Vector competence, vectorial capacity of Nyssorhynchus darlingi and the basic reproduction number of Plasmodium vivax in agricultural settlements in the Amazonian Region of Brazil

Abstract

Background: Brazilian malaria control programmes successfully reduced the incidence and mortality rates from 2005 to 2016. Since 2017, increased malaria has been reported across the Amazon. Few field studies focus on the primary malaria vector in high to moderate endemic areas, Nyssorhynchus darlingi, as the key entomological component of malaria risk, and on the metrics of Plasmodium vivax propagation in Amazonian rural communities. Methods: Human landing catch collections were carried out in 36 houses of 26 communities in five municipalities in the Brazilian states of Acre, Amazonas and Rondonia states, with API (>30). In addition, data on the number of locally acquired symptomatic infections were employed in mathematical modelling analyses carried out to determine Ny. darlingi vector competence and vectorial capacity to P. vivax; and to calculate the basic reproduction number for P. vivax. Results: Entomological indices and malaria metrics ranged among localities: prevalence of P. vivax infection in Ny. darlingi, from 0.243% in Mancio Lima, Acre to 3.96% in Machadinho D'Oeste, Rondonia; daily human-biting rate per person from 23 +/- 1.18 in Cruzeiro do Sul, Acre, to 66 +/- 2.41 in Labrea, Amazonas; vector competence from 0.00456 in Sao Gabriel da Cachoeira, Amazonas to 0.04764 in Mancio Lima, Acre; vectorial capacity from 0.0836 in Mancio Lima, to 1.5 in Machadinho D'Oeste. The estimated R-0 for P. vivax (PvR(0)) was 3.3 in Mancio Lima, 7.0 in Labrea, 16.8 in Cruzeiro do Sul, 55.5 in Sao Gabriel da Cachoeira, and 58.7 in Machadinho D'Oeste. Correlation between P. vivax prevalence in Ny. darlingi and vector competence was non-linear whereas association between prevalence of P. vivax in mosquitoes, vectorial capacity and R-0 was linear and positive. Conclusions: In spite of low vector competence of Ny. darlingi to P. vivax, parasite propagation in the human population is enhanced by the high human-biting rate, and relatively high vectorial capacity. The high PvR(0) values suggest hyperendemicity in Machadinho D'Oeste and SAo Gabriel da Cachoeira at levels similar to those found for P. falciparum in sub-Saharan Africa regions. Mass screening for parasite reservoirs, effective anti-malarial drugs and vector control interventions will be necessary to shrinking transmission in Amazonian rural communities, Brazil.