Differential contribution of Anopheles coustani and Anopheles arabiensis to the transmission of Plasmodium falciparum and Plasmodium vivax in two neighbouring villages of Madagascar

Abstract

Background: Malaria is still a heavy public health concern in Madagascar. Few studies combining parasitology and entomology have been conducted despite the need for accurate information to design effective vector control measures. In a Malagasy region of moderate to intense transmission of both Plasmodium falciparum and P. vivax, parasitology and entomology have been combined to survey malaria transmission in two nearby villages.

Methods: Community-based surveys were conducted in the villages of Ambohitromby and Miarinarivo at three time points (T1, T2 and T3) during a single malaria transmission season. Human malaria prevalence was determined by rapid diagnostic tests (RDTs), microscopy and real-time PCR. Mosquitoes were collected by human landing catches and pyrethrum spray catches and the presence of Plasmodium sporozoites was assessed by TaqMan assay.

Results: Malaria prevalence was not significantly different between villages, with an average of 8.0% by RDT, 4.8% by microscopy and 11.9% by PCR. This was mainly due to P. falciparum and to a lesser extent to P. vivax. However, there was a significantly higher prevalence rate as determined by PCR at T2 ([Formula: see text] = 7.46, P = 0.025). Likewise, mosquitoes were significantly more abundant at T2 ([Formula: see text] = 64.8, P < 0.001), especially in Ambohitromby. At T1 and T3 mosquito abundance was higher in Miarinarivo than in Ambohitromby ([Formula: see text] = 14.92, P < 0.001). Of 1550 Anopheles mosquitoes tested, 28 (1.8%) were found carrying Plasmodium sporozoites. The entomological inoculation rate revealed that Anopheles coustani played a major contribution in malaria transmission in Miarinarivo, being responsible of 61.2 infective bites per human (ib/h) during the whole six months of the survey, whereas, it was An. arabiensis, with 36 ib/h, that played that role in Ambohitromby.

Conclusions: Despite a similar malaria prevalence in two nearby villages, the entomological survey showed a different contribution of An. coustani and An. arabiensis to malaria transmission in each village. Importantly, the suspected secondary malaria vector An. coustani, was found playing the major role in malaria transmission in one village. This highlights the importance of combining parasitology and entomology surveys for better targeting local malaria vectors. Such study should contribute to the malaria pre-elimination goal established under the 2018-2022 National Malaria Strategic Plan.

Keywords: Andriba; Anopheles arabiensis; Anopheles coustani; Madagascar; Plasmodium falciparum; Plasmodium vivax; Vector biology dynamics.

Fig. 1

Study site. The map of Madagascar is depicted in the left panel with a focus on the Andriba region presented in more details in the upper right panel. The bottom right panel is a satellite image of the study villages, Ambohitromby and Miarinarivo (Modified Copernicus Sentinel data [2019]/Sentinel Hub)

Fig. 2

Typical Malagasy houses in Andriba rural area. The houses are built with adobe walls and thatched roofs, and usually composed of one or two rooms. The picture was taken in the village of Ambohitromby located in the rural commune of Andriba, Madagascar

Fig. 3

Indoor and outdoor human-biting rate of malaria vectors at the three time points in Ambohitromby and Miarinarivo. Light numbers within the graphs indicate the mean bite per human and per night for each of the four Anopheles species

Fig. 4

Hourly biting rate of malaria vectors at the three time points in Ambohitromby and Miarinarivo. Data represent both indoor and outdoor HLCs collected mosquitoes

Fig. 5

Variation of the density and EIR of An. arabiensis and An. coustani over time in Ambohitromby and Miarinarivo. Prev: human malaria prevalence

Fig. 6

Malaria prevalence in Ambohitromby and Miarinarivo in 2016, 2017 and 2018. Data were collected from asymptomatic school-aged children tested with RDT in March each year (at T2). P values < 0.05 are significant; n: sample size