Toxoplasma gondii exposure in Brazilian indigenous populations, their dogs, environment, and healthcare professionals

Although Toxoplasma gondii exposure has been reported in indigenous populations worldwide, a One Health approach has not been applied to date. This study concurrently assessed T. gondii exposure in indigenous populations, and their dogs, environment, and indigenous or non-indigenous healthcare profe...

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Main Authors: Fernando Rodrigo Doline, João Henrique Farinhas, Leandro Meneguelli Biondo, Pollyanne Raysa Fernandes de Oliveira, Nássarah Jabur Lot Rodrigues, Karina Pavão Patrício, Rinaldo Aparecido Mota, Helio Langoni, Christina Pettan-Brewer, Rogério Giuffrida, Vamilton Alvares Santarém, Wagner Antônio Chiba de Castro, Andrea Pires dos Santos, Louise Bach Kmetiuk, Alexander Welker Biondo
Format: Article
Language:English
Published: Elsevier 2023-06-01
Series:One Health
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2352771423000873
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author Fernando Rodrigo Doline
João Henrique Farinhas
Leandro Meneguelli Biondo
Pollyanne Raysa Fernandes de Oliveira
Nássarah Jabur Lot Rodrigues
Karina Pavão Patrício
Rinaldo Aparecido Mota
Helio Langoni
Christina Pettan-Brewer
Rogério Giuffrida
Vamilton Alvares Santarém
Wagner Antônio Chiba de Castro
Andrea Pires dos Santos
Louise Bach Kmetiuk
Alexander Welker Biondo
author_facet Fernando Rodrigo Doline
João Henrique Farinhas
Leandro Meneguelli Biondo
Pollyanne Raysa Fernandes de Oliveira
Nássarah Jabur Lot Rodrigues
Karina Pavão Patrício
Rinaldo Aparecido Mota
Helio Langoni
Christina Pettan-Brewer
Rogério Giuffrida
Vamilton Alvares Santarém
Wagner Antônio Chiba de Castro
Andrea Pires dos Santos
Louise Bach Kmetiuk
Alexander Welker Biondo
author_sort Fernando Rodrigo Doline
collection DOAJ
description Although Toxoplasma gondii exposure has been reported in indigenous populations worldwide, a One Health approach has not been applied to date. This study concurrently assessed T. gondii exposure in indigenous populations, and their dogs, environment, and indigenous or non-indigenous healthcare professionals (HPs). Human and dog serum samples from 9 indigenous communities in Brazil were assessed by indirect immunofluorescence antibody test for anti-T. gondii antibodies. Soil samples (30 per community) were processed with PCR to amplify T. gondii DNA. Associated risk factors and seroprevalence were analyzed using logistic regression models. Human seropositivity and type of water source were assessed by generalized linear mixed model (GLMM) with binomial error distribution, and game meat consumption with chi-squared test. Overall, 225/463 (49%) indigenous persons were seropositive for anti-T. gondii antibodies. Of all the HPs, 67/168 (40%) were positive, and included 54/147 (37%) positive non-indigenous HPs. Indigenous persons more likely to be seropositive compared with non-indigenous HPs (OR: 1.63; 95% CI: 1.11–2.39). A total of 97/253 (38%) dogs were seropositive and highly associated with seropositive owners (p < 0.001). Based on univariate analysis for indigenous individuals, state location of community (p < 0.001), ethnicity (p < 0.001), consumption of game meat (p < 0.001), type of water source (p < 0.001), and educational level (p = 0.026) were associated with seropositivity. Logistic regression showed that indigenous seropositivity was associated with eating game meat (p = 0.002), drinking water from rivers (p < 0.001), and inversely proportional to the educational level. According to univariate analysis for non-indigenous HP, age (p = 0.005), frequency of visits to the indigenous populations (p < 0.001), consumption of water at the indigenous communities (p < 0.001), and ingestion of raw meat (p = 0.023) were associated with T. gondii seropositivity. Logistic regression revealed living outdoors (p = 0.042), habit of hunting (p = 0.008), and drinking river water (p = 0.007) as risk factors associated to seropositivity in dogs. In addition, indigenous communities lacking water treatment had higher seroprevalence for all groups including indigenous persons (GLMM; z = −7.153; p < 0.001), their dogs (GLMM; z = −2.405; p = 0.0162), and all HPs (GLMM; z = −2.420; p = 0.0155). Human seropositivity was associated with that of their dogs (p < 0.001). A single soil sample, out of 270 (0.37%), was positive for T. gondii by PCR. Our results indicate water source is a risk for human and dog toxoplasmosis in indigenous communities; both share similar exposure. Moreover, quality water access was shown to be crucial to prevent toxoplasmosis in both total and non-indigenous HPs who work in these indigenous communities.
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spelling doaj.art-a009be176cfe4d1094e6d7b67898d7a52023-06-13T04:12:33ZengElsevierOne Health2352-77142023-06-0116100567Toxoplasma gondii exposure in Brazilian indigenous populations, their dogs, environment, and healthcare professionalsFernando Rodrigo Doline0João Henrique Farinhas1Leandro Meneguelli Biondo2Pollyanne Raysa Fernandes de Oliveira3Nássarah Jabur Lot Rodrigues4Karina Pavão Patrício5Rinaldo Aparecido Mota6Helio Langoni7Christina Pettan-Brewer8Rogério Giuffrida9Vamilton Alvares Santarém10Wagner Antônio Chiba de Castro11Andrea Pires dos Santos12Louise Bach Kmetiuk13Alexander Welker Biondo14Graduate College of Cellular and Molecular Biology, Federal University of Paraná, Curitiba, PR, BrazilGraduate College of Cellular and Molecular Biology, Federal University of Paraná, Curitiba, PR, BrazilNational Institute of the Atlantic Forest (INMA), Brazilian Ministry of Science, Technology, and Innovation, Santa Teresa, Espirito Santo, BrazilGraduate College of Animal Bioscience, Federal Rural University of Pernambuco, Recife, PE, BrazilDepartment for Animal Production and Preventive Veterinary Medicine department for Animal Production and Preventive Veterinary Medicine, Botucatu, SP, BrazilDepartment of Public Health, Medical School, São Paulo State University, Botucatu, SP, BrazilGraduate College of Animal Bioscience, Federal Rural University of Pernambuco, Recife, PE, BrazilDepartment for Animal Production and Preventive Veterinary Medicine department for Animal Production and Preventive Veterinary Medicine, Botucatu, SP, BrazilDepartment of Comparative Medicine, School of Medicine, University of Washington, Seattle, WA, USALaboratory of Veterinary Parasitology, Veterinary Teaching Hospital, University of Western São Paulo, Presidente Prudente, SP, BrazilLaboratory of Veterinary Parasitology, Veterinary Teaching Hospital, University of Western São Paulo, Presidente Prudente, SP, BrazilLatin-American Institute of Life and Nature Sciences, Federal University for Latin American Integration, Foz do Iguaçu, PR, BrazilDepartment of Comparative Pathobiology, Purdue University, West Lafayette, IN, USADepartment of Comparative Pathobiology, Purdue University, West Lafayette, IN, USAGraduate College of Cellular and Molecular Biology, Federal University of Paraná, Curitiba, PR, Brazil; Department of Comparative Pathobiology, Purdue University, West Lafayette, IN, USAAlthough Toxoplasma gondii exposure has been reported in indigenous populations worldwide, a One Health approach has not been applied to date. This study concurrently assessed T. gondii exposure in indigenous populations, and their dogs, environment, and indigenous or non-indigenous healthcare professionals (HPs). Human and dog serum samples from 9 indigenous communities in Brazil were assessed by indirect immunofluorescence antibody test for anti-T. gondii antibodies. Soil samples (30 per community) were processed with PCR to amplify T. gondii DNA. Associated risk factors and seroprevalence were analyzed using logistic regression models. Human seropositivity and type of water source were assessed by generalized linear mixed model (GLMM) with binomial error distribution, and game meat consumption with chi-squared test. Overall, 225/463 (49%) indigenous persons were seropositive for anti-T. gondii antibodies. Of all the HPs, 67/168 (40%) were positive, and included 54/147 (37%) positive non-indigenous HPs. Indigenous persons more likely to be seropositive compared with non-indigenous HPs (OR: 1.63; 95% CI: 1.11–2.39). A total of 97/253 (38%) dogs were seropositive and highly associated with seropositive owners (p < 0.001). Based on univariate analysis for indigenous individuals, state location of community (p < 0.001), ethnicity (p < 0.001), consumption of game meat (p < 0.001), type of water source (p < 0.001), and educational level (p = 0.026) were associated with seropositivity. Logistic regression showed that indigenous seropositivity was associated with eating game meat (p = 0.002), drinking water from rivers (p < 0.001), and inversely proportional to the educational level. According to univariate analysis for non-indigenous HP, age (p = 0.005), frequency of visits to the indigenous populations (p < 0.001), consumption of water at the indigenous communities (p < 0.001), and ingestion of raw meat (p = 0.023) were associated with T. gondii seropositivity. Logistic regression revealed living outdoors (p = 0.042), habit of hunting (p = 0.008), and drinking river water (p = 0.007) as risk factors associated to seropositivity in dogs. In addition, indigenous communities lacking water treatment had higher seroprevalence for all groups including indigenous persons (GLMM; z = −7.153; p < 0.001), their dogs (GLMM; z = −2.405; p = 0.0162), and all HPs (GLMM; z = −2.420; p = 0.0155). Human seropositivity was associated with that of their dogs (p < 0.001). A single soil sample, out of 270 (0.37%), was positive for T. gondii by PCR. Our results indicate water source is a risk for human and dog toxoplasmosis in indigenous communities; both share similar exposure. Moreover, quality water access was shown to be crucial to prevent toxoplasmosis in both total and non-indigenous HPs who work in these indigenous communities.http://www.sciencedirect.com/science/article/pii/S2352771423000873Health inequitiesPublic healthWater quality
spellingShingle Fernando Rodrigo Doline
João Henrique Farinhas
Leandro Meneguelli Biondo
Pollyanne Raysa Fernandes de Oliveira
Nássarah Jabur Lot Rodrigues
Karina Pavão Patrício
Rinaldo Aparecido Mota
Helio Langoni
Christina Pettan-Brewer
Rogério Giuffrida
Vamilton Alvares Santarém
Wagner Antônio Chiba de Castro
Andrea Pires dos Santos
Louise Bach Kmetiuk
Alexander Welker Biondo
Toxoplasma gondii exposure in Brazilian indigenous populations, their dogs, environment, and healthcare professionals
One Health
Health inequities
Public health
Water quality
title Toxoplasma gondii exposure in Brazilian indigenous populations, their dogs, environment, and healthcare professionals
title_full Toxoplasma gondii exposure in Brazilian indigenous populations, their dogs, environment, and healthcare professionals
title_fullStr Toxoplasma gondii exposure in Brazilian indigenous populations, their dogs, environment, and healthcare professionals
title_full_unstemmed Toxoplasma gondii exposure in Brazilian indigenous populations, their dogs, environment, and healthcare professionals
title_short Toxoplasma gondii exposure in Brazilian indigenous populations, their dogs, environment, and healthcare professionals
title_sort toxoplasma gondii exposure in brazilian indigenous populations their dogs environment and healthcare professionals
topic Health inequities
Public health
Water quality
url http://www.sciencedirect.com/science/article/pii/S2352771423000873
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