Human IgG responses to Anopheles gambiae immunogenic salivary proteins in urban and rural populations of Burkina Faso: biomarkers of exposure to malaria vector bites

Abstract

Background: Malaria control would be greatly facilitated by the development of new tools for rapidly assessing malaria transmission intensity. In malaria-endemic areas such as Burkina Faso, human populations are frequently exposed to immunomodulatory salivary components injected during mosquito blood feeding. Numerous studies have examined parasite immunity; however, there are few data available on vector immunity as a means of assessing malaria transmission in sub-Saharan Africa. The present study aims to compare IgG-specific response to salivary gland extracts (SGE) of Anopheles gambiae (An. gambiae) in populations living in urban and rural areas in Burkina Faso.

Methods: A cross-sectional descriptive study was carried out in two sites, Ouagadougou city and Sapouy village, where blood samples (n = 676) from children (0-15 years) and adults were collected. After An. gambiae salivary protein isolation, the antibody (IgG) response to those SGE was evaluated by enzyme-linked immunosorbent assay (ELISA), representing a proxy of Anopheles exposure. The difference in antibody concentrations between groups was tested using parametric tests (Student's t-test and analysis of variance [ANOVA]) and the nonparametric Mann-Whitney U (Wilcoxon rank-sum) test. All differences were considered significant at P < 0.05.

Results: The study population consisted of 63.0% males and 37.0% females (average age = 31.2 ± 17.8 years). IgG antibodies against An. gambiae salivary protein were detected in all study participants. Urban participants demonstrated a greater mean IgG level to An. gambiae bites than rural (P < 0.0001). The mean IgG level was higher in secondary school children compared with primary school children (P < 0.0001). Organic cotton farmers held higher IgG to An. gambiae bites than conventional cotton farmers (P = 0.0027).

Conclusions: The evaluation of IgG specific to mosquito salivary gland extracts as immunological biomarkers in populations in Burkina Faso allowed us to show that the human anti-SGE IgG level to An. gambiae bites is strongly influenced by the living environment and the use of insecticides in agriculture.

Keywords: An. gambiae bites; Burkina Faso; IgG antibodies; Malaria; Salivary proteins.

Fig. 1

Map highlighting study areas with dots

Fig. 2

Flowchart of the study population

Fig. 3

Mean concentration of the IgG response to Anopheles gambiae salivary proteins by village. Participants were grouped by village (n = 10), and the mean IgG level against An. gambiae SGE was calculated using individual IgG levels in each village. In these villages, cotton farmers used only chemical compounds (synthetic pesticides) such as carbamates, organophosphates, pyrethroids, and others to control cotton pests

Fig. 4

Mean concentration of IgG responses to Anopheles gambiae salivary gland extracts by village. Participants were grouped by villages (n = 6), and the mean IgG against An. gambiae SGE was calculated on the basis of individual IgGs to An. gambiae SGE in each village. In these villages, farmers cultivated cotton without using chemical compounds, relying solely on pesticides derived from natural substances (plant extract mixtures, bacteria, and others) to control pests