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

Abstract

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.

Trypanosomatid infections in captive wild mammals and potential vectors at the Brasilia Zoo, Federal District, Brazil

“…We identified triatomines using dichotomic keys (Lent & Wygodzinsky, ). We examined the faeces of the collected triatomines by optical microscopy according to Minuzzi‐Souza et al (); fresh (400x) and Giemsa 10%‐stained (1000x) hindgut contents were examined to detect T. cruzi (Cuba Cuba, ).…”

“…We extracted DNA from blood samples (300 μl) according to the recommendations of the Biopur DNA Extraction Kit (Biometrix). We extracted DNA from triatomines (intestinal tissues) and sandflies (female thoraces and proximal abdominal segments) with the Illustra Tissue and Cells Genomic kit (GE Healthcare), according to Minuzzi‐Souza et al () and Machado et al (), respectively. We quantified DNA samples with the NanoVue™ Plus Spectrophotometer (GE Healthcare) using the wavelength 220–330 nm; the data were expressed in ng/μL.…”

“…A standard curve was taken for absolute quantification of the samples. The curve was based on cycle quantification values of different concentrations of T. cruzi DNA extracted from cultures (Berenice strain) according to Minuzzi‐Souza et al (). We detected Leishmania in individual female sandflies by quantitative PCR of the first internal transcribed spacer of the ribosomal DNA (rDNA ITS‐qPCR) using the primers, 219 F (5′‐AGC TGG ATC ATT TTC CGA TG‐3′) and 219R (5′‐ATC GCG ACA CGT TAT GTG AG‐3′) (Talmi‐Frank et al, ) that amplify a fragment of 265‐288bp.…”

“…In the Federal District of Brazil (FD hereafter), estimates indicate high rates of triatomine infection by T . cruzi (Minuzzi‐Souza et al, ), which may be related to the enzootic transmission of this parasite in gallery forests. For example, 33% of 18 white‐eared opossums ( Didelphis albiventris ) were infected by T .…”

Factors associated with the presence of triatomines in rural areas of south Argentine Chaco

“…The low percentage of domiciliary infestations found in this work is probably not only due to a few vulnerable houses recorded in the study area, but also due to the low sensitivity of the manual method used for searching for triatomines (hour-man technique). Previous investigations of routine surveillance systems used in the context of detecting vector-borne diseases like Chagas, have shown that these systems have sensitivity estimates frequently below 50%, likely resulting in underestimates in the real infestation vector numbers 36,37 . Historically, the house has been considered a risk factor, especially those houses whose structure offers suitable refuge for triatomines.…”