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Field-derived Schistosoma mansoni and Biomphalaria pfeifferi in Kenya: a compatible association characterized by lack of strong local adaptation, and presence of some snails able to persistently produce cercariae for over a year

BACKGROUND: Schistosoma mansoni is widely distributed in sub-Saharan Africa with Biomphalaria pfeifferi being its most widespread and important snail intermediate host. Few studies have examined the compatibility of field-derived B. pfeifferi snails with S. mansoni miracidia derived from human hosts...

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Autores principales: Mutuku, Martin W, Dweni, Celestine K, Mwangi, Moses, Kinuthia, Joseph M, Mwangi, Ibrahim N, Maina, Geoffrey M, Agola, Lelo E, Zhang, Si-Ming, Maranga, Rosebella, Loker, Eric S, Mkoji, Gerald M
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4253995/
https://www.ncbi.nlm.nih.gov/pubmed/25425455
http://dx.doi.org/10.1186/s13071-014-0533-3
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author Mutuku, Martin W
Dweni, Celestine K
Mwangi, Moses
Kinuthia, Joseph M
Mwangi, Ibrahim N
Maina, Geoffrey M
Agola, Lelo E
Zhang, Si-Ming
Maranga, Rosebella
Loker, Eric S
Mkoji, Gerald M
author_facet Mutuku, Martin W
Dweni, Celestine K
Mwangi, Moses
Kinuthia, Joseph M
Mwangi, Ibrahim N
Maina, Geoffrey M
Agola, Lelo E
Zhang, Si-Ming
Maranga, Rosebella
Loker, Eric S
Mkoji, Gerald M
author_sort Mutuku, Martin W
collection PubMed
description BACKGROUND: Schistosoma mansoni is widely distributed in sub-Saharan Africa with Biomphalaria pfeifferi being its most widespread and important snail intermediate host. Few studies have examined the compatibility of field-derived B. pfeifferi snails with S. mansoni miracidia derived from human hosts. We investigated compatibility (as defined by shedding of cercariae following exposure to miracidia) of two isolates of S. mansoni from school children from Asao (western Kenya) and Mwea (central Kenya) with B. pfeifferi collected directly from Asao stream or the Mwea rice fields. METHODS: We exposed snails from both regions to four different doses of miracidia (1, 5, 10 and 25) from sympatric or allopatric S. mansoni, and maintained them in a shaded, screened out-of-doors rearing facility in Kisian, in western Kenya. Both snail survival and the number of snails that became infected were monitored weekly. This was done for 25 weeks post-exposure (PE). Those infected snails which survived beyond this period were monitored until they all died. RESULTS: Although overall survival of Mwea snails maintained in western Kenya was generally low, both sympatric and allopatric combinations of parasites and snails exhibited high compatibility (approximately 50% at a dose of one miracidium per snail), with an increase in infection rates as the miracidial dose was increased (P < 0.002). Schistosomes were no more compatible with sympatric than allopatric snails, nor were snails less compatible with sympatric than allopatric schistosomes. Snail mortality increased significantly with dose of miracidia (P < 0.05). Approximately 3% of Asao snails exposed to a low dose of sympatric miracidia (1 or 5) continued to shed cercariae for as long as 58 weeks post exposure. CONCLUSIONS: There were no significant local adaptation effects for either schistosomes or snails. Also, the existence of “super-survivor” snails is noteworthy for its implications for current control initiatives that mostly rely on mass drug administration (MDA). Long-term shedders could provide an ongoing source of cercariae to initiate human infections for many months, suggesting care is required in considering how human MDA treatments are timed. Future control programs should incorporate means to eliminate infected snails to complement chemotherapy interventions in controlling schistosomiasis. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13071-014-0533-3) contains supplementary material, which is available to authorized users.
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spelling pubmed-42539952014-12-04 Field-derived Schistosoma mansoni and Biomphalaria pfeifferi in Kenya: a compatible association characterized by lack of strong local adaptation, and presence of some snails able to persistently produce cercariae for over a year Mutuku, Martin W Dweni, Celestine K Mwangi, Moses Kinuthia, Joseph M Mwangi, Ibrahim N Maina, Geoffrey M Agola, Lelo E Zhang, Si-Ming Maranga, Rosebella Loker, Eric S Mkoji, Gerald M Parasit Vectors Research BACKGROUND: Schistosoma mansoni is widely distributed in sub-Saharan Africa with Biomphalaria pfeifferi being its most widespread and important snail intermediate host. Few studies have examined the compatibility of field-derived B. pfeifferi snails with S. mansoni miracidia derived from human hosts. We investigated compatibility (as defined by shedding of cercariae following exposure to miracidia) of two isolates of S. mansoni from school children from Asao (western Kenya) and Mwea (central Kenya) with B. pfeifferi collected directly from Asao stream or the Mwea rice fields. METHODS: We exposed snails from both regions to four different doses of miracidia (1, 5, 10 and 25) from sympatric or allopatric S. mansoni, and maintained them in a shaded, screened out-of-doors rearing facility in Kisian, in western Kenya. Both snail survival and the number of snails that became infected were monitored weekly. This was done for 25 weeks post-exposure (PE). Those infected snails which survived beyond this period were monitored until they all died. RESULTS: Although overall survival of Mwea snails maintained in western Kenya was generally low, both sympatric and allopatric combinations of parasites and snails exhibited high compatibility (approximately 50% at a dose of one miracidium per snail), with an increase in infection rates as the miracidial dose was increased (P < 0.002). Schistosomes were no more compatible with sympatric than allopatric snails, nor were snails less compatible with sympatric than allopatric schistosomes. Snail mortality increased significantly with dose of miracidia (P < 0.05). Approximately 3% of Asao snails exposed to a low dose of sympatric miracidia (1 or 5) continued to shed cercariae for as long as 58 weeks post exposure. CONCLUSIONS: There were no significant local adaptation effects for either schistosomes or snails. Also, the existence of “super-survivor” snails is noteworthy for its implications for current control initiatives that mostly rely on mass drug administration (MDA). Long-term shedders could provide an ongoing source of cercariae to initiate human infections for many months, suggesting care is required in considering how human MDA treatments are timed. Future control programs should incorporate means to eliminate infected snails to complement chemotherapy interventions in controlling schistosomiasis. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13071-014-0533-3) contains supplementary material, which is available to authorized users. BioMed Central 2014-11-26 /pmc/articles/PMC4253995/ /pubmed/25425455 http://dx.doi.org/10.1186/s13071-014-0533-3 Text en © Mutuku et al.; licensee BioMed Central Ltd. 2014 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Mutuku, Martin W
Dweni, Celestine K
Mwangi, Moses
Kinuthia, Joseph M
Mwangi, Ibrahim N
Maina, Geoffrey M
Agola, Lelo E
Zhang, Si-Ming
Maranga, Rosebella
Loker, Eric S
Mkoji, Gerald M
Field-derived Schistosoma mansoni and Biomphalaria pfeifferi in Kenya: a compatible association characterized by lack of strong local adaptation, and presence of some snails able to persistently produce cercariae for over a year
title Field-derived Schistosoma mansoni and Biomphalaria pfeifferi in Kenya: a compatible association characterized by lack of strong local adaptation, and presence of some snails able to persistently produce cercariae for over a year
title_full Field-derived Schistosoma mansoni and Biomphalaria pfeifferi in Kenya: a compatible association characterized by lack of strong local adaptation, and presence of some snails able to persistently produce cercariae for over a year
title_fullStr Field-derived Schistosoma mansoni and Biomphalaria pfeifferi in Kenya: a compatible association characterized by lack of strong local adaptation, and presence of some snails able to persistently produce cercariae for over a year
title_full_unstemmed Field-derived Schistosoma mansoni and Biomphalaria pfeifferi in Kenya: a compatible association characterized by lack of strong local adaptation, and presence of some snails able to persistently produce cercariae for over a year
title_short Field-derived Schistosoma mansoni and Biomphalaria pfeifferi in Kenya: a compatible association characterized by lack of strong local adaptation, and presence of some snails able to persistently produce cercariae for over a year
title_sort field-derived schistosoma mansoni and biomphalaria pfeifferi in kenya: a compatible association characterized by lack of strong local adaptation, and presence of some snails able to persistently produce cercariae for over a year
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4253995/
https://www.ncbi.nlm.nih.gov/pubmed/25425455
http://dx.doi.org/10.1186/s13071-014-0533-3
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