Natural arbovirus infection rate and detectability of indoor female Aedes aegypti from Mérida, Yucatán, Mexico

Abstract

Arbovirus infection in Aedes aegypti has historically been quantified from a sample of the adult population by pooling collected mosquitoes to increase detectability. However, there is a significant knowledge gap about the magnitude of natural arbovirus infection within areas of active transmission, as well as the sensitivity of detection of such an approach. We used indoor Ae. aegypti sequential sampling with Prokopack aspirators to collect all mosquitoes inside 200 houses with suspected active ABV transmission from the city of Mérida, Mexico, and tested all collected specimens by RT-PCR to quantify: a) the absolute arbovirus infection rate in individually tested Ae. aegypti females; b) the sensitivity of using Prokopack aspirators in detecting ABV-infected mosquitoes; and c) the sensitivity of entomological inoculation rate (EIR) and vectorial capacity (VC), two measures ABV transmission potential, to different estimates of indoor Ae. aegypti abundance. The total number of Ae. aegypti (total catch, the sum of all Ae. aegypti across all collection intervals) as well as the number on the first 10-min of collection (sample, equivalent to a routine adult aspiration session) were calculated. We individually tested by RT-PCR 2,161 Aedes aegypti females and found that 7.7% of them were positive to any ABV. Most infections were CHIKV (77.7%), followed by DENV (11.4%) and ZIKV (9.0%). The distribution of infected Aedes aegypti was overdispersed; 33% houses contributed 81% of the infected mosquitoes. A significant association between ABV infection and Ae. aegypti total catch indoors was found (binomial GLMM, Odds Ratio > 1). A 10-min indoor Prokopack collection led to a low sensitivity of detecting ABV infection (16.3% for detecting infected mosquitoes and 23.4% for detecting infected houses). When averaged across all infested houses, mean EIR ranged between 0.04 and 0.06 infective bites per person per day, and mean VC was 0.6 infectious vectors generated from a population feeding on a single infected host per house/day. Both measures were significantly and positively associated with Ae. aegypti total catch indoors. Our findings provide evidence that the accurate estimation and quantification of arbovirus infection rate and transmission risk is a function of the sampling effort, the local abundance of Aedes aegypti and the intensity of arbovirus circulation.

Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1. Distribution of the number of female Ae. aegypti positive for CHIKV, DENV and ZIKV per house with positive mosquitoes collected in the ABV transmission seasons of 2016 and 2017 from Yucatán, Mexico.

Fig 2. Percentage of houses infested with female Ae. aegypti positive for any of the three targeted viruses in low-density (<10 total mosquitos per house, n = 98) and high-density (> 10 total mosquitoes per house, n = 70) premises, estimated from Ae. aegypti collected indoors during the ABV transmission seasons of 2016 and 207 in Yucatán, Mexico.

Panel A shows houses with positive bodies and heads and panel B shows the percentage of houses where only heads were positive. The variable co-occurrence contains percentages of houses where mosquitoes where positive for either virus within the same house, including three positive mosquitoes with coinfection between CHIKV and ZIKV.

Fig 3. Predicted probability of ABV infection in female Ae. aeypti.

Probability of detecting an infected female Ae. aegypti (0, uninfected, 1, infected) as a function of the total Ae. aegypti catch per house with evidence of recent arbovirus human infection, estimated from collections conducted during the ABV transmission seasons of 2016 and 2017 in Yucatán, Mexico. Solid line represents the mean prediction from a binomial generalized linear mixed effects model and gray band the 95% CI of the prediction, dots indicate the binomial data, with dark dots showing the occurrence of multiple (overlapping) observations.

Fig 4. Sensitivity of indoor adult aspiration to the detection of ABV-positive Ae. aegypti.

A) Cumulative probability of detecting houses with positive female Ae. aegypti (body and head) and B) cumulative probability of detecting positive female Ae. aegypti (body and head) for Chikungunya (CHIKV), Dengue (DENV) and/or Zika (ZIKV) in house as the collection effort increases in 10-min intervals. Estimates obtained from collections conducted indoors during the ABV transmission seasons of 2016 and 2017 in Yucatán, Mexico.

Fig 5. Household-level estimates of ABV transmission potential.

The proportion of vectors per host (m), entomologic inoculation rate (EIR) and vectorial capacity (VC) were calculated per house and used to compare estimated between the first 10-min collection (sample) and the Ae. aegypti total catch (Total)(panels A, C, E). Panels B, D and F show the association between total Ae. aegypti female abundance per house, and estimates of m, EIR and VC, respectively. Lines show the fit and confidence interval of a generalized-linear mixed model fitted to the data (S3 Table).