Identifying wildlife reservoirs of neglected taeniid tapeworms: Non-invasive diagnosis of endemic Taenia serialis infection in a wild primate population.

Despite the global distribution and public health consequences of Taenia tapeworms, the life cycles of taeniids infecting wildlife hosts remain largely undescribed. The larval stage of Taenia serialis commonly parasitizes rodents and lagomorphs, but has been reported in a wide range of hosts that in...

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Main Authors: India Schneider-Crease, Randi H Griffin, Megan A Gomery, Pierre Dorny, John C Noh, Sukwan Handali, Holly M Chastain, Patricia P Wilkins, Charles L Nunn, Noah Snyder-Mackler, Jacinta C Beehner, Thore J Bergman
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2017-07-01
Series:PLoS Neglected Tropical Diseases
Online Access:https://doi.org/10.1371/journal.pntd.0005709
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spelling doaj-f971215e6ec842b498a7c9471aff3fc82021-04-21T23:53:36ZengPublic Library of Science (PLoS)PLoS Neglected Tropical Diseases1935-27271935-27352017-07-01117e000570910.1371/journal.pntd.0005709Identifying wildlife reservoirs of neglected taeniid tapeworms: Non-invasive diagnosis of endemic Taenia serialis infection in a wild primate population.India Schneider-CreaseRandi H GriffinMegan A GomeryPierre DornyJohn C NohSukwan HandaliHolly M ChastainPatricia P WilkinsCharles L NunnNoah Snyder-MacklerJacinta C BeehnerThore J BergmanDespite the global distribution and public health consequences of Taenia tapeworms, the life cycles of taeniids infecting wildlife hosts remain largely undescribed. The larval stage of Taenia serialis commonly parasitizes rodents and lagomorphs, but has been reported in a wide range of hosts that includes geladas (Theropithecus gelada), primates endemic to Ethiopia. Geladas exhibit protuberant larval cysts indicative of advanced T. serialis infection that are associated with high mortality. However, non-protuberant larvae can develop in deep tissue or the abdominal cavity, leading to underestimates of prevalence based solely on observable cysts. We adapted a non-invasive monoclonal antibody-based enzyme-linked immunosorbent assay (ELISA) to detect circulating Taenia spp. antigen in dried gelada urine. Analysis revealed that this assay was highly accurate in detecting Taenia antigen, with 98.4% specificity, 98.5% sensitivity, and an area under the curve of 0.99. We used this assay to investigate the prevalence of T. serialis infection in a wild gelada population, finding that infection is substantially more widespread than the occurrence of visible T. serialis cysts (16.4% tested positive at least once, while only 6% of the same population exhibited cysts). We examined whether age or sex predicted T. serialis infection as indicated by external cysts and antigen presence. Contrary to the female-bias observed in many Taenia-host systems, we found no significant sex bias in either cyst presence or antigen presence. Age, on the other hand, predicted cyst presence (older individuals were more likely to show cysts) but not antigen presence. We interpret this finding to indicate that T. serialis may infect individuals early in life but only result in visible disease later in life. This is the first application of an antigen ELISA to the study of larval Taenia infection in wildlife, opening the doors to the identification and description of infection dynamics in reservoir populations.https://doi.org/10.1371/journal.pntd.0005709
collection DOAJ
language English
format Article
sources DOAJ
author India Schneider-Crease
Randi H Griffin
Megan A Gomery
Pierre Dorny
John C Noh
Sukwan Handali
Holly M Chastain
Patricia P Wilkins
Charles L Nunn
Noah Snyder-Mackler
Jacinta C Beehner
Thore J Bergman
spellingShingle India Schneider-Crease
Randi H Griffin
Megan A Gomery
Pierre Dorny
John C Noh
Sukwan Handali
Holly M Chastain
Patricia P Wilkins
Charles L Nunn
Noah Snyder-Mackler
Jacinta C Beehner
Thore J Bergman
Identifying wildlife reservoirs of neglected taeniid tapeworms: Non-invasive diagnosis of endemic Taenia serialis infection in a wild primate population.
PLoS Neglected Tropical Diseases
author_facet India Schneider-Crease
Randi H Griffin
Megan A Gomery
Pierre Dorny
John C Noh
Sukwan Handali
Holly M Chastain
Patricia P Wilkins
Charles L Nunn
Noah Snyder-Mackler
Jacinta C Beehner
Thore J Bergman
author_sort India Schneider-Crease
title Identifying wildlife reservoirs of neglected taeniid tapeworms: Non-invasive diagnosis of endemic Taenia serialis infection in a wild primate population.
title_short Identifying wildlife reservoirs of neglected taeniid tapeworms: Non-invasive diagnosis of endemic Taenia serialis infection in a wild primate population.
title_full Identifying wildlife reservoirs of neglected taeniid tapeworms: Non-invasive diagnosis of endemic Taenia serialis infection in a wild primate population.
title_fullStr Identifying wildlife reservoirs of neglected taeniid tapeworms: Non-invasive diagnosis of endemic Taenia serialis infection in a wild primate population.
title_full_unstemmed Identifying wildlife reservoirs of neglected taeniid tapeworms: Non-invasive diagnosis of endemic Taenia serialis infection in a wild primate population.
title_sort identifying wildlife reservoirs of neglected taeniid tapeworms: non-invasive diagnosis of endemic taenia serialis infection in a wild primate population.
publisher Public Library of Science (PLoS)
series PLoS Neglected Tropical Diseases
issn 1935-2727
1935-2735
publishDate 2017-07-01
description Despite the global distribution and public health consequences of Taenia tapeworms, the life cycles of taeniids infecting wildlife hosts remain largely undescribed. The larval stage of Taenia serialis commonly parasitizes rodents and lagomorphs, but has been reported in a wide range of hosts that includes geladas (Theropithecus gelada), primates endemic to Ethiopia. Geladas exhibit protuberant larval cysts indicative of advanced T. serialis infection that are associated with high mortality. However, non-protuberant larvae can develop in deep tissue or the abdominal cavity, leading to underestimates of prevalence based solely on observable cysts. We adapted a non-invasive monoclonal antibody-based enzyme-linked immunosorbent assay (ELISA) to detect circulating Taenia spp. antigen in dried gelada urine. Analysis revealed that this assay was highly accurate in detecting Taenia antigen, with 98.4% specificity, 98.5% sensitivity, and an area under the curve of 0.99. We used this assay to investigate the prevalence of T. serialis infection in a wild gelada population, finding that infection is substantially more widespread than the occurrence of visible T. serialis cysts (16.4% tested positive at least once, while only 6% of the same population exhibited cysts). We examined whether age or sex predicted T. serialis infection as indicated by external cysts and antigen presence. Contrary to the female-bias observed in many Taenia-host systems, we found no significant sex bias in either cyst presence or antigen presence. Age, on the other hand, predicted cyst presence (older individuals were more likely to show cysts) but not antigen presence. We interpret this finding to indicate that T. serialis may infect individuals early in life but only result in visible disease later in life. This is the first application of an antigen ELISA to the study of larval Taenia infection in wildlife, opening the doors to the identification and description of infection dynamics in reservoir populations.
url https://doi.org/10.1371/journal.pntd.0005709
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