; Tunholi, Victor Menezes; Lustrino, Danilo; Amaral, Ludimila Santos; Thiengo, Silvana Carvalho; Pinheiro, Jairo

doi:10.1016/j.jip.2011.08.009

Cited by 34 publications

(26 citation statements)

References 11 publications

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“…also affect the snails through aminergic pathways as suggested by Delgado et al [34] and Vallejo et al [35]. For example, serotonin may be involved in parasitic castration [67], leading to a redirection of energy resources in infected snails [68][69][70][71][72]. Similarly, the presence of tyrosine hydroxylase-like immunoreactivity in the dorsal bodies of Biomphalaria [35] suggests that dopamine could also be involved in the diminished egg laying observed in infected snails [73].…”

Section: Discussionmentioning

confidence: 99%

Histamine Immunoreactive Elements in the Central and Peripheral Nervous Systems of the Snail, Biomphalaria spp., Intermediate Host for Schistosoma mansoni

et al. 2015

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Histamine appears to be an important transmitter throughout the Animal Kingdom. Gastropods, in particular, have been used in numerous studies establishing potential roles for this biogenic amine in the nervous system and showing its involvement in the generation of diverse behaviours. And yet, the distribution of histamine has only previously been described in a small number of molluscan species. The present study examined the localization of histamine-like immunoreactivity in the central and peripheral nervous systems of pulmonate snails of the genus Biomphalaria. This investigation demonstrates immunoreactive cells throughout the buccal, cerebral, pedal, left parietal and visceral ganglia, indicative of diverse regulatory functions in Biomphalaria. Immunoreactivity was also present in statocyst hair cells, supporting a role for histamine in graviception. In the periphery, dense innervation by immunoreactive fibers was observed in the anterior foot, perioral zone, and other regions of the body wall. This study thus shows that histamine is an abundant transmitter in these snails and its distribution suggest involvement in numerous neural circuits. In addition to providing novel subjects for comparative studies of histaminegic neurons in gastropods, Biomphalaria is also the major intermediate host for the digenetic trematode parasite, which causes human schistosomiasis. The study therefore provides a foundation for understanding potential roles for histamine in interactions between the snail hosts and their trematode parasites.

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Section: Discussionmentioning

confidence: 99%

Histamine Immunoreactive Elements in the Central and Peripheral Nervous Systems of the Snail, Biomphalaria spp., Intermediate Host for Schistosoma mansoni

et al. 2015

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“…It has been demonstrated that S. mansoni parasitism is able to suppress the production of eggs by the host snail. The process of partial or definitive reduction or interruption of fecundity is called parasitic castration, and two mechanisms have been postulated to explain its outcomes: a direct process related to parasite-induced snail tissue damage that destroys the hermaphrodite gland or an indirect process that is associated with decreased energy reserves (Baudoin, 1975;Thornhill et al, 1986;Thompson and Lee, 1986;Pan, 1965;Tunholi-Alves et al, 2011). The carbohydrate reserves in snails comprise two polysaccharides, glycogen and galactogen (Lustrino et al, 2008).…”

Section: Introductionmentioning

confidence: 99%

Biological, biochemical and histopathological features related to parasitic castration of Biomphalaria glabrata infected by Schistosoma mansoni

Faro

Perazzini

Corrêa

et al. 2013

Experimental Parasitology

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Parasitic castration in the snail-trematode relationship can be understood as any change in the reproductive function of the snail that is due to interference by the developing larvae inside the snail that leads to the reduction or complete disruption of egg-laying activity. This study was designed to observe the parasitic castration of Biomphalaria glabrata infected with Schistosoma mansoni during both the pre-patent and patent periods. The effect of infection on snail fecundity and fertility, growth rate and survival was studied during the 62 days following miracidia exposure. An integrated approach was employed that used biochemical and histological tools over the same period. To study the effect of infection on reproduction, we individually exposed 30 snails to 5 miracidia each and tracked their fertility and fecundity. For our histopathological studies, 50 snails were exposed to 20 miracidia each, and for our histochemical studies, 50 snails were exposed to 5 miracidia each. An equal number of uninfected snails were used as a control for each group. The B. glabrata exposed to the BH strain of S. mansoni showed 50% positivity for cercarial shedding. Both the experimental and control groups showed 100% survival. The pre-patent period lasted until 39 days after exposure to miracidia. Exposed snails that showed cercarial shedding exhibited higher growth rates than either exposed snails that did not demonstrate cercarial shedding or uninfected controls. Exposed snails without cercarial shedding and uninfected controls showed no differences in the reproductive parameters evaluated during the patent period; snails experiencing cercarial shedding showed a reduction in fecundity and fertility. These snails began to lay eggs only after the 50th day post miracidia exposure. The haemolymph glucose levels showed an oscillating pattern that decreased during periods of greater mobilisation of energy by the larvae and was accompanied by a depletion of glycogen in the cephalopodal mass and digestive gland. Histopathological examination at 55 days showed that the ovotestis was highly atrophied. There was almost complete disappearance of germ cells, and the supporting stroma formed a nearly empty net. At day 45, the infected digestive gland showed a high cylindrical epithelium with little preserved cytoplasm. The contents of the secretory granules of the albumen gland of infected animals stained with Alcian blue (AB), pH 1.0, indicating the presence of sulphated carbohydrates. Thus, parasitic castration in the B. glabrata-S. mansoni model may be regulated directly and indirectly by the developmental stage of the trematode and the biochemical and histopathological alterations during the patent period of infection.

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“…The nematode Angiostrongylus cantonensis and trematode parasites belonging to the genus Plagiorchis or Echinostoma are known to affect growth as well as fecundity and fertility of B . glabrata , and have thus been proposed as biological control agents [74–76]. However, their use is not recommended since they may also cause severe human or animal infections.…”

Section: Discussionmentioning

confidence: 99%

“…A castration-like phenomenon similar to that observed in heavily infected snails has also been reported during parasitic infestation by S . mansoni [99,100], Plagiorchis elegans [74], and the nematode Angiostrongylus cantonensis [76]. This late infertility appears to be related to competition for energy resources between the host and pathogen [76,100].…”

Section: Discussionmentioning

confidence: 99%

“…mansoni [99,100], Plagiorchis elegans [74], and the nematode Angiostrongylus cantonensis [76]. This late infertility appears to be related to competition for energy resources between the host and pathogen [76,100]. Paenibacillus was also observed in the secondary reproductive organs, namely muciparous and albumin glands, which could be a sign of vertically transmitted infection from parent to offspring.…”

Section: Discussionmentioning

confidence: 99%

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A Novel Bacterial Pathogen of Biomphalaria glabrata: A Potential Weapon for Schistosomiasis Control?

et al. 2015

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BackgroundSchistosomiasis is the second-most widespread tropical parasitic disease after malaria. Various research strategies and treatment programs for achieving the objective of eradicating schistosomiasis within a decade have been recommended and supported by the World Health Organization. One of these approaches is based on the control of snail vectors in endemic areas. Previous field studies have shown that competitor or predator introduction can reduce snail numbers, but no systematic investigation has ever been conducted to identify snail microbial pathogens and evaluate their molluscicidal effects.Methodology/Principal findingsIn populations of Biomphalaria glabrata snails experiencing high mortalities, white nodules were visible on snail bodies. Infectious agents were isolated from such nodules. Only one type of bacteria, identified as a new species of Paenibacillus named Candidatus Paenibacillus glabratella, was found, and was shown to be closely related to P. alvei through 16S and Rpob DNA analysis. Histopathological examination showed extensive bacterial infiltration leading to overall tissue disorganization. Exposure of healthy snails to Paenibacillus-infected snails caused massive mortality. Moreover, eggs laid by infected snails were also infected, decreasing hatching but without apparent effects on spawning. Embryonic lethality was correlated with the presence of pathogenic bacteria in eggs.Conclusions/SignificanceThis is the first account of a novel Paenibacillus strain, Ca. Paenibacillus glabratella, as a snail microbial pathogen. Since this strain affects both adult and embryonic stages and causes significant mortality, it may hold promise as a biocontrol agent to limit schistosomiasis transmission in the field.

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Changes in the reproductive biology of Biomphalaria glabrata experimentally infected with the nematode Angiostrongylus cantonensis

Cited by 34 publications

References 11 publications

Histamine Immunoreactive Elements in the Central and Peripheral Nervous Systems of the Snail, Biomphalaria spp., Intermediate Host for Schistosoma mansoni

Histamine Immunoreactive Elements in the Central and Peripheral Nervous Systems of the Snail, Biomphalaria spp., Intermediate Host for Schistosoma mansoni

Biological, biochemical and histopathological features related to parasitic castration of Biomphalaria glabrata infected by Schistosoma mansoni

A Novel Bacterial Pathogen of Biomphalaria glabrata: A Potential Weapon for Schistosomiasis Control?

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