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Endemicity of Paragonimus and paragonimiasis in Sub-Saharan Africa: A systematic review and mapping reveals stability of transmission in endemic foci for a multi-host parasite system

Paragonimiasis is caused by zoonotic trematodes of Paragonimus spp., found in Asia, the Americas and Africa, particularly in tropical regions. These parasites have a complex, multi-host life cycle, with mammalian definitive hosts and larval stages cycling through two intermediate hosts (snails and f...

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Autores principales: Rabone, Muriel, Wiethase, Joris, Clark, Paul F., Rollinson, David, Cumberlidge, Neil, Emery, Aidan M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7891758/
https://www.ncbi.nlm.nih.gov/pubmed/33544705
http://dx.doi.org/10.1371/journal.pntd.0009120
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author Rabone, Muriel
Wiethase, Joris
Clark, Paul F.
Rollinson, David
Cumberlidge, Neil
Emery, Aidan M.
author_facet Rabone, Muriel
Wiethase, Joris
Clark, Paul F.
Rollinson, David
Cumberlidge, Neil
Emery, Aidan M.
author_sort Rabone, Muriel
collection PubMed
description Paragonimiasis is caused by zoonotic trematodes of Paragonimus spp., found in Asia, the Americas and Africa, particularly in tropical regions. These parasites have a complex, multi-host life cycle, with mammalian definitive hosts and larval stages cycling through two intermediate hosts (snails and freshwater decapod crustaceans). In Africa, paragonimiasis is particularly neglected, and remains the only human parasitic disease without a fully characterised life cycle. However paragonimiasis has potentially significant impacts on public health in Africa, and prevalence has likely been underestimated through under-reporting and misdiagnosis as tuberculosis due to a similar clinical presentation. We identified the need to synthesise current knowledge and map endemic foci for African Paragonimus spp. together with Poikilorchis congolensis, a rare, taxonomically distant trematode with a similar distribution and morphology. We present the first systematic review of the literature relating to African paragonimiasis, combined with mapping of all reported occurrences of Paragonimus spp. throughout Africa, from the 1910s to the present. In human surveys, numerous reports of significant recent transmission in Southeast Nigeria were uncovered, with high prevalence and intensity of infection. Overall prevalence was significantly higher for P. uterobilateralis compared to P. africanus across studies. The potential endemicity of P. africanus in Côte d’Ivoire is also reported. In freshwater crab intermediate hosts, differences in prevalence and intensity of either P. uterobilateralis or P. africanus were evident across genera and species, suggesting differences in susceptibility. Mapping showed temporal stability of endemic foci, with the majority of known occurrences of Paragonimus found in the rainforest zone of West and Central Africa, but with several outliers elsewhere on the continent. This suggests substantial under sampling and localised infection where potential host distributions overlap. Our review highlights the urgent need for increased sampling in active disease foci in Africa, particularly using molecular analysis to fully characterise Paragonimus species and their hosts.
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spelling pubmed-78917582021-03-01 Endemicity of Paragonimus and paragonimiasis in Sub-Saharan Africa: A systematic review and mapping reveals stability of transmission in endemic foci for a multi-host parasite system Rabone, Muriel Wiethase, Joris Clark, Paul F. Rollinson, David Cumberlidge, Neil Emery, Aidan M. PLoS Negl Trop Dis Research Article Paragonimiasis is caused by zoonotic trematodes of Paragonimus spp., found in Asia, the Americas and Africa, particularly in tropical regions. These parasites have a complex, multi-host life cycle, with mammalian definitive hosts and larval stages cycling through two intermediate hosts (snails and freshwater decapod crustaceans). In Africa, paragonimiasis is particularly neglected, and remains the only human parasitic disease without a fully characterised life cycle. However paragonimiasis has potentially significant impacts on public health in Africa, and prevalence has likely been underestimated through under-reporting and misdiagnosis as tuberculosis due to a similar clinical presentation. We identified the need to synthesise current knowledge and map endemic foci for African Paragonimus spp. together with Poikilorchis congolensis, a rare, taxonomically distant trematode with a similar distribution and morphology. We present the first systematic review of the literature relating to African paragonimiasis, combined with mapping of all reported occurrences of Paragonimus spp. throughout Africa, from the 1910s to the present. In human surveys, numerous reports of significant recent transmission in Southeast Nigeria were uncovered, with high prevalence and intensity of infection. Overall prevalence was significantly higher for P. uterobilateralis compared to P. africanus across studies. The potential endemicity of P. africanus in Côte d’Ivoire is also reported. In freshwater crab intermediate hosts, differences in prevalence and intensity of either P. uterobilateralis or P. africanus were evident across genera and species, suggesting differences in susceptibility. Mapping showed temporal stability of endemic foci, with the majority of known occurrences of Paragonimus found in the rainforest zone of West and Central Africa, but with several outliers elsewhere on the continent. This suggests substantial under sampling and localised infection where potential host distributions overlap. Our review highlights the urgent need for increased sampling in active disease foci in Africa, particularly using molecular analysis to fully characterise Paragonimus species and their hosts. Public Library of Science 2021-02-05 /pmc/articles/PMC7891758/ /pubmed/33544705 http://dx.doi.org/10.1371/journal.pntd.0009120 Text en © 2021 Rabone 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
Rabone, Muriel
Wiethase, Joris
Clark, Paul F.
Rollinson, David
Cumberlidge, Neil
Emery, Aidan M.
Endemicity of Paragonimus and paragonimiasis in Sub-Saharan Africa: A systematic review and mapping reveals stability of transmission in endemic foci for a multi-host parasite system
title Endemicity of Paragonimus and paragonimiasis in Sub-Saharan Africa: A systematic review and mapping reveals stability of transmission in endemic foci for a multi-host parasite system
title_full Endemicity of Paragonimus and paragonimiasis in Sub-Saharan Africa: A systematic review and mapping reveals stability of transmission in endemic foci for a multi-host parasite system
title_fullStr Endemicity of Paragonimus and paragonimiasis in Sub-Saharan Africa: A systematic review and mapping reveals stability of transmission in endemic foci for a multi-host parasite system
title_full_unstemmed Endemicity of Paragonimus and paragonimiasis in Sub-Saharan Africa: A systematic review and mapping reveals stability of transmission in endemic foci for a multi-host parasite system
title_short Endemicity of Paragonimus and paragonimiasis in Sub-Saharan Africa: A systematic review and mapping reveals stability of transmission in endemic foci for a multi-host parasite system
title_sort endemicity of paragonimus and paragonimiasis in sub-saharan africa: a systematic review and mapping reveals stability of transmission in endemic foci for a multi-host parasite system
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7891758/
https://www.ncbi.nlm.nih.gov/pubmed/33544705
http://dx.doi.org/10.1371/journal.pntd.0009120
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