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...

Full description

Bibliographic Details
Main Authors: Muriel Rabone, Joris Wiethase, Paul F Clark, David Rollinson, Neil Cumberlidge, Aidan M Emery
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2021-02-01
Series:PLoS Neglected Tropical Diseases
Online Access:https://doi.org/10.1371/journal.pntd.0009120
_version_ 1818581707631099904
author Muriel Rabone
Joris Wiethase
Paul F Clark
David Rollinson
Neil Cumberlidge
Aidan M Emery
author_facet Muriel Rabone
Joris Wiethase
Paul F Clark
David Rollinson
Neil Cumberlidge
Aidan M Emery
author_sort Muriel Rabone
collection DOAJ
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.
first_indexed 2024-12-16T07:37:46Z
format Article
id doaj.art-b90e74dcbfec43d1a18dd384768fa739
institution Directory Open Access Journal
issn 1935-2727
1935-2735
language English
last_indexed 2024-12-16T07:37:46Z
publishDate 2021-02-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS Neglected Tropical Diseases
spelling doaj.art-b90e74dcbfec43d1a18dd384768fa7392022-12-21T22:39:10ZengPublic Library of Science (PLoS)PLoS Neglected Tropical Diseases1935-27271935-27352021-02-01152e000912010.1371/journal.pntd.0009120Endemicity 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.Muriel RaboneJoris WiethasePaul F ClarkDavid RollinsonNeil CumberlidgeAidan M EmeryParagonimiasis 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.https://doi.org/10.1371/journal.pntd.0009120
spellingShingle Muriel Rabone
Joris Wiethase
Paul F Clark
David Rollinson
Neil Cumberlidge
Aidan M Emery
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.
PLoS Neglected Tropical Diseases
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
url https://doi.org/10.1371/journal.pntd.0009120
work_keys_str_mv AT murielrabone endemicityofparagonimusandparagonimiasisinsubsaharanafricaasystematicreviewandmappingrevealsstabilityoftransmissioninendemicfociforamultihostparasitesystem
AT joriswiethase endemicityofparagonimusandparagonimiasisinsubsaharanafricaasystematicreviewandmappingrevealsstabilityoftransmissioninendemicfociforamultihostparasitesystem
AT paulfclark endemicityofparagonimusandparagonimiasisinsubsaharanafricaasystematicreviewandmappingrevealsstabilityoftransmissioninendemicfociforamultihostparasitesystem
AT davidrollinson endemicityofparagonimusandparagonimiasisinsubsaharanafricaasystematicreviewandmappingrevealsstabilityoftransmissioninendemicfociforamultihostparasitesystem
AT neilcumberlidge endemicityofparagonimusandparagonimiasisinsubsaharanafricaasystematicreviewandmappingrevealsstabilityoftransmissioninendemicfociforamultihostparasitesystem
AT aidanmemery endemicityofparagonimusandparagonimiasisinsubsaharanafricaasystematicreviewandmappingrevealsstabilityoftransmissioninendemicfociforamultihostparasitesystem