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Surveillance of vector-borne pathogens under imperfect detection: lessons from Chagas disease risk (mis)measurement

Vector-borne pathogens threaten human health worldwide. Despite their critical role in disease prevention, routine surveillance systems often rely on low-complexity pathogen detection tests of uncertain accuracy. In Chagas disease surveillance, optical microscopy (OM) is routinely used for detecting...

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Autores principales: Minuzzi-Souza, Thaís Tâmara Castro, Nitz, Nadjar, Cuba, César Augusto Cuba, Hagström, Luciana, Hecht, Mariana Machado, Santana, Camila, Ribeiro, Marcelle, Vital, Tamires Emanuele, Santalucia, Marcelo, Knox, Monique, Obara, Marcos Takashi, Abad-Franch, Fernando, Gurgel-Gonçalves, Rodrigo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5760667/
https://www.ncbi.nlm.nih.gov/pubmed/29317702
http://dx.doi.org/10.1038/s41598-017-18532-2
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author Minuzzi-Souza, Thaís Tâmara Castro
Nitz, Nadjar
Cuba, César Augusto Cuba
Hagström, Luciana
Hecht, Mariana Machado
Santana, Camila
Ribeiro, Marcelle
Vital, Tamires Emanuele
Santalucia, Marcelo
Knox, Monique
Obara, Marcos Takashi
Abad-Franch, Fernando
Gurgel-Gonçalves, Rodrigo
author_facet Minuzzi-Souza, Thaís Tâmara Castro
Nitz, Nadjar
Cuba, César Augusto Cuba
Hagström, Luciana
Hecht, Mariana Machado
Santana, Camila
Ribeiro, Marcelle
Vital, Tamires Emanuele
Santalucia, Marcelo
Knox, Monique
Obara, Marcos Takashi
Abad-Franch, Fernando
Gurgel-Gonçalves, Rodrigo
author_sort Minuzzi-Souza, Thaís Tâmara Castro
collection PubMed
description Vector-borne pathogens threaten human health worldwide. Despite their critical role in disease prevention, routine surveillance systems often rely on low-complexity pathogen detection tests of uncertain accuracy. In Chagas disease surveillance, optical microscopy (OM) is routinely used for detecting Trypanosoma cruzi in its vectors. Here, we use replicate T. cruzi detection data and hierarchical site-occupancy models to assess the reliability of OM-based T. cruzi surveillance while explicitly accounting for false-negative and false-positive results. We investigated 841 triatomines with OM slides (1194 fresh, 1192 Giemsa-stained) plus conventional (cPCR, 841 assays) and quantitative PCR (qPCR, 1682 assays). Detections were considered unambiguous only when parasitologists unmistakably identified T. cruzi in Giemsa-stained slides. qPCR was >99% sensitive and specific, whereas cPCR was ~100% specific but only ~55% sensitive. In routine surveillance, examination of a single OM slide per vector missed ~50–75% of infections and wrongly scored as infected ~7% of the bugs. qPCR-based and model-based infection frequency estimates were nearly three times higher, on average, than OM-based indices. We conclude that the risk of vector-borne Chagas disease may be substantially higher than routine surveillance data suggest. The hierarchical modelling approach we illustrate can help enhance vector-borne disease surveillance systems when pathogen detection is imperfect.
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spelling pubmed-57606672018-01-17 Surveillance of vector-borne pathogens under imperfect detection: lessons from Chagas disease risk (mis)measurement Minuzzi-Souza, Thaís Tâmara Castro Nitz, Nadjar Cuba, César Augusto Cuba Hagström, Luciana Hecht, Mariana Machado Santana, Camila Ribeiro, Marcelle Vital, Tamires Emanuele Santalucia, Marcelo Knox, Monique Obara, Marcos Takashi Abad-Franch, Fernando Gurgel-Gonçalves, Rodrigo Sci Rep Article Vector-borne pathogens threaten human health worldwide. Despite their critical role in disease prevention, routine surveillance systems often rely on low-complexity pathogen detection tests of uncertain accuracy. In Chagas disease surveillance, optical microscopy (OM) is routinely used for detecting Trypanosoma cruzi in its vectors. Here, we use replicate T. cruzi detection data and hierarchical site-occupancy models to assess the reliability of OM-based T. cruzi surveillance while explicitly accounting for false-negative and false-positive results. We investigated 841 triatomines with OM slides (1194 fresh, 1192 Giemsa-stained) plus conventional (cPCR, 841 assays) and quantitative PCR (qPCR, 1682 assays). Detections were considered unambiguous only when parasitologists unmistakably identified T. cruzi in Giemsa-stained slides. qPCR was >99% sensitive and specific, whereas cPCR was ~100% specific but only ~55% sensitive. In routine surveillance, examination of a single OM slide per vector missed ~50–75% of infections and wrongly scored as infected ~7% of the bugs. qPCR-based and model-based infection frequency estimates were nearly three times higher, on average, than OM-based indices. We conclude that the risk of vector-borne Chagas disease may be substantially higher than routine surveillance data suggest. The hierarchical modelling approach we illustrate can help enhance vector-borne disease surveillance systems when pathogen detection is imperfect. Nature Publishing Group UK 2018-01-09 /pmc/articles/PMC5760667/ /pubmed/29317702 http://dx.doi.org/10.1038/s41598-017-18532-2 Text en © The Author(s) 2017 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Minuzzi-Souza, Thaís Tâmara Castro
Nitz, Nadjar
Cuba, César Augusto Cuba
Hagström, Luciana
Hecht, Mariana Machado
Santana, Camila
Ribeiro, Marcelle
Vital, Tamires Emanuele
Santalucia, Marcelo
Knox, Monique
Obara, Marcos Takashi
Abad-Franch, Fernando
Gurgel-Gonçalves, Rodrigo
Surveillance of vector-borne pathogens under imperfect detection: lessons from Chagas disease risk (mis)measurement
title Surveillance of vector-borne pathogens under imperfect detection: lessons from Chagas disease risk (mis)measurement
title_full Surveillance of vector-borne pathogens under imperfect detection: lessons from Chagas disease risk (mis)measurement
title_fullStr Surveillance of vector-borne pathogens under imperfect detection: lessons from Chagas disease risk (mis)measurement
title_full_unstemmed Surveillance of vector-borne pathogens under imperfect detection: lessons from Chagas disease risk (mis)measurement
title_short Surveillance of vector-borne pathogens under imperfect detection: lessons from Chagas disease risk (mis)measurement
title_sort surveillance of vector-borne pathogens under imperfect detection: lessons from chagas disease risk (mis)measurement
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5760667/
https://www.ncbi.nlm.nih.gov/pubmed/29317702
http://dx.doi.org/10.1038/s41598-017-18532-2
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