Coinfection modifies carriage of enzootic and zoonotic parasites in Norway rats from an urban slum

Abstract We examine coinfection between helminth species and the bacterium Leptospira interrogans in a natural population of the Norway rat, Rattus norvegicus. We ask whether coinfection can influence the probability and intensity of infection of these enzootic and zoonotic parasites in urban rats,...

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Main Authors: Ticiana S. A. Carvalho‐Pereira, Fábio Neves Souza, Luana Ribeiro do Nascimento Santos, Gabriel Ghizzi Pedra, Amanda Minter, Thiago Campanharo Bahiense, Mitermayer Galvão Reis, Albert Icksang Ko, James E. Childs, Eduardo M. daSilva, Federico Costa, Mike Begon
Format: Article
Language:English
Published: Wiley 2019-10-01
Series:Ecosphere
Subjects:
Online Access:https://doi.org/10.1002/ecs2.2887
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author Ticiana S. A. Carvalho‐Pereira
Fábio Neves Souza
Luana Ribeiro do Nascimento Santos
Gabriel Ghizzi Pedra
Amanda Minter
Thiago Campanharo Bahiense
Mitermayer Galvão Reis
Albert Icksang Ko
James E. Childs
Eduardo M. daSilva
Federico Costa
Mike Begon
author_facet Ticiana S. A. Carvalho‐Pereira
Fábio Neves Souza
Luana Ribeiro do Nascimento Santos
Gabriel Ghizzi Pedra
Amanda Minter
Thiago Campanharo Bahiense
Mitermayer Galvão Reis
Albert Icksang Ko
James E. Childs
Eduardo M. daSilva
Federico Costa
Mike Begon
author_sort Ticiana S. A. Carvalho‐Pereira
collection DOAJ
description Abstract We examine coinfection between helminth species and the bacterium Leptospira interrogans in a natural population of the Norway rat, Rattus norvegicus. We ask whether coinfection can influence the probability and intensity of infection of these enzootic and zoonotic parasites in urban rats, which may affect the loads of parasites excreted into the environment. Rodent sampling was carried out during two seasons in 2014 in a Brazilian urban slum. We sampled rats’ feces, kidney imprints, and urine to identify and quantify helminth eggs/larvae and infection by L. interrogans. Eleven species/groups of helminths and L. interrogans were identified among 299 captured rats. Simple correlation tests and generalized linear models were performed to identify general patterns of coinfection and potential direction of effects, respectively, after controlling for consolidated environmental and host biotic variables. Significant associations were illustrated in an interaction network. Focusing on parasites with the potential to cause zoonoses among humans, we observed that coinfection between L. interrogans and the nematode Angiostrongylus cantonensis was significantly more frequent than expected. Reduced prevalence of A. cantonensis was found in the presence of Nippostrongylus brasiliensis, and N. brasiliensis intensities (eggs per gram of feces) were increased with greater intensities of both L. interrogans and Strongyloides sp., the latter of which was, in turn, found to increase the intensities of A. cantonensis. A higher probability of finding L. interrogans was associated with infection by Strongyloides sp. Our study provides a novel perspective on evaluating helminth coinfection profiles in populations of naturally infected urban rats, moving beyond previous studies which have been limited to descriptions of co‐occurrence. Noticeably, infection risk was dependent on coinfection and this should be accounted for when targeting the control of zoonotic pathogens in natural populations.
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spelling doaj.art-19090352616f4c10a90cda2621fcd43f2022-12-21T18:13:59ZengWileyEcosphere2150-89252019-10-011010n/an/a10.1002/ecs2.2887Coinfection modifies carriage of enzootic and zoonotic parasites in Norway rats from an urban slumTiciana S. A. Carvalho‐Pereira0Fábio Neves Souza1Luana Ribeiro do Nascimento Santos2Gabriel Ghizzi Pedra3Amanda Minter4Thiago Campanharo Bahiense5Mitermayer Galvão Reis6Albert Icksang Ko7James E. Childs8Eduardo M. daSilva9Federico Costa10Mike Begon11Instituto de Biologia, Instituto de Ciências da Saúde, Faculdade de Medicina, Instituto de Saúde Coletiva Federal University of Bahia (UFBA) Salvador BrazilInstituto de Biologia, Instituto de Ciências da Saúde, Faculdade de Medicina, Instituto de Saúde Coletiva Federal University of Bahia (UFBA) Salvador BrazilInstituto Gonçalo Moniz Fundação Oswaldo Cruz Ministério da Saúde Salvador BrazilInstitute of Integrative Biology University of Liverpool Liverpool UKInstitute of Integrative Biology University of Liverpool Liverpool UKInstituto de Biologia, Instituto de Ciências da Saúde, Faculdade de Medicina, Instituto de Saúde Coletiva Federal University of Bahia (UFBA) Salvador BrazilInstituto de Biologia, Instituto de Ciências da Saúde, Faculdade de Medicina, Instituto de Saúde Coletiva Federal University of Bahia (UFBA) Salvador BrazilDepartment of Epidemiology of Microbial Disease Yale School of Public Health New Haven Connecticut USADepartment of Epidemiology of Microbial Disease Yale School of Public Health New Haven Connecticut USAInstituto de Biologia, Instituto de Ciências da Saúde, Faculdade de Medicina, Instituto de Saúde Coletiva Federal University of Bahia (UFBA) Salvador BrazilInstituto de Biologia, Instituto de Ciências da Saúde, Faculdade de Medicina, Instituto de Saúde Coletiva Federal University of Bahia (UFBA) Salvador BrazilInstitute of Integrative Biology University of Liverpool Liverpool UKAbstract We examine coinfection between helminth species and the bacterium Leptospira interrogans in a natural population of the Norway rat, Rattus norvegicus. We ask whether coinfection can influence the probability and intensity of infection of these enzootic and zoonotic parasites in urban rats, which may affect the loads of parasites excreted into the environment. Rodent sampling was carried out during two seasons in 2014 in a Brazilian urban slum. We sampled rats’ feces, kidney imprints, and urine to identify and quantify helminth eggs/larvae and infection by L. interrogans. Eleven species/groups of helminths and L. interrogans were identified among 299 captured rats. Simple correlation tests and generalized linear models were performed to identify general patterns of coinfection and potential direction of effects, respectively, after controlling for consolidated environmental and host biotic variables. Significant associations were illustrated in an interaction network. Focusing on parasites with the potential to cause zoonoses among humans, we observed that coinfection between L. interrogans and the nematode Angiostrongylus cantonensis was significantly more frequent than expected. Reduced prevalence of A. cantonensis was found in the presence of Nippostrongylus brasiliensis, and N. brasiliensis intensities (eggs per gram of feces) were increased with greater intensities of both L. interrogans and Strongyloides sp., the latter of which was, in turn, found to increase the intensities of A. cantonensis. A higher probability of finding L. interrogans was associated with infection by Strongyloides sp. Our study provides a novel perspective on evaluating helminth coinfection profiles in populations of naturally infected urban rats, moving beyond previous studies which have been limited to descriptions of co‐occurrence. Noticeably, infection risk was dependent on coinfection and this should be accounted for when targeting the control of zoonotic pathogens in natural populations.https://doi.org/10.1002/ecs2.2887Angiostrongylus cantonensiscoinfectionhelminthsinteraction networkLeptospira interrogansNippostrongylus brasiliensis
spellingShingle Ticiana S. A. Carvalho‐Pereira
Fábio Neves Souza
Luana Ribeiro do Nascimento Santos
Gabriel Ghizzi Pedra
Amanda Minter
Thiago Campanharo Bahiense
Mitermayer Galvão Reis
Albert Icksang Ko
James E. Childs
Eduardo M. daSilva
Federico Costa
Mike Begon
Coinfection modifies carriage of enzootic and zoonotic parasites in Norway rats from an urban slum
Ecosphere
Angiostrongylus cantonensis
coinfection
helminths
interaction network
Leptospira interrogans
Nippostrongylus brasiliensis
title Coinfection modifies carriage of enzootic and zoonotic parasites in Norway rats from an urban slum
title_full Coinfection modifies carriage of enzootic and zoonotic parasites in Norway rats from an urban slum
title_fullStr Coinfection modifies carriage of enzootic and zoonotic parasites in Norway rats from an urban slum
title_full_unstemmed Coinfection modifies carriage of enzootic and zoonotic parasites in Norway rats from an urban slum
title_short Coinfection modifies carriage of enzootic and zoonotic parasites in Norway rats from an urban slum
title_sort coinfection modifies carriage of enzootic and zoonotic parasites in norway rats from an urban slum
topic Angiostrongylus cantonensis
coinfection
helminths
interaction network
Leptospira interrogans
Nippostrongylus brasiliensis
url https://doi.org/10.1002/ecs2.2887
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