Higher risk of malaria transmission outdoors than indoors by Nyssorhynchus darlingi in riverine communities in the Peruvian Amazon

Abstract

Background: Malaria remains an important public health problem in Peru where incidence has been increasing since 2011. Of over 55,000 cases reported in 2017, Plasmodium vivax was the predominant species (76%), with P. falciparum responsible for the remaining 24%. Nyssorhynchus darlingi (previously Anopheles darlingi) is the main vector in Amazonian Peru, where hyperendemic Plasmodium transmission pockets have been found. Mazán district has pronounced spatial heterogeneity of P. vivax malaria. However, little is known about behavior, ecology or seasonal dynamics of Ny. darlingi in Mazán. This study aimed to gather baseline information about bionomics of malaria vectors and transmission risk factors in a hyperendemic malaria area of Amazonian Peru.

Methods: To assess vector biology metrics, five surveys (two in the dry and three in the rainy season), including collection of sociodemographic information, were conducted in four communities in 2016-2017 on the Napo (Urco Miraño, URC; Salvador, SAL) and Mazán Rivers (Visto Bueno, VIB; Libertad, LIB). Human-biting rate (HBR), entomological inoculation rate (EIR) and human blood index (HBI) were measured to test the hypothesis of differences in entomological indices of Ny. darlingi between watersheds. A generalized linear mixed effect model (GLMM) was constructed to model the relationship between household risk factors and the EIR.

Results: Nyssorhynchus darlingi comprised 95% of 7117 Anophelinae collected and its abundance was significantly higher along the Mazán River. The highest EIRs (3.03-4.54) were detected in March and June in URC, LIB and VIB, and significantly more Ny. darlingi were infected outdoors than indoors. Multivariate analysis indicated that the EIR was >12 times higher in URC compared with SAL. The HBI ranged from 0.42-0.75; humans were the most common blood source, followed by Galliformes and cows. There were dramatic differences in peak biting time and malaria incidence with similar bednet coverage in the villages.

Conclusions: Nyssorhynchus darlingi is the predominant contributor to malaria transmission in the Mazán District, Peru. Malaria risk in these villages is higher in the peridomestic area, with pronounced heterogeneities between and within villages on the Mazán and the Napo Rivers. Spatiotemporal identification and quantification of the prevailing malaria transmission would provide new evidence to orient specific control measures for vulnerable or at high risk populations.

Keywords: Blood meal source; Entomological inoculation rate; GLMM; Human blood index; Mazán District; Nyssorhynchus darlingi; Peruvian Amazon; Plasmodium.

Fig. 1

Map showing mosquito collection sites on the Mazán and Napo Rivers, Mazán District, Loreto Department, Amazonian Peru, 2016–2017

Fig. 2

Mean indoor (intradomestic) and outdoor (peridomestic) human-biting rate at four communities in the Mazán District 2016–2017. a Salvador (SAL). b Urco Miraño (URC). c Libertad (LIB). d Visto Bueno (VIB). No specimens were collected in November and March 2017 in Salvador or in November 2016 in Urco Miraño. Right Y-axis is the human-biting rate. Grey background shading represents the proportion of the human population under bednets (left Y-axis) each hour of the night (X-axis)

Fig. 3

Quantitative interaction network of Ny. darlingi blood meal sources in SAL, URC, LIB and VIB, 2016–2017. Network is constructed based on blood meal source analysis for 622 Ny. darlingi females

Fig. 4

Proportion of blood meal sources based on Ny. darlingi collected by barrier screens in Mazán District between 2016 and 2017