**5. Challenges to entomological surveillance**

Entomological surveillance has been employed to (1) determine changes in the geographical distribution of *Ae. aegypti*, (2) obtain relative measurements of *Ae. aegypti* populations through time and identify areas of "high" infestation or periods of growth in vector populations and (3) evaluate the impact of anti-vector interventions. These indicators cannot be used straightforwardly to estimate the risk of virus transmission in the population at a certain time or location.

The limitations of these methods for measuring mosquito populations are the absence of a "gold standard," the fact that all measurements have a range of error (they are not precise) and that only a proportion of the total mosquito population (eggs, larvae or adults) is measured. Furthermore, it must be understood that the risk of transmission can occur in various locations and not necessarily where the measurement and/or intervention is performed and that in the selection of methods of measurement and entomological monitoring, precision is always sacrificed. This is to say that, despite being less precise, easier and cheaper methods are chosen over those (e.g., adult surveys) that require more resources and thus are more

Challenges for the Introduction and Evaluation of the Impact of Innovative *Aedes aegypti*…

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An additional challenge is the combination of strategies (not yet their integration) and the differentiated evaluation of their impact, since while one intervention can modify the physical availability of breeding sites, it does not necessarily result in a decrease of vector density nor control the most stable and productive breeding sites. On the other hand, there is insufficient evidence to support the idea that achieving a lower egg or larval density through a variety of available interventions has an impact on the rate of disease transmission. Nevertheless, the combined use of old strategies and/or the incorporation of new vector control tools imposes various challenges: (1) the use of indicators that measure more specifically the density of mosquitoes in all stages of development in order to more concretely evaluate all available modes of intervention, (2) the definition of risk thresholds and (3) that the programs demonstrate their capacity (in terms of human resources, equipment and finances) to be executed with the

The evaluation of interventions to control *Ae. aegypti* faces diverse challenges regarding the potential impact they may have on the risk of transmission not only of dengue but also of other arboviruses recently associated with the region's epidemiological profile: Zika, chikungunya and yellow fever. The first challenge is estimating the impact derived from the disease that may be affected and the second in measuring the direct impact of the interventions on the vector populations in all of their stages and their relation to transmission risk (vectorial

Systems of epidemiological surveillance now have the task of measuring, in the most precise manner possible, three infections transmitted by *Ae. aegypti*. Now things are complicated because the syndrome of fever and exanthema may be indicative of dengue, Zika and chikungunya. The diseases are also associated with other signs, distinctive symptoms and highly specific clinical complications (hemorrhages with severe dengue, chronic arthralgia with the chikungunya virus and congenital syndromes and neurological complications with Zika).

The estimate of the actual number of dengue cases, and now of Zika and chikungunya, is very difficult to calculate due to *biological problems* inherent to the infection, such as the number asymptomatic infections, or of unspecified fevers, which hinders the correct quantification of the impact of each of these illnesses. Clinical confusion regarding symptomatic

coverage and frequency necessary to make them valid [1, 2].

**6. Challenges to epidemiological surveillance**

competence and capacity).

expensive [32].

*Entomological indexes*: There are various indicators (indexes) and methods to detect or monitor *Aedes* populations (egg, larval, pupal and adult stages) in relation to their location (containers, home or geographical area). The indicators were initially qualitative (negative/positive breeding sites or houses) and evolved toward being quantitative in order to identify the number of mosquitoes, though without specifying density, productivity or breeding site relevance (cryptic). The indices are not sufficiently exact to identify the risk of transmission [14].

One element of the evolution of control programs has been the slow innovation of entomological monitoring indicators, an area dominated by the traditional *Stegomyia* indexes used in the campaign to eliminate *Ae. aegypti* in the fight against yellow fever: house (HI), container (CI) and Breteau (BI) indexes. These indices were useful in the extent to which they indicated the (qualitative) presence and absence of the vector in a campaign that sought its elimination and attempted to evaluate the endeavors toward physical elimination of breeding sites (positive breeding sites or houses). The focus now turned toward the reduction in density (rather than the elimination) of the vector, and these indicators have lost their usefulness [15, 16].

The need for better indicators led to indices of pupae and oviposition, closer life stages to the ideal measure of adult (female) mosquito populations, which would allow for a better approximation of the estimated risk of transmitting dengue [17, 18]. These indicators of entomological risk did not reduce or eliminate the challenges to evaluate the interventions because the need to relate density and/or the threshold of the different vector stages to risk of transmission still persists [19–21].

The use of "nonentomological" (though associated with infestation and facilitators of vectorhuman contact and epidemiological risk) indicators has also been proposed and ought to be considered in order to better understand the dynamics of dengue transmission—for example, density and distribution of human populations, socioeconomic conditions, living and public services, climate, etc. [22–27].

The selection of indicators and surveillance methods depends on the objective of surveillance (density reduction, risk detection and outbreak prevention), the levels of infestation and the capacity for implementation. Nevertheless, there is little evidence showing that the control programs employ systematic monitoring of vector populations—in particular, monitoring of adult females—in order to measure infestation and risk of dengue transmission [18, 28, 29]. In the best of cases, programs still employ indices of infested sites/breeding sites [29, 30] in order to establish "areas" of transmission risk without demonstrating the predictive capacity of these indices as indicators of dengue transmission risk in the last 50 years [31].

The limitations of these methods for measuring mosquito populations are the absence of a "gold standard," the fact that all measurements have a range of error (they are not precise) and that only a proportion of the total mosquito population (eggs, larvae or adults) is measured. Furthermore, it must be understood that the risk of transmission can occur in various locations and not necessarily where the measurement and/or intervention is performed and that in the selection of methods of measurement and entomological monitoring, precision is always sacrificed. This is to say that, despite being less precise, easier and cheaper methods are chosen over those (e.g., adult surveys) that require more resources and thus are more expensive [32].

An additional challenge is the combination of strategies (not yet their integration) and the differentiated evaluation of their impact, since while one intervention can modify the physical availability of breeding sites, it does not necessarily result in a decrease of vector density nor control the most stable and productive breeding sites. On the other hand, there is insufficient evidence to support the idea that achieving a lower egg or larval density through a variety of available interventions has an impact on the rate of disease transmission. Nevertheless, the combined use of old strategies and/or the incorporation of new vector control tools imposes various challenges: (1) the use of indicators that measure more specifically the density of mosquitoes in all stages of development in order to more concretely evaluate all available modes of intervention, (2) the definition of risk thresholds and (3) that the programs demonstrate their capacity (in terms of human resources, equipment and finances) to be executed with the coverage and frequency necessary to make them valid [1, 2].
