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

Parasites & Vectors volume 18, Article number: 179 (2025) Cite this article

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.

Graphical Abstract

Background

Mosquitoes are involved in numerous human diseases, such as malaria, that kill or debilitate millions of people each year [1]. Despite the progress achieved in controlling malaria, it remains a major public health problem, contributing to morbidity and mortality, especially in children under 5 years of age in sub-Saharan Africa (80%). According to the latest World Malaria Report, there were 249 million cases of malaria in 2022 against 244 million in 2021 [2]. The estimated number of deaths attributable to malaria was 608,000 in 2022 against 610,000 in 2021. About 94% of malaria cases (233 million) and 95% of deaths (580,000) from the disease were recorded in the World Health Organization (WHO) African Region [2]. In 2022, Burkina Faso recorded 11,656,675 cases of malaria, including 539,488 cases of the severe form. Unfortunately, 4243 deaths were recorded, of which 2925 were children under 5 years of age [3].

Globally, nearly 2.2 billion people are at risk of malaria [4]. In the context of prevention, several strategies have been implemented, including vector control and vaccines. Vector control is an essential component of malaria control and elimination strategies, as it is highly effective in preventing infection and reducing transmission.

The two primary interventions are long-lasting insecticide-treated nets (LLINs) and indoor residual spraying (IRS), which reduce contact with infected mosquitoes [5, 6]. There are approximately 422 species of Anopheles worldwide, but only about 68 act as vectors of Plasmodium spp. In sub-Saharan Africa, malaria vectors are classified into three main categories, consisting of about 12 species. An. gambiae and An. funestus are major vectors of malaria, with a wide geographical distribution, high vectorial capacity, and sporozoite indices greater than 1% [7,8,9,10].

Malaria is endemic to Burkina Faso, and populations are frequently exposed to bites from only one or a few Anopheles mosquito species, which are the predominant malaria vectors. During the rainy season, An. gambiae is the major malaria vector in Burkina Faso [11,12,13,14]. Significant differences were observed between urban areas and villages (parasite index: 16% versus indices ranging from 51% to 88%) [15].

Entomological surveillance for malaria is inherently resource-intensive and produces crude population-level measures of vector exposure. Currently, the gold standard measurement of malaria transmission intensity is the entomological inoculation rate (EIR), a population measure defined as the number of infective Anopheles mosquito bites a person receives per unit of time [16].

In some individuals, the bite of a blood-sucking arthropod is often followed by a hypersensitivity reaction at the bite site. This is due to the production of IgG and IgE specific to immunogenic salivary proteins [17,18,19,20]. Over the past decade, several studies showed that quantifying the antibody (Ab) response to vector saliva in human populations could serve as a pertinent biomarker tool to assess human exposure to vector bites and, consequently, the risk of transmission of vector-borne diseases [21]. In addition, new immuno-epidemiological tools have been developed to assess exposure to mosquito bites at both the population and individual levels [22, 23]. These innovative tools are based on measuring human antibody responses to the salivary proteins of arthropod vectors injected during the bite [23,24,25,26,27,28,29,30,31,32].

Studies are being conducted at multiple sites to generate standardized surveillance data that improve understanding of malaria transmission [30, 33, 34] and to monitor and evaluate the impact of interventions to inform malaria control and elimination programs [35]. The IgG response to An. gambiae salivary gland extracts (SGE) has been identified and validated as a relevant biomarker of mosquito bites [23, 24, 36]. It is a reliable tool for assessing the spatial and temporal heterogeneity of exposure at both the population and individual levels [10, 37].

Despite the importance of antibodies against An. gambiae salivary peptides as a relevant biomarker of mosquito bites [23, 24, 34, 37,38,39,40], data on immuno-epidemiological biomarkers of human exposure to An. gambiae bites remain relatively scarce in Burkina Faso. These data are needed to better understand and reduce malaria transmission.

For this reason, the present study aims to evaluate and compare the IgG specific response to SGE of An. gambiae in populations living in urban areas (children) and rural areas (adults). The IgG specific response to SGE was also assessed across children based on age groups, and in cotton farmers following their agricultural practices (i.e., the use of synthetic pesticides or not).

Methods

Study area

The study was conducted at two sites: (i) 16 villages located in the province of Ziro (11°33′16″N, 1°46′25″W), 100 km from Ouagadougou; and (ii) Ouagadougou, the capital city of Burkina Faso (Fig. 1). A cross-sectional descriptive study was carried out from September 2020 to March 2021 for the collection of samples from children, and from June to July 2022 for the collection of samples from adult cotton farmers. Conventional cotton farmers used only chemical compounds (synthetic pesticides) such as carbamates, organophosphates, and pyrethroids, while organic cotton farmers used pesticides derived from natural substances (plant extract mixtures, bacteria, and others) to control pests.

Fig. 1
figure 1

Map highlighting study areas with dots

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Study design and sample collection

The studies were conducted according to the principles of the Declaration of Helsinki [41] and in full conformity with relevant country regulations. Ethical assessments were obtained in Burkina Faso by: Comité d’Éthique pour la Recherche en Santé du Burkina Faso (No. 2020-10-217) and Institutional Ethics Committee for Health Research of the Research Institute for Health Sciences in Burkina Faso (No. 009–2022/CEIRES of 20 January 2022). The study was approved by the Burkina Faso Ministry of Health and Public Hygiene. Site leaders provided prior permission to survey each site.

Adult farmers of organic and conventional cotton were included in Sapouy, and children under 15 years of age attending primary and secondary school in Ouagadougou were included in the study. Participants were selected using a simple random sampling technique, ensuring equal probability for all eligible individuals. Permission was granted for consent, assent, and collection sheets. Validated consent was obtained from a parent or guardian of each participating child, as well as from the adult participants. In addition to parental consent, children aged 12 and over provided their free, informed, and written assent.

During the administration of consent, we provided information about the study, the amount of blood to be collected, the risks of participating in the study, the confidentiality of participants’ information, and the freedom to withdraw consent at any time without consequences.

Overall, blood samples were collected from 200 children aged 3–14 years in urban areas and 477 cotton farmers aged 17–76 years in rural areas. One cotton farmer withdrew from the study. Therefore, 200 children and 476 cotton farmers were included in the analysis (Fig. 2).

Fig. 2
figure 2

Flowchart of the study population

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Blood samples (5 mL) were collected in tubes containing ethylenediaminetetraacetic acid (EDTA) as an anticoagulant for immunological assays. Thick and thin blood films were prepared for microscopic examination, and plasma samples (aliquots of 150 µL) were stored at −20 °C until analysis.

Parasitological diagnosis

Thick and thin blood films were air-dried, fixed with methanol, stained with 3% Giemsa, and examined double-blind by two certified microscopists. Discordant readings were re-examined by a third qualified independent microscopist. One hundred high-power fields (HPFs) were examined, and the number of malaria parasites of each species and stage was recorded. The number of parasites per microliter of blood was calculated by assuming 20 white blood cells per high-power field and a fixed white blood cell count of 8000/µL. A blood smear was considered negative if no parasites were observed.

Salivary gland dissection

The protein extracts were produced from reared An. gambiae specimens. Female mosquitoes were anesthetized on ice for 10 minutes before being dissected to remove the salivary glands. Salivary glands were dissected in phosphate-buffered saline [10 mM NaH₂PO₄, 145 mM NaCl (pH 7.2)] and carefully transferred to a microcentrifuge tube in a small volume of phosphate-buffered saline (50 µL). The samples were kept at −80 °C until use.

Extraction by sonication

Sonication is the process of converting an electrical signal into a physical vibration for various purposes. It is usually performed to disrupt cell membranes and release cell contents for later evaluation. The salivary glands of An. gambiae were placed in a sonicator for 10 min at a maximum of 60 Hz. The crude extracts were centrifuged at 15,000 rpm for 15 min. After centrifugation, the proteins were placed into Eppendorf tubes for quantification.

Protein quantification

Salivary gland proteins were quantified using a NanoDrop spectrophotometer (ND-1000; No. 414). A 1 µL sample of salivary proteins was deposited at the center of the spectrophotometer, and the measurement was performed at 280 nm. The spectrophotometer was connected to a monitor that displayed the amount of salivary protein per microliter (µL).

Assessment of antibody responses

The enzyme-linked immunosorbent assay (ELISA) was performed following a standardized methodology described in the AIA standard operating procedures, as detailed elsewhere [37]. Venous blood samples were collected in tubes, and plasma was obtained after centrifugation at 3000 rpm for 10 min. Plasma samples were fractionated into aliquots and then frozen at −20 °C until use.

In brief, 96-well Maxisorp micro-assay plates were coated with An. gambiae salivary gland extracts (SGE) at 0.1 µg/mL and incubated at 4 °C overnight. The plates were blocked with skimmed milk buffer (3% milk powder in phosphate-buffered saline containing 0.1% Tween 20, abbreviated as 0.1% PBST) for 1 h at room temperature and covered with adhesive paper (Parafilm). This blocking solution was chosen owing to its lower background value. It lines the bottom of the plate, reducing background noise.

After this step, human plasma samples diluted 1/200 (vol:vol), positive and negative controls, and diluted standards of known concentrations were added in duplicate and incubated at room temperature with stirring for 2 h. Then, a specific anti-human IgG (secondary antibody) conjugated to peroxidase (1/100) was added to each well. The plates were incubated with stirring for another hour. The wells were washed three times with PBS between each step.

Bound secondary antibodies for IgG were quantified by adding 100 µL/well of ready-to-use TMB (3,3',5,5'-tetramethylbenzidine) substrate and incubating for 30 min in the dark at room temperature. Following incubation with stop solution (hydrochloric acid), optical density (OD) was read at 450 nm.

Individual results were expressed as the ΔOD value:

ΔOD = ODx − ODn,

where ODx represents the mean individual optical density (OD) value in both wells with An. gambiae SGE, and ODn represents the individual OD value for each serum without An. gambiae SGE. The ΔOD value of the test sample was converted into arbitrary units using the ADAMSEL program (Microsoft Excel worksheets).

Statistical analysis

All statistical analyses were performed using STATA™ version 17.0 (Stata Corporation). Parametric tests (Student’s t-tests and analysis of variance [ANOVA]) were used for independent groups with normally distributed antibody levels. The nonparametric Mann–Whitney U (Wilcoxon rank-sum) test was used to compare IgG levels between two independent groups with non-normally distributed antibody levels. All differences were considered significant at P < 0.05.

Results

Approximately two-thirds (63.0%, 426/676) of the study population were male. The mean age of participants was 31.2 ± 17.8 years. The most represented age group was ≥ 25 years (62.1%, 420/676). More than two-thirds (70.4%, 476/676) of the study population lived in rural areas (Table 1).

Table 1 Baseline characteristics of the study participants
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Human IgG response to Anopheles gambiae salivary proteins

Human anti-SGE IgG were detected in all samples tested, indicating that all participants were exposed to An. gambiae mosquito bites, albeit at different levels of exposure.

Urban participants demonstrated greater exposure to An. gambiae bites than rural participants (P < 0.0001). Significant differences in mean IgG levels were observed between the two groups of children (primary and secondary school) (P < 0.0001). Organic cotton farmers expressed higher IgG levels compared with conventional cotton farmers (P = 0.0027). The mean antibody level to antigenic proteins of An. gambiae salivary glands was significantly associated with age (P = 0.0001). Gender had no significant influence on the mean IgG level against An. gambiae salivary gland extracts (P = 0.2175) (Table 2).

Table 2 Mean level of human IgG response to Anopheles gambiae salivary gland extracts
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Prevalence of Plasmodium falciparum among children according to Anopheles gambiae exposure

Overall, Plasmodium falciparum prevalence detected by microscopy was 4.5% (9/200) in children (Table 3). The mean concentration of the IgG response to An. gambiae SGE was higher in P. falciparum-positive children (0.6) compared with P. falciparum-negative children (0.5). However, the difference was not statistically significant (P = 0.7345).

Table 3 Plasmodium falciparum prevalence according to Anopheles gambiae exposure in children
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No significant difference in the prevalence or density of P. falciparum was observed between children in primary and secondary school (P = 0.342 and P = 0.4040, respectively) (Table 3).

IgG responses to Anopheles gambiae salivary gland extracts in conventional cotton farmer villages

Among the ten villages where conventional cotton was cultivated, Bouem had the highest mean IgG level, while Niliri had the lowest mean IgG level to An. gambiae SGE among conventional cotton farmers (Fig. 3).

Fig. 3
figure 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

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Human IgG responses to Anopheles gambiae salivary proteins among organic cotton farmer villages

Among organic cotton farmers, the mean IgG level to An. gambiae SGE was highest in Latian village and lowest in Sia village (Fig. 4).

Fig. 4
figure 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

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Discussion

The serological evaluation of the antibody response to mosquito saliva and its association with exposure to malaria vectors has received increasing attention owing to the limitations of current techniques in estimating malaria transmission [42]. An. gambiae-specific salivary polypeptides have been shown to be reliable markers of human exposure to Afrotropical malaria vectors, as demonstrated by studies in Burkina Faso, Tanzania, and Uganda [43,44,45].

In this study, we used an innovative serological marker tool to quantify human–vector contact and estimate the risk of malaria transmission in endemic areas on the basis of living environment (urban or rural), age (primary or secondary school), and type of agriculture practiced (conventional or organic cotton).

Human anti-SGE IgG was detected in all samples tested, indicating that all participants were exposed to An. gambiae mosquito bites, albeit at different levels. Urban participants were more exposed to An. gambiae bites than rural participants (P < 0.0001), as evidenced by higher average anti-SGE IgG levels in urban areas in our study. In cities, household drinking water storage practices and the discharge of sewage into streets could create potential breeding sites for Anopheles. In Ouagadougou, a reservoir has been transformed for vegetable farming and other cultivation, increasing the heterogeneity of urban environments in terms of vegetation and standing water (small puddles and breeding sites), each of which can influence mosquito abundance, particularly An. gambiae, the major malaria vector in Africa and a key driver of disease transmission [46,47,48]. In addition, malaria control strategies may be more difficult to plan and coordinate in urban areas, where the unregulated occupation of space could promote the proliferation of breeding sites for malaria vectors [46, 49, 50]. Previous research suggests that lower-income neighborhoods generally have more standing water due to residential abandonment, garbage dumps, and inadequate sewage systems [48]. Many such poor neighborhoods exist in Ouagadougou, where we collected data, the capital of a low-income country. A limitation of this comparison is the absence of adults in our urban study population and the absence of children among participants in rural areas.

Significant differences in mean IgG levels were noted between the two groups of children (primary and secondary school) (P < 0.0001). This result reflects differences in the way immune responses develop in individuals who are continuously exposed to Anopheles bites. Anti-SGE IgG levels to An. gambiae increased with age in all children (P < 0.0001) and in P. falciparum-positive children (P = 0.0220), with a less intense response in primary school children. This pattern is similar to those observed with salivary antigen proteins of An. gambiae [27, 51] and various P. falciparum antigens in the same epidemiological setting [52]. In addition, secondary school children stay outside later in the evenings, increasing their exposure to Anopheles bites [53].

The mean antibody level to antigenic proteins of An. gambiae SGE was statistically associated with age (P = 0.0001). The average IgG level increased with age up to the 15–20 year age group before decreasing. This decline could be explained by the high number (n = 283) of conventional cotton farmers (ages > 15 years) in our study population. The pesticides used in conventional cotton farming may repel mosquitoes, reducing exposure to mosquito bites.

Our findings demonstrated that the antibody response to An. gambiae SGE varies according to age, agricultural practices, and area of residence. Organic cotton farmers exhibited higher IgG levels than conventional cotton farmers, a statistically significant difference (P = 0.0027). Agricultural practices likely modulate human–vector contact in our study area. Conventional cotton farmers used only chemical compounds (synthetic pesticides) such as carbamates (e.g., propoxur and bendiocarb), organophosphates (e.g., malathion and fenitrothion), organochlorines (e.g., DDT), pyrethroids (e.g., deltamethrin, permethrin, cypermethrin, and lambda-cyhalothrin), and others to control cotton pests. These same classes of pesticides are widely used in mosquito control programs, including the deployment of insecticide-treated mosquito nets (ITNs) and indoor residual spraying (IRS) of insecticides [54]. These practices likely contribute to lower vector exposure in conventional cotton farmers by repelling mosquitoes. In recent years, the use of insecticides to combat mosquito-borne diseases has increased [55].

We found that An. gambiae SGE antibody concentration was positively correlated with malaria infection status in children in Ouagadougou, but this correlation was not statistically significant. Dipomin F. Traoré et al. reported a similar finding in their study [56], whereas other studies showed a statistically significant correlation [30]. The lack of statistical significance in our study could be due to the small sample size or a high level of exposure to Anopheles bites.

Bouem village had the highest mean IgG level to An. gambiae SGE, while Niliri had the lowest in conventional cotton farmers. In organic cotton farmers, the highest mean IgG level to An. gambiae SGE was recorded in Latian village, while the lowest was in Sia village. The reason for the higher vector exposure in these villages is unknown, but it may be influenced by factors such as human behavior, agricultural practices, vector control measures, population movement, and/or immunogenicity characteristics.

Using individual salivary components, such as An. gambiae SGE, could simplify and standardize experimental systems, providing insights into the complex relationships between vectors, parasites, and vertebrate hosts.

There are a few weaknesses in our study.

  • Unavailability of data from children in rural areas and lack of data from adults in urban areas: these absences can be explained by the fact that the data were collected at different time periods and with different initial objectives: (1) comparison of human anti-SGE IgG according to education level (age) in children; and (2) according to the type of agriculture practiced in rural areas,

  • Unavailability of information of vector control parameters in the study population. Indeed, this data was not collected.

Conclusions

To advance progress toward malaria elimination, the World Health Organization has called for innovative tools and improved approaches to enhance vector surveillance, as well as the monitoring and evaluation of interventions [57].

Our study evaluated human–vector contact using a new tool vector immunity as a means of assessing the relationship between the parasite, vectors, and humans. The results showed a significant difference in the mean anti-SGE IgG level between rural and urban populations. Age and type of agriculture also had a significant impact on the mean level of anti-salivary gland extract IgG of Anopheles gambiae.

Availability of data and materials

Data will be made available on reasonable request.

Abbreviations

ELISA:

Enzyme-linked immunosorbent assay

IgG:

Immunoglobulin G

OD:

Optical density

CI:

Confidence interval

References

  1. Gubler DJ. The global emergence/resurgence of arboviral diseases as public health problems. Arch Med Res. 2002;33:330–42.

    Article  PubMed  Google Scholar 

  2. WHO. Malaria. 2023. https://www.who.int/fr/news-room/fact-sheets/detail/malaria. Accessed 11 Dec 2024.

  3. Ministry of Health and Public Hygiene, Burkina Faso. 2022. https://www.aa.com.tr/fr/afrique/burkina-faso-plus-de-4-mille-décès-dus-au-paludisme-en-2022/2956187.

  4. Horii T. Malaria vaccine. Nihon Rinsho Jpn J Clin Med. 2008;66:1990–8.

    Google Scholar 

  5. Hilton ER, Tougri G, Camara T, Pagabelem A, Ouedraogo JB, Millar J, et al. An observational analysis of the impact of indoor residual spraying in two distinct contexts of Burkina Faso. Malar J. 2024;23:229. https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12936-024-05054-2.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Lepère JF, Collet L, Idaroussi AB, Youssouf H, Soler M, Pradines B. A malaria elimination milestone reached on Mayotte Island. Infect Dis Now. 2024;54:104868.

    Article  PubMed  Google Scholar 

  7. Hamon J. Secondary vectors of human malaria in Africa. Mouchet J Med Trop Rev Corps Sante Colon. 1961;21:643–60.

    Google Scholar 

  8. Jean M, Pierre C, Marc C. Biodiversité du paludisme dans le monde. Montrouge: John Libbey Eurotext; 2004. p. 460.

    Google Scholar 

  9. Adja AM, N’Goran KE, Kengne P, Koudou GB, Toure M, Koffi AA, et al. Vectorial transmission of malaria in shrubby Savannah area at Ganse, Ivory Coast. Med Trop Rev Corps Sante Colon. 2006;66:449–55.

    CAS  Google Scholar 

  10. Kearney EA, Agius PA, Chaumeau V, Cutts JC, Simpson JA, Fowkes FJ. Anopheles salivary antigens as serological biomarkers of vector exposure and malaria transmission: a systematic review with multilevel modelling. Elife. 2021;10:e73080.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Baldet T, Diabaté A, Guiguemdé TR. Malaria transmission in 1999 in the rice field area of the Kou Valley (Bama), (Burkina Faso). Sante Montrouge Fr. 2003;13:55–60.

    Google Scholar 

  12. Hughes A, Lissenden N, Viana M, Toé KH, Ranson H. Anopheles gambiae populations from Burkina Faso show minimal delayed mortality after exposure to insecticide-treated nets. Parasit Vectors. 2020;13:17.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Carnevale P, Fouque F, Gay F, Manguin S. Lessons from the malaria vector control program based on indoors residual spraying with DDT or dieldrin in the pilot zone of bobo-dioulasso: failure or success? Med Trop Sante Int. 2021. https://doiorg.publicaciones.saludcastillayleon.es/10.48327/mtsibulletin.v9i9.66.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Epopa PS, Collins CM, North A, Millogo AA, Benedict MQ, Tripet F, et al. Seasonal malaria vector and transmission dynamics in western Burkina Faso. Malar J. 2019;18:113. https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12936-019-2747-5.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Sabatinelli G, Bosman A, Lamizana L, Rossi P. Prevalence of malaria in Ouagadougou and the surrounding rural environment during the period of maximal transmission. Parassitologia. 1986;28:17–31.

    CAS  PubMed  Google Scholar 

  16. Monroe A, Moore S, Okumu F, Kiware S, Lobo NF, Koenker H, et al. Methods and indicators for measuring patterns of human exposure to malaria vectors. Malar J. 2020;19:207.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Reunala T, Brummer-Korvenkontio H, Palosuo K, Miyanij M, Ruiz-Maldonado R, Löve A, et al. Frequent occurrence of IgE and IgG4 antibodies against saliva of Aedes communis and Aedes aegypti mosquitoes in children. Int Arch Allergy Immunol. 1994;104:366–71.

    Article  CAS  PubMed  Google Scholar 

  18. Peng Z, Yang M, Simons FE. Immunologic mechanisms in mosquito allergy: correlation of skin reactions with specific IgE and IgG antibodies and lymphocyte proliferation response to mosquito antigens. Ann Allergy Asthma Immunol Off Publ Am Coll Allergy Asthma Immunol. 1996;77:238–44.

    Article  CAS  Google Scholar 

  19. Peng Z, Li H, Simons FER. Immunoblot analysis of IgE and IgG binding antigens in extracts of mosquitoes Aedes vexans, Culex tarsalis and Culiseta inornata. Int Arch Allergy Immunol. 1996;110:46–51.

    Article  CAS  PubMed  Google Scholar 

  20. Brummer-Korvenkontio H, Palosuo T, François G, Reunala T. Characterization of Aedes communis, Aedes aegypti and Anopheles stephensi mosquito saliva antigens by immunoblotting. Int Arch Allergy Immunol. 1997;112:169–74.

    Article  CAS  PubMed  Google Scholar 

  21. Sagna A, Poinsignon A, Remoue F. Chapter 12 - Epidemiological applications of assessing mosquito exposure in a malaria-endemic area. In: Wikel SK, Aksoy S, Dimopoulos G, editors. Arthropod vector: controller of disease transmission, volume 2. Cambridge: Academic Press; 2017. p. 209–29.

    Chapter  Google Scholar 

  22. Billingsley PF, Baird J, Mitchell JA, Drakeley C. Immune interactions between mosquitoes and their hosts. Parasite Immunol. 2006;28:143–53.

    Article  CAS  PubMed  Google Scholar 

  23. Waitayakul A, Somsri S, Sattabongkot J, Looareesuwan S, Cui L, Udomsangpetch R. Natural human humoral response to salivary gland proteins of Anopheles mosquitoes in Thailand. Acta Trop. 2006;98:66–73.

    Article  CAS  PubMed  Google Scholar 

  24. Remoue F, Cisse B, Ba F, Sokhna C, Herve JP, Boulanger D, et al. Evaluation of the antibody response to Anopheles salivary antigens as a potential marker of risk of malaria. Trans R Soc Trop Med Hyg. 2006;100:363–70.

    Article  PubMed  Google Scholar 

  25. Cornelie S, Remoue F, Doucoure S, Ndiaye T, Sauvage FX, Boulanger D, et al. An insight into immunogenic salivary proteins of Anopheles gambiae in African children. Malar J. 2007;6:75.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Poinsignon A, Cornelie S, Mestres-Simon M, Lanfrancotti A, Rossignol M, Boulanger D, et al. Novel peptide marker corresponding to salivary protein gSG6 potentially identifies exposure to Anopheles bites. PLoS ONE. 2008;3:e2472.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Drame PM, Poinsignon A, Besnard P, Cornelie S, Mire JL, Toto JC, et al. Human antibody responses to the Anopheles salivary gSG6-P1 peptide: a novel tool for evaluating the efficacy of ITNs in malaria vector control. PLoS ONE. 2010;5:e15596. https://doiorg.publicaciones.saludcastillayleon.es/10.1371/journal.pone.0015596.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Poinsignon A, Samb B, Doucoure S, Drame PM, Sarr JB, Sow C, et al. First attempt to validate the gSG6-P1 salivary peptide as an immuno-epidemiological tool for evaluating human exposure to Anopheles funestus bites. Trop Med Int Health TM IH. 2010;15:1198–203.

    Article  CAS  PubMed  Google Scholar 

  29. Rizzo C, Ronca R, Fiorentino G, Verra F, Mangano V, Poinsignon A, et al. Humoral response to the Anopheles gambiae salivary protein gSG6: a serological indicator of exposure to Afrotropical malaria vectors. PLoS ONE. 2011;6:e17980.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Londono-Renteria B, Drame PM, Weitzel T, Rosas R, Gripping C, Cardenas JC, et al. An. gambiae gSG6-P1 evaluation as a proxy for human-vector contact in the Americas: a pilot study. Parasit Vectors. 2015;8:533.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Helb DA, Tetteh KKA, Felgner PL, Skinner J, Hubbard A, Arinaitwe E, et al. Novel serologic biomarkers provide accurate estimates of recent Plasmodium falciparum exposure for individuals and communities. Proc Natl Acad Sci U S A. 2015;112:E4438-4447.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Sagna AB, Kassié D, Couvray A, Adja AM, Hermann E, Riveau G, et al. Spatial assessment of contact between humans and Anopheles and Aedes mosquitoes in a medium-sized African urban setting, using salivary antibody-based biomarkers. J Infect Dis. 2019;220:1199–208.

    Article  CAS  PubMed  Google Scholar 

  33. Noukpo MH, Damien GB, Elanga-N’Dille E, Sagna AB, Drame PM, Chaffa E, et al. Operational assessment of long-lasting insecticidal nets by using an anopheles salivary biomarker of human-vector contact. Am J Trop Med Hyg. 2016;95:1376–82.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Ya-Umphan P, Cerqueira D, Parker DM, Cottrell G, Poinsignon A, Remoue F, et al. Use of an Anopheles salivary biomarker to assess malaria transmission risk along the Thailand–Myanmar border. J Infect Dis. 2017;215:396–404.

    CAS  PubMed  Google Scholar 

  35. Moss WJ, Dorsey G, Mueller I, Laufer MK, Krogstad DJ, Vinetz JM, et al. Malaria epidemiology and control within the international centers of excellence for malaria research. Am J Trop Med Hyg. 2015. https://doiorg.publicaciones.saludcastillayleon.es/10.4269/ajtmh.15-0006.

    Article  PubMed  PubMed Central  Google Scholar 

  36. Barral A, Honda E, Caldas A, Costa J, Vinhas V, Rowton ED, et al. Human immune response to sand fly salivary gland antigens: a useful epidemiological marker? Am J Trop Med Hyg. 2000;62:740–5.

    Article  CAS  PubMed  Google Scholar 

  37. Londono-Renteria B, Cardenas JC, Cardenas LD, Christofferson RC, Chisenhall DM, Wesson DM, et al. Use of anti-Aedes aegypti salivary extract antibody concentration to correlate risk of vector exposure and dengue transmission risk in Colombia. PLoS ONE. 2013;8:e81211.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Sagna A, Faye E, Konaté S, Rey JY, Diarra K, Diouf D, et al. Host suitability of cultivated plants to Bactrocera dorsalis and Ceratitis cosyra (Diptera Tephritidae) in mango orchards in Senegal. In: Programme and Book of Abstracts of the 8th Annual Conference of the IOBC-Africa, Yaoundé, Cameroon. Montpellier: CIRAD; 2013.https://agritrop.cirad.fr/593198/.

  39. Sagna AB, Gaayeb L, Sarr JB, Senghor S, Poinsignon A, Boutouaba-Combe S, et al. Plasmodium falciparum infection during dry season: IgG responses to Anopheles gambiae salivary gSG6-P1 peptide as sensitive biomarker for malaria risk in Northern Senegal. Malar J. 2013;12:301. https://agritrop.cirad.fr/593198/

    Article  PubMed  PubMed Central  Google Scholar 

  40. Orlandi-Pradines E, Almeras L, Denis de Senneville L, Barbe S, Remoué F, Villard C, et al. Antibody response against saliva antigens of Anopheles gambiae and Aedes aegypti in travellers in tropical Africa. Microbes Infect. 2007;9:1454–62.

    Article  CAS  PubMed  Google Scholar 

  41. World Medical Association. World Medical Association Declaration of Helsinki: ethical principles for medical research involving human subjects. JAMA. 2013;310:2191–4.

    Article  Google Scholar 

  42. Drakeley CJ, Corran PH, Coleman PG, Tongren JE, McDonald SLR, Carneiro I, et al. Estimating medium- and long-term trends in malaria transmission by using serological markers of malaria exposure. Proc Natl Acad Sci U S A. 2005;102:5108–13.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Stone W, Bousema T, Jones S, Gesase S, Hashim R, Gosling R, et al. IgG responses to Anopheles gambiae salivary antigen gSG6 detect variation in exposure to malaria vectors and disease risk. PLoS ONE. 2012;7:e40170.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Proietti C, Verra F, Bretscher MT, Stone W, Kanoi BN, Balikagala B, et al. Influence of infection on malaria-specific antibody dynamics in a cohort exposed to intense malaria transmission in northern Uganda. Parasite Immunol. 2013;35:164–73.

    Article  CAS  PubMed  Google Scholar 

  45. Rizzo C, Ronca R, Lombardo F, Mangano V, Sirima SB, Nèbiè I, et al. IgG1 and IgG4 antibody responses to the Anopheles gambiae salivary protein gSG6 in the sympatric ethnic groups Mossi and Fulani in a malaria hyperhendemic area of Burkina Faso. PLoS ONE. 2014;9:e96130.

    Article  PubMed  PubMed Central  Google Scholar 

  46. Pages F, Orlandi-Pradines E, Corbel V. Vectors of malaria: biology, diversity, prevention, and individual protection. Med Mal Infect. 2007;37:153–61.

    Article  CAS  PubMed  Google Scholar 

  47. Dossou-Yovo J, Doannio JM, Diarrassouba S, Chauvancy G. The impact of rice fields on malaria transmission in the city of Bouaké, Côte d’Ivoire. Bull Soc Pathol Exot 1990. 1998;91:327–33.

    CAS  Google Scholar 

  48. Yitbarek S, Chen K, Celestin M, McCary M. Urban mosquito distributions are modulated by socioeconomic status and environmental traits in the USA. Ecol Appl. 2023;33:e2869.

    Article  PubMed  Google Scholar 

  49. Byrne N. Urban malaria risk in sub-Saharan Africa: where is the evidence? Travel Med Infect Dis. 2007;5:135–7.

    Article  PubMed  Google Scholar 

  50. Martens P, Hall L. Malaria on the move: human population movement and malaria transmission. Emerg Infect Dis. 2000;6:103.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Rizzo C, Lombardo F, Ronca R, Mangano V, Sirima SB, Nèbiè I, et al. Differential antibody response to the Anopheles gambiae gSG6 and cE5 salivary proteins in individuals naturally exposed to bites of malaria vectors. Parasit Vectors. 2014;7:549.

    Article  PubMed  PubMed Central  Google Scholar 

  52. Modiano D, Chiucchiuini A, Petrarca V, Sirima BS, Luoni G, Perlmann H, et al. Humoral response to Plasmodium falciparum Pf155/ring-infected erythrocyte surface antigen and Pf332 in three sympatric ethnic groups of Burkina Faso. Am J Trop Med Hyg. 1998;58:220–4.

    Article  CAS  PubMed  Google Scholar 

  53. Robert V, Macintyre K, Keating J, Trape JF, Duchemin JB, Warren M, et al. Malaria transmission in urban sub-Saharan Africa. Am J Trop Med Hyg. 2003;68:169–76.

    Article  PubMed  Google Scholar 

  54. WHO. Global report on insecticide resistance in malaria vectors: 2010–2016. Geneva: World Health Organ; 2018.

    Google Scholar 

  55. Sengul Demirak M, Canpolat E. Plant-based bioinsecticides for mosquito control: impact on insecticide resistance and disease transmission. Insects. 2022;13:8–24.

    Article  Google Scholar 

  56. Traoré DF, Sagna AB, Adja AM, Zoh DD, Lingué KN, Coulibaly I, et al. Evaluation of malaria urban risk using an immuno-epidemiological biomarker of human exposure to Anopheles bites. Am J Trop Med Hyg. 2018;98:1353–9.

    Article  PubMed  PubMed Central  Google Scholar 

  57. WHO. Global vector control response 2017–2030. Geneva: World Health Organization; 2017.

    Google Scholar 

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Acknowledgements

We thank all the participants for their kind support and collaboration, the Centre National de Recherche et de Formation sur le Paludisme (CNRFP) and the Laboratoire de Biochimie et Immunologie Appliquées (LaBIA) for providing the use of their technical equipment.

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Authors and Affiliations

  1. Laboratoire de Biochimie et Immunologie Appliquées (LaBIA), École Doctorale Sciences et Technologies, Université Joseph KI-ZERBO, 03 BP 7021 03, Ouagadougou, Burkina Faso

    Michaël Kaboré, Yéri Esther Hien, Abdoul Rahamani Nikiema & Enock Ibrango

  2. Centre National de Recherche et de Formation sur le Paludisme (CNRFP), Ouagadougou, Burkina Faso

    Mireille Ouédraogo, Nicolas Ouédraogo & Guillaume Sylvestre Sanou

  3. Institut de Recherche en Sciences de la Santé (IRSS), Ouagadougou, Burkina Faso

    Sylvain Ilboudo

  4. Université Nazi BONI, Bobo-Dioulasso, Burkina Faso

    Fatimata Thiombiano & Mariama K. Cherif

  5. Unité de Recherche Clinique de Nanoro (URCN), Nanoro, Burkina Faso

    Toussaint Rouamba

  6. Laboratoire de Développement du Médicament, Centre d’Excellence Africain de Formation, de Recherche et d’Expertises en Sciences du Médicament, Université Joseph KI-ZERBO (LADME/CEA-CFOREM/UJKZ), Ouagadougou, Burkina Faso

    Dado Jean Noël Koussé

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  1. Michaël Kaboré
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Contributions

M.K., F.T., J.K., Y.E.H., and S.G.S. participated in the conception, the design of the work, and data acquisition/analysis/interpretation. M.K., N.A.R., M.O., E.I., and N.O. contributed to sample acquisition and analysis. Y.E.H., M.K.C., S.I., T.R., and S.G.S. contributed to the final validation of the manuscript. All authors contributed to writing versions of the manuscript. All authors read and approved the final manuscript. All authors approved the submitted version of the manuscript.

Corresponding author

Correspondence to Michaël Kaboré.

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Consent was obtained from a parent or guardian of each participating child and from the adult participants. In addition to parental consent, children aged 12 years and over gave their free, informed, and written consent.

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The authors declare no competing interests.

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Kaboré, M., Hien, Y.E., Koussé, D.J.N. et al. Human IgG responses to Anopheles gambiae immunogenic salivary proteins in urban and rural populations of Burkina Faso: biomarkers of exposure to malaria vector bites. Parasites Vectors 18, 179 (2025). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s13071-025-06792-1

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Keywords

Parasites & Vectors

ISSN: 1756-3305

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