Host immunity, nutrition and coinfection alter longitudinal infection patterns of schistosomes in a free ranging African buffalo population.

Schistosomes are trematode parasites of global importance, causing infections in millions of people, livestock, and wildlife. Most studies on schistosomiasis, involve human subjects; as such, there is a paucity of longitudinal studies investigating parasite dynamics in the absence of intervention. A...

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Main Authors: Brianna R Beechler, Anna E Jolles, Sarah A Budischak, Paul L A M Corstjens, Vanessa O Ezenwa, Mireya Smith, Robert S Spaan, Govert J van Dam, Michelle L Steinauer
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2017-12-01
Series:PLoS Neglected Tropical Diseases
Online Access:http://europepmc.org/articles/PMC5755937?pdf=render
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spelling doaj-bc9c85bb72b74b67bfee63999ea8497a2020-11-25T01:42:56ZengPublic Library of Science (PLoS)PLoS Neglected Tropical Diseases1935-27271935-27352017-12-011112e000612210.1371/journal.pntd.0006122Host immunity, nutrition and coinfection alter longitudinal infection patterns of schistosomes in a free ranging African buffalo population.Brianna R BeechlerAnna E JollesSarah A BudischakPaul L A M CorstjensVanessa O EzenwaMireya SmithRobert S SpaanGovert J van DamMichelle L SteinauerSchistosomes are trematode parasites of global importance, causing infections in millions of people, livestock, and wildlife. Most studies on schistosomiasis, involve human subjects; as such, there is a paucity of longitudinal studies investigating parasite dynamics in the absence of intervention. As a consequence, despite decades of research on schistosomiasis, our understanding of its ecology in natural host populations is centered around how environmental exposure and acquired immunity influence acquisition of parasites, while very little is known about the influence of host physiology, coinfection and clearance in the absence of drug treatment. We used a 4-year study in free-ranging African buffalo to investigate natural schistosome dynamics. We asked (i) what are the spatial and temporal patterns of schistosome infections; (ii) how do parasite burdens vary over time within individual hosts; and (iii) what host factors (immunological, physiological, co-infection) and environmental factors (season, location) explain patterns of schistosome acquisition and loss in buffalo? Schistosome infections were common among buffalo. Microgeographic structure explained some variation in parasite burdens among hosts, indicating transmission hotspots. Overall, parasite burdens ratcheted up over time; however, gains in schistosome abundance in the dry season were partially offset by losses in the wet season, with some hosts demonstrating complete clearance of infection. Variation among buffalo in schistosome loss was associated with immunologic and nutritional factors, as well as co-infection by the gastrointestinal helminth Cooperia fuelleborni. Our results demonstrate that schistosome infections are surprisingly dynamic in a free-living mammalian host population, and point to a role for host factors in driving variation in parasite clearance, but not parasite acquisition which is driven by seasonal changes and spatial habitat utilization. Our study illustrates the power of longitudinal studies for discovering mechanisms underlying parasite dynamics in individual animals and populations.http://europepmc.org/articles/PMC5755937?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Brianna R Beechler
Anna E Jolles
Sarah A Budischak
Paul L A M Corstjens
Vanessa O Ezenwa
Mireya Smith
Robert S Spaan
Govert J van Dam
Michelle L Steinauer
spellingShingle Brianna R Beechler
Anna E Jolles
Sarah A Budischak
Paul L A M Corstjens
Vanessa O Ezenwa
Mireya Smith
Robert S Spaan
Govert J van Dam
Michelle L Steinauer
Host immunity, nutrition and coinfection alter longitudinal infection patterns of schistosomes in a free ranging African buffalo population.
PLoS Neglected Tropical Diseases
author_facet Brianna R Beechler
Anna E Jolles
Sarah A Budischak
Paul L A M Corstjens
Vanessa O Ezenwa
Mireya Smith
Robert S Spaan
Govert J van Dam
Michelle L Steinauer
author_sort Brianna R Beechler
title Host immunity, nutrition and coinfection alter longitudinal infection patterns of schistosomes in a free ranging African buffalo population.
title_short Host immunity, nutrition and coinfection alter longitudinal infection patterns of schistosomes in a free ranging African buffalo population.
title_full Host immunity, nutrition and coinfection alter longitudinal infection patterns of schistosomes in a free ranging African buffalo population.
title_fullStr Host immunity, nutrition and coinfection alter longitudinal infection patterns of schistosomes in a free ranging African buffalo population.
title_full_unstemmed Host immunity, nutrition and coinfection alter longitudinal infection patterns of schistosomes in a free ranging African buffalo population.
title_sort host immunity, nutrition and coinfection alter longitudinal infection patterns of schistosomes in a free ranging african buffalo population.
publisher Public Library of Science (PLoS)
series PLoS Neglected Tropical Diseases
issn 1935-2727
1935-2735
publishDate 2017-12-01
description Schistosomes are trematode parasites of global importance, causing infections in millions of people, livestock, and wildlife. Most studies on schistosomiasis, involve human subjects; as such, there is a paucity of longitudinal studies investigating parasite dynamics in the absence of intervention. As a consequence, despite decades of research on schistosomiasis, our understanding of its ecology in natural host populations is centered around how environmental exposure and acquired immunity influence acquisition of parasites, while very little is known about the influence of host physiology, coinfection and clearance in the absence of drug treatment. We used a 4-year study in free-ranging African buffalo to investigate natural schistosome dynamics. We asked (i) what are the spatial and temporal patterns of schistosome infections; (ii) how do parasite burdens vary over time within individual hosts; and (iii) what host factors (immunological, physiological, co-infection) and environmental factors (season, location) explain patterns of schistosome acquisition and loss in buffalo? Schistosome infections were common among buffalo. Microgeographic structure explained some variation in parasite burdens among hosts, indicating transmission hotspots. Overall, parasite burdens ratcheted up over time; however, gains in schistosome abundance in the dry season were partially offset by losses in the wet season, with some hosts demonstrating complete clearance of infection. Variation among buffalo in schistosome loss was associated with immunologic and nutritional factors, as well as co-infection by the gastrointestinal helminth Cooperia fuelleborni. Our results demonstrate that schistosome infections are surprisingly dynamic in a free-living mammalian host population, and point to a role for host factors in driving variation in parasite clearance, but not parasite acquisition which is driven by seasonal changes and spatial habitat utilization. Our study illustrates the power of longitudinal studies for discovering mechanisms underlying parasite dynamics in individual animals and populations.
url http://europepmc.org/articles/PMC5755937?pdf=render
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