Quantifying Seasonal and Diel Variation in Anopheline and Culex Human Biting Rates in Southern Ecuador Sadie J
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Ryan et al. Malar J (2017) 16:479 DOI 10.1186/s12936-017-2121-4 Malaria Journal RESEARCH Open Access Quantifying seasonal and diel variation in Anopheline and Culex human biting rates in Southern Ecuador Sadie J. Ryan1,2,3,4* , Catherine A. Lippi1,2* , Philipp H. Boersch‑Supan1,2,5 , Naveed Heydari3, Mercy Silva6, Jeferson Adrian3, Leonardo F. Noblecilla7, Efraín B. Ayala8, Mayling D. Encalada9, David A. Larsen10, Jesse T. Krisher11, Lyndsay Krisher12,13, Lauren Fregosi1,10 and Anna M. Stewart‑Ibarra3 Abstract Background: Quantifying mosquito biting rates for specifc locations enables estimation of mosquito-borne disease risk, and can inform intervention eforts. Measuring biting itself is fraught with ethical concerns, so the landing rate of mosquitoes on humans is often used as a proxy measure. Southern coastal Ecuador was historically endemic for malaria (Plasmodium falciparum and Plasmodium vivax), although successful control eforts in the 2000s eliminated autochthonous transmission (since 2011). This study presents an analysis of data collected during the elimination period. Methods: Human landing catch (HLC) data for three mosquito taxa: two malaria vectors, Anopheles albimanus and Anopheles punctimacula, and grouped Culex spp. were examined for this study. These data were collected by the National Vector Control Service of the Ministry of Health over a 5-year time span (2007–2012) in fve cities in southern coastal Ecuador, at multiple households, in all months of the year, during dusk–dawn (18:00–6:00) hours, often at both indoor and outdoor locations. Hurdle models were used to determine if biting activity was fundamentally diferent for the three taxa, and to identify spatial and temporal factors infuencing bite rate. Due to the many diferent approaches to studying and quantifying bite rates in the literature, a glossary of terms was created, to facilitate comparative stud‑ ies in the future. Results: Biting trends varied signifcantly with species and time. All taxa exhibited exophagic feeding behavior, and outdoor locations increased both the odds and incidence of bites across taxa. Anopheles albimanus was most frequently observed biting, with an average of 4.7 bites/h. The highest and lowest respective months for signifcant biting activity were March and July for An. albimanus, July and August for An. punctimacula, and February and July for Culex spp. Conclusions: Fine-scale diferences in endophagy and exophagy, and temporal diferences among months and hours exist in biting patterns among mosquito taxa in southern coastal Ecuador. This analysis provides detailed information for targeting vector control activities, and household level vector prevention strategies. These data were collected as part of routine vector surveillance conducted by the Ministry of Health, and such data have not been collected since. Reinstating such surveillance measures would provide important information to aid in preventing malaria re-emergence. Keywords: Anopheles albimanus, Anopheles punctimacula, Bite rate, Ecuador, Malaria, Culex *Correspondence: [email protected]; [email protected] 1 Emerging Pathogens Institute, University of Florida, Gainesville, FL, USA Full list of author information is available at the end of the article © The Author(s) 2017. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided 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 Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Ryan et al. Malar J (2017) 16:479 Page 2 of 10 Background so. Tus, a simplifed attempt to quantify potential dis- Despite major eforts to control and eliminate vector- ease transmission is the development of human bite rate borne diseases through vector control, mosquito-borne (HBR) and landing rate (LR) indices, generally described diseases such as malaria, dengue, yellow fever, and now as the number of mosquitoes of a species respectively chikungunya and zika virus remain a major threat to exhibiting feeding or resting behaviour on a human people’s livelihoods in the Americas. An estimated 108 recorded for a given location and time period [20–22]. million people per year are at risk for malaria infections Although used for estimating the number of female mos- in the Americas, pointing to a need to maintain elimina- quitoes that are attempting to take blood meals in feld or tion status in areas that have successfully eliminated local laboratory conditions, there is a great deal of variability infections, and to prevent reestablishment [1]. In Latin in the literature with regards to the defnitions and feld America there is high endemic diversity in both vectors protocols associated with these metrics. and pathogens, including three species of malaria-caus- A glossary of biting rate terms encountered in the liter- ing parasites, Plasmodium vivax, Plasmodium falcipa- ature was developed, to facilitate communication of def- rum, and Plasmodium malariae [1–4]. To monitor and nitions, as a means to both measure and interpret study measure the potential for mosquito-borne transmission, fndings for comparison (Table 1). In general, the pro- it is important to assess the risk or rate of infectious bites tocol for HBR and LR studies involves an initial survey on humans. Tere are many challenges associated with for potential sites, a species inventory to establish vector the direct surveillance of pathogens, such as Plasmodium, presence, training feld entomology technicians in identi- in mosquito populations, thus vector-borne diseases are fcation of species and behaviours, and establishing spa- often monitored in terms of human case data [5–7]. Te tial points and temporal intervals for data collection [23]. reliance on human cases to monitor vector-borne dis- Like raw mosquito density, HBR and LR do not directly ease outbreaks is subject to many forms of reporting bias, measure infections, but these indices are often cited as and these biases may be further exacerbated in Ecuador, a proxy for species presence, density of blood-seeking where disparities in clinical access may contribute to females, and the capacity for disease transmission [23, underreporting of cases, as is seen with dengue [8–10]. 24]. Potential issues with HBR include reliance on visual Even when clinical access is more widely available, as in identifcation of mosquito species, inter-observer agree- urban areas, much of the public health data reported by ment, and exposure of workers to pathogens [25–28]. Ecuador’s Ministry of Health relies on suspected clini- Human landing catch (HLC), wherein mosquitoes cal cases rather than laboratory confrmation [11]. Fur- counted in the landing rate survey are captured and later thermore, human case data does not provide information examined in the lab, can overcome most of these obsta- in sufcient time to target vector control to mosquito cles, but at the cost of additional feld and laboratory activity. Although malaria surveillance and diagnostics resources [22]. Depending on study design and data col- in Ecuador are much stronger relative to those of other lection protocol, bite rate indices have the potential to mosquito-borne diseases, detection of asymptomatic provide a wealth of information regarding vector behav- malaria and cases in remission remain a challenge to sur- iour at very fne spatial and temporal scales in a manner veillance and disease elimination [12, 13]. that is both relatively cost-efective and efcient. Measuring force of infection, or transmission risk of Ecuador’s southern El Oro province (Fig. 1) has been mosquito-borne diseases through models of vital rates free of locally acquired malaria infections since 2011, [14–17], require knowledge of many components of although the mosquito species capable of vectoring P. the transmission cycle, including biting rates. Te ento- vivax and P. falciparum malaria are still prevalent in the mological inoculation rate (EIR) is commonly used as a area [13]. Disease surveillance and control programmes means of describing potential risk of infection from vec- in developing countries typically sufer from limited tor-borne diseases; this is the rate of infectious bites per resources in the face of high disease burden, however person per day, usually estimated, or derived from biting the Ecuadorian government has devoted a great deal of rates and a measure of vector infection prevalence. EIR funding and logistic support to their Ministry of Health is considered a more direct measure of infection inten- specifcally for the detection and control of malaria fol- sity than human incidence or other traditional epidemio- lowing a resurgence of the disease in the late 1990s, logical measures [18, 19]. However, in low-transmission which has been previously described in detail [13]. Nev- situations, estimating sporozoite rates is stymied by ertheless, with recent outbreaks of malaria occurring in large statistical error range, and thus biting rate is a bet- other Ecuadorian provinces and neighbouring countries, ter means of estimating transmission. Clearly, measuring the potential for re-emergence of malaria in El Oro cre- the rate of infection in vectors can be logistically com-