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Seasonal and Spatial Environmental Influence on Opisthorchis viverrini Intermediate Hosts, Abundance, and Distribution: Insights on Transmission Dynamics and Sustainable Control

BACKGROUND: Opisthorchis viverrini (Ov) is a complex-life-cycle trematode affecting 10 million people in SEA (Southeast Asia). Human infection occurs when infected cyprinid fish are consumed raw or undercooked. Ov requires three hosts and presents two free-living parasitic stages. As a consequence O...

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Autores principales: Kim, Christina Sunyoung, Echaubard, Pierre, Suwannatrai, Apiporn, Kaewkes, Sasithorn, Wilcox, Bruce A., Sripa, Banchob
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5120785/
https://www.ncbi.nlm.nih.gov/pubmed/27880787
http://dx.doi.org/10.1371/journal.pntd.0005121
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author Kim, Christina Sunyoung
Echaubard, Pierre
Suwannatrai, Apiporn
Kaewkes, Sasithorn
Wilcox, Bruce A.
Sripa, Banchob
author_facet Kim, Christina Sunyoung
Echaubard, Pierre
Suwannatrai, Apiporn
Kaewkes, Sasithorn
Wilcox, Bruce A.
Sripa, Banchob
author_sort Kim, Christina Sunyoung
collection PubMed
description BACKGROUND: Opisthorchis viverrini (Ov) is a complex-life-cycle trematode affecting 10 million people in SEA (Southeast Asia). Human infection occurs when infected cyprinid fish are consumed raw or undercooked. Ov requires three hosts and presents two free-living parasitic stages. As a consequence Ov transmission and infection in intermediate and human hosts are strongly mediated by environmental factors and understanding how environmental variability influences intermediate host abundance is critical. The objectives of this study were 1) to document water parameters, intermediate hosts abundance and infection spatio-temporal variation, 2) to assess their causal relationships and identify windows of transmission risk. METHODOLOGY/PRINCIPAL FINDINGS: Fish and snails were collected monthly for one year at 12 sites in Lawa Lake, an Ov-endemic region of Khon Kaen Province in Northeast Thailand. Physicochemical water parameters [pH, temperature (Tp), dissolved oxygen (DO), Salinity, electrical conductivity (EC), total dissolved solid (TDS), nitrite nitrogen (NO(2)-N), lead (Pb), total coliform bacteria (TCB) and fecal coliform bacteria (FCB)] were measured. Multivariate analyses, linear models and kriging were used to characterize water parameter variation and its influence on host abundance and infection prevalence. We found that sampling sites could be grouped in three clusters and discriminated along a nitrogen-salinity gradient where higher levels in the lake’s southern region predicted higher Bithynia relative abundance (P<0.05) and lower snail and fish species diversity (P<0.05). Highest Bithynia abundance occurred during rainy season (P<0.001), independently of site influence. Cyprinids were the most abundant fish family and higher cyprinid relative abundance was found in areas with higher Bithynia relative abundance (P<0.05). Ov infection in snails was anecdotal while Ov infection in fish was higher in the southern region (P<0.001) at sites showing high FCB. CONCLUSIONS/SIGNIFICANCE: Our results indicate that water contamination and waterways configuration can influence freshwater communities’ assemblages possibly creating ideal conditions for sustained transmission. Sustainable control may require a better appreciation of the system’s ecology with wise governance and development planning particularly in the current context of SEA agricultural intensification and landscape modification.
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spelling pubmed-51207852016-12-15 Seasonal and Spatial Environmental Influence on Opisthorchis viverrini Intermediate Hosts, Abundance, and Distribution: Insights on Transmission Dynamics and Sustainable Control Kim, Christina Sunyoung Echaubard, Pierre Suwannatrai, Apiporn Kaewkes, Sasithorn Wilcox, Bruce A. Sripa, Banchob PLoS Negl Trop Dis Research Article BACKGROUND: Opisthorchis viverrini (Ov) is a complex-life-cycle trematode affecting 10 million people in SEA (Southeast Asia). Human infection occurs when infected cyprinid fish are consumed raw or undercooked. Ov requires three hosts and presents two free-living parasitic stages. As a consequence Ov transmission and infection in intermediate and human hosts are strongly mediated by environmental factors and understanding how environmental variability influences intermediate host abundance is critical. The objectives of this study were 1) to document water parameters, intermediate hosts abundance and infection spatio-temporal variation, 2) to assess their causal relationships and identify windows of transmission risk. METHODOLOGY/PRINCIPAL FINDINGS: Fish and snails were collected monthly for one year at 12 sites in Lawa Lake, an Ov-endemic region of Khon Kaen Province in Northeast Thailand. Physicochemical water parameters [pH, temperature (Tp), dissolved oxygen (DO), Salinity, electrical conductivity (EC), total dissolved solid (TDS), nitrite nitrogen (NO(2)-N), lead (Pb), total coliform bacteria (TCB) and fecal coliform bacteria (FCB)] were measured. Multivariate analyses, linear models and kriging were used to characterize water parameter variation and its influence on host abundance and infection prevalence. We found that sampling sites could be grouped in three clusters and discriminated along a nitrogen-salinity gradient where higher levels in the lake’s southern region predicted higher Bithynia relative abundance (P<0.05) and lower snail and fish species diversity (P<0.05). Highest Bithynia abundance occurred during rainy season (P<0.001), independently of site influence. Cyprinids were the most abundant fish family and higher cyprinid relative abundance was found in areas with higher Bithynia relative abundance (P<0.05). Ov infection in snails was anecdotal while Ov infection in fish was higher in the southern region (P<0.001) at sites showing high FCB. CONCLUSIONS/SIGNIFICANCE: Our results indicate that water contamination and waterways configuration can influence freshwater communities’ assemblages possibly creating ideal conditions for sustained transmission. Sustainable control may require a better appreciation of the system’s ecology with wise governance and development planning particularly in the current context of SEA agricultural intensification and landscape modification. Public Library of Science 2016-11-23 /pmc/articles/PMC5120785/ /pubmed/27880787 http://dx.doi.org/10.1371/journal.pntd.0005121 Text en © 2016 Kim et al http://creativecommons.org/licenses/by/4.0/ 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 author and source are credited.
spellingShingle Research Article
Kim, Christina Sunyoung
Echaubard, Pierre
Suwannatrai, Apiporn
Kaewkes, Sasithorn
Wilcox, Bruce A.
Sripa, Banchob
Seasonal and Spatial Environmental Influence on Opisthorchis viverrini Intermediate Hosts, Abundance, and Distribution: Insights on Transmission Dynamics and Sustainable Control
title Seasonal and Spatial Environmental Influence on Opisthorchis viverrini Intermediate Hosts, Abundance, and Distribution: Insights on Transmission Dynamics and Sustainable Control
title_full Seasonal and Spatial Environmental Influence on Opisthorchis viverrini Intermediate Hosts, Abundance, and Distribution: Insights on Transmission Dynamics and Sustainable Control
title_fullStr Seasonal and Spatial Environmental Influence on Opisthorchis viverrini Intermediate Hosts, Abundance, and Distribution: Insights on Transmission Dynamics and Sustainable Control
title_full_unstemmed Seasonal and Spatial Environmental Influence on Opisthorchis viverrini Intermediate Hosts, Abundance, and Distribution: Insights on Transmission Dynamics and Sustainable Control
title_short Seasonal and Spatial Environmental Influence on Opisthorchis viverrini Intermediate Hosts, Abundance, and Distribution: Insights on Transmission Dynamics and Sustainable Control
title_sort seasonal and spatial environmental influence on opisthorchis viverrini intermediate hosts, abundance, and distribution: insights on transmission dynamics and sustainable control
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5120785/
https://www.ncbi.nlm.nih.gov/pubmed/27880787
http://dx.doi.org/10.1371/journal.pntd.0005121
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