Skip to main content

Distribution of Anopheles gambiae thioester-containing protein 1 alleles along malaria transmission gradients in The Gambia



Thioester-containing protein 1 (TEP1) is a highly polymorphic gene playing an important role in mosquito immunity to parasite development and associated with Anopheles gambiae vectorial competence. Allelic variations in TEP1 could render mosquito either susceptible or resistant to parasite infection. Despite reports of TEP1 genetic variations in An. gambiae, the correlation between TEP1 allelic variants and transmission patterns in malaria endemic settings remains unclear.


TEP1 allelic variants were characterized by PCR from archived genomic DNA of > 1000 An. gambiae mosquitoes collected at 3 time points between 2009 and 2019 from eastern Gambia, where malaria transmission remains moderately high, and western regions with low transmission.


Eight common TEP1 allelic variants were identified at varying frequencies in An. gambiae from both transmission settings. These comprised the wild type TEP1, homozygous susceptible genotype, TEP1s; homozygous resistance genotypes: TEP1rA and TEP1rB, and the heterozygous resistance genotypes: TEP1srA, TEP1srB, TEP1rArB and TEP1srArB. There was no significant disproportionate distribution of the TEP1 alleles by transmission setting and the temporal distribution of alleles was also consistent across the transmission settings. TEP1s was the most common in all vector species in both settings (allele frequencies: East = 21.4–68.4%. West = 23.5–67.2%). In Anopheles arabiensis, the frequency of wild type TEP1 and susceptible TEP1s was significantly higher in low transmission setting than in high transmission setting (TEP1: Z = − 4.831, P < 0.0001; TEP1s: Z = − 2.073, P = 0.038).


The distribution of TEP1 allele variants does not distinctly correlate with malaria endemicity pattern in The Gambia. Further studies are needed to understand the link between genetic variations in vector population and transmission pattern in the study settings. Future studies on the implication for targeting TEP1 gene for vector control strategy such as gene drive systems in this settings is also recommended.


Anopheles gambiae is the most efficient vector of Plasmodium falciparum, responsible for most of the malaria transmission in sub-Saharan Africa [1]. The vectorial competence of a mosquito species is dependent on its immune response to the invading parasites [2, 3], and diversity in An. gambiae immune-related genes modulates the variation in vector’s susceptibility to parasite transmission [4, 5]. Hence, genetic diversity of vectors could be explored in understanding its contribution to transmission dynamics of malaria across varying endemicity settings and as they adapt to interventions.

Mosquito immune response to parasite occurs in two phases: an initial response to ookinetes while crossing the midgut epithelium; and a later phase, elicited against oocysts and sporozoites in the midgut and salivary gland, respectively [6,7,8,9]. In An. gambiae, the initial immune response is mediated by complement-like proteins in the haemolymph, where invading Plasmodium is opsonized and killed [6, 8, 10]. Here, the main protein of the complement-like innate immune response is the thioester-containing protein 1 (TEP1) [10], similar to the human complement factor C3 [8, 10]. TEP1 opsonizes Plasmodium ookinete surface through thioester bonds and enhances lysis and melanization; inhibiting parasite development in the mosquito midgut [6, 11]. It is recognized as an important factor in genotype determining An. gambiae vectorial competence [6, 11].

TEP1 gene, located on chromosome 3L, is highly polymorphic with multiple allelic variants [8, 11]. Earlier studies found variants of TEP1 determine mosquito resistance or susceptibility to parasite. The TEP1s allelic variant is associated with higher susceptibility to malaria parasite infection, while TEP1r is linked to reduced susceptibility [7, 11, 12]. Recombinant subtypes of TEP1s and TEP1r (hybrids) which amplify the vector’s resistance to Plasmodium infection have also been described [8, 11].

Allelic variants of TEP1 have been previously investigated in An. gambiae sensu stricto (s.s.) and Anopheles coluzzii from Mali, Burkina Faso, Ghana, Cameroon and Tanzania; where they were associated with malaria phenotypes [12]. TEP1 variants seem to be geographically restricted and some variants are more common in a particular Anopheles species. TEP1s was most prevalent in An. gambiae s.s. and recorded from all countries studied. TEP1rA and TEP1rB which were subclusters of TEP1r were also identified and differentially distributed in both vector species.. TEP1rB was most common in An. coluzzii from Ghana, Mali and Burkina Faso and rarely found in the eastern African setting. TEP1rA co-occurred mainly with An. gambiae s.s. and An. coluzzii at relatively low frequency. Recombinant TEP1s/rB sub-type was also identified in both vectors from the three west African countries.

The distribution of TEP1 variants is currently unknown in Gambian vector populations, where malaria transmission has significantly declined but incidence remains heterogeneous [13, 14]. During the rainy season, there are pockets of relatively high malaria transmission in the eastern region with peaks in October and November compared to the western coastal regions [13, 14]. Malaria prevalence was previously estimated to be about 19% in eastern Gambia and below 15% in the western Gambia [13, 15]. The main vectors maintaining transmission are: An. gambiae s.s, An. coluzzii, Anopheles arabiensis and Anopheles melas [16,17,18]. These vectors are widely distributed across the country, where An. arabiensis predominates in the east, and An. gambiae s.s. and An. coluzzii in the west of the country [16,17,18]. Anopheles melas is limited to the coastal ecosystem but extends inwards to the middle of the country during high ocean tides [18,19,20]. The variation in transmission intensity between the eastern and western regions in the country could also be explained by vector parity [13] and insecticide resistance [16, 21], which were reportedly higher in the eastern than the western region.

With the drive towards pre-elimination, analysis of genetic variations that could be driving local transmission may help to improve strategies for optimizing the effectiveness of interventions. Here, we determined the distribution of TEP1 alleles in the sibling members of An. gambiae collected at 3 time points between 2009 and 2019 from high and low transmission settings in The Gambia.


Mosquito specimens

Archived genomic DNA from three previous studies: 2009 [22], 2016 [21] and 2019 [16] were analysed. These studies collected An. gambiae specimens during malaria transmission season (July to October) using mouth aspiration, pyrethrum spray catches and larval sampling. Specimens were collected from twenty villages that are sentinel sites of Gambian National Malaria Control Programme (GNMCP) covering the six administrative regions in The Gambia. Anopheles gambiae specimens were randomly selected from all sites and from each study.

Mosquito species identification

Molecular speciation of each vector was performed by these previous studies following different previously described PCR protocols identifying An. gambiae s.s, An. coluzzi, An. arabiensi and An. melas [23, 24]. Briefly, the PCR assay involves initial amplification of ribosomal DNA specific to each of these mosquito species [23], followed by restriction enzyme digestion to discriminate An. coluzzii, An. gambiae s.s. and their hybrids (An. coluzzii-An. gambiae s.s.) [24].

TEP1 alleles genotyping

Two TEP1 allele-specific PCR assays were employed to genotype the variants previously described in An. gambiae populations [4, 12]. The first assay [4] amplifies a 428 bp fragment for the susceptible allele (TEP1s) and 349 bp fragment for the resistant allele (TEP1r). The genotypes of TEP1r were amplified using the second assay [12], which targets 510 bp fragment for TEP1rA and 155 bp fragment for TEP1rB. The wild type (TEP1) (646 bp) was also amplified from the second assay. PCR products were analysed using QIAxcel capillary electrophoresis to identify the different fragments. Only fragments that were positive from both PCR assays were finally analysed. A total of 1400 mosquitoes were genotyped (2009 = 335; 2016 = 525; 2019 = 540).

Data analyses

TEP1 allele frequencies were determined as the percentage of the respective alleles in the overall vector population from each transmission setting (#allele/#total mosquito × 100). The prevalence of each vector species per setting per year was similarly calculated in percentages. The statistical differences in the proportions between the vector species and across each year were determined using Z score test. The statistical difference in the proportion of TEP1 alleles was not compared between the transmission settings because 30% of the samples from 2009, mostly from the low setting could not be characterized. All data analyses were done using Stata/IC 16.0 (2019 StataCorp LP).


Distribution of An. gambiae population along the east and west transmission settings

A total of 1,031 (74%) of the 1400 mosquitoes were successfully amplified for both species identification and TEP1 genotyping. The DNA from these specimens could have degraded, following a decade storage. Most of the successfully amplified mosquitoes (724, 70%), were from high transmission setting (eastern Gambia) and 307 (30%) were from the low transmission setting (west). The composition of the vector species comprised An. arabiensis, An. coluzzii, An. gambiae s.s., An. melas and hybrids of An. coluzzii-gambiae s.s. All vector species were identified from both settings except An. melas, which was only recorded from high transmission setting. The predominant Anopheles species identified in the high and the low transmission settings were An. arabiensis (n = 669, 65%), followed by An. coluzzii (n = 164, 16%), An. gambiae s.s. (n = 129, 13%), An. coluzzii-gambiae s.s. hybrids (n = 53, 5%) and An. melas (n = 16, 1%). Anopheles melas was not included in further analyses because of the low number of specimens obtained.

The composition of the local vector species was consistent in both transmission settings, where An. arabiensis remained predominant throughout the period except 2019 when the densities were lower in the low transmission setting (Fig. 1). There was a significant difference in the composition of the vector species per year per transmission setting (East: Z = − 4.5–15.6, P < 0.0001. West: Z = − 6.4–10, P < 0.0001).

Fig. 1
figure 1

Composition of An. gambiae collected per year from high transmission eastern (left panel) and lower transmission western (right panel) regions of The Gambia

Distribution of TEP1 alleles in An. gambiae populations across The Gambia

Irrespective of the study year, eight variants of TEP1 alleles were identified at different frequencies along the transmission settings (Fig. 2). The susceptible allele, TEP1s was the most prevalent in all species identified from both transmission settings. In high transmission setting, TEP1s was lowest in An. gambiae s.s. with an allele frequencies of 21.4% compared to the other vector species in the high transmission setting (Table 1). Anopheles gambiae s.s. from this setting mainly harboured (48.2%) the resistance TEP1rA sub-type allele, while this allele was rare in other species. In the low transmission setting, TEP1s was the most frequent in all vector species (allele frequency: 23.5–67.2%) except An. coluzzii which harboured mainly (allele frequency: 47%) the TEP1rB sub-type. In An. arabiensis, the wild type allele, TEP1 and susceptible allele, TEP1s were significantly higher in the low transmission setting than the high setting (TEP1: Z = − 4.831, P < 0.0001. TEPs: Z = − 2.073, P = 0.038).

Fig. 2
figure 2

Distribution of TEP1 alleles in An. gambiae populations along the transmission gradients. TEP1 alleles from all study years were combined together in the plot. N is the total number of species Anopheles species positive for all alleles in the specific setting. The green dots inside the map indicates the study sites in the eastern Gambia, the high transmission setting while the red dots are those sites from the Western Gambia, the low transmission setting

Table 1 TEP1 allele frequencies in vector species along the transmission gradients

Heterozygous TEP1 genotypes, TEP1srB, TEP1rArB and TEP1srArB were highly prevalent in An. arabiensis and An. coluzzii but rare in An. gambiae s.s. from both settings (Fig. 2). Only TEP1srA was found in An. gambiae s.s. (genotype frequency: East = 5.4%, West = 2.7%).

Dynamics of TEP1 diversity in vector species along the transmission gradients

The pattern of allele diversity was temporally consistent in each vector species identified. The majority of the TEP1 alleles detected in 2009 were still present in 2016 and 2019 at both settings (Table 2 and Fig. 3). Most of the species harboured TEP1s which was consistently the most frequent allele over time at both settings; and the frequency steadily increased in An. coluzzii over the years especially in high transmission setting (allele frequencies: 2009 = 0%; 2016 = 18.2%; 2019 = 59%). TEP1rA was uncommon in all vector species prior to 2019 in both settings. TEP1rB was equally uncommon and was detected in An. arabiensis and An. coluzzii in the high transmission setting in 2019 (allele frequencies 1.9% and 9%, respectively).

Table 2 Dynamics of TEP1 diversity in vector species along the transmission gradients
Fig. 3
figure 3

Dynamics of TEP1 alleles in An. gambiae populations over time along the transmission gradients. TEP1 alleles from all study years were separated by year. The green dots inside the map indicates the study sites in the eastern Gambia, the high transmission setting while the red dots are those sites from the Western Gambia, the low transmission setting

Heterozygous TEP1 genotypes: TEP1srB, TEP1rArB and TEP1srArB were not detected in the vectors from both settings in 2009. TEP1rArB was identified mainly in An. arabiensis and An. coluzzii in 2019 in high transmission setting.


As malaria transmission is relatively higher in eastern than western Gambia [13, 14], determining if genetic variation in the local vector populations could be partly driving this difference could improve our understanding on local vector competence. This knowledge is highly important as The Gambia aims for pre-elimination phase. This study characterized TEP1 gene alleles in vector populations collected at 3 time points within a decade from different regions of The Gambia. Eight previously described variants were found at varying frequencies across the country. There was no distinct restriction of specific TEP1 alleles by vector species or transmission setting; as the distribution of TEP1 alleles was similar and consistent in the vectors from both transmission settings across the study periods. However, the alleles were recorded at heterogenous levels, with the susceptible allele (TEP1s) predominating in both settings across years.

Lack of clustering of TEP1 alleles to specific vector species or transmission setting could be explained by similar composition of vector species in both settings and selective pressure on this gene that is maintained overtime. More importantly, these findings may imply that TEP1 plays limited role in the heterogeneous prevalence of malaria in The Gambia. Previous studies [17, 22, 29] have attributed the variance in transmission to insecticide resistance, which is currently higher in vectors in high transmission setting. Additionally, other studies [16,17,18] suggested that the relatively higher abundance of highly efficient vectors in the high transmission setting could be a factor. Further studies are needed to understand the role of other possible factors including human and vector behaviour [30, 31], as well as environment factors [32, 33]. The implication of targeting TEP1 gene for vector control in this setting also requires further investigations.

The pattern of distribution of TEP1 recorded between high and low transmission setting is consistent with a recent study in western Kenya [25], which did not document any significant difference in TEP1 alleles in vector populations in study areas comprising high and low transmission settings. The study suggested that the expanded vector control interventions in the study areas could have impacted the genetic structure of the vector population as documented in other settings [26, 27]. Vector interventions were scaled up during the period studied here, with a shift from DDT to pirimiphos methyl for IRS; as well as high coverage of LLINs throughout the country [28]. This indicates that despite this selection pressure against the vectors, there was no significant temporal shifts in alleles on TEP1 locus, and the effect of insecticides on the overall genetic structure of the natural vector population is unclear.

The observed high frequency of the resistant allele (TEP1rA) along with low frequency of the susceptible allele (TEP1s) in the highly competent vector, An. gambiae s.s. in high transmission setting prompts future investigations to further understand the role of adaptive interaction between this vector and parasite populations in this setting. Earlier studies have shown that adaption of the circulating P. falciparum populations to TEP1-mediated killing in sympatric An. gambiae population may be a driving factor for endemicity of malaria in sub-Saharan Africa [34]. Already, TEP1rA and TEP1s were previously associated with low and high infection prevalence respectively in specific parasite-vector populations [4, 34], suggesting ongoing local host-parasite adaption, which can be investigated in future with concomitant generation of parasite prevalence and genetic data.

This study recorded similar patterns of TEP1rA and TEP1rB in An. gambiae s.s. and An. coluzzii, respectively, where TEP1rA was common in both vectors but TEP1rB was exclusively found in An. coluzzii, as previously documented from Mali, Burkina Faso, Ghana, Cameroon and Tanzania [12]. However, the frequencies of these resistance-associated alleles were generally low and similar in both transmission settings. Taken together TEP1 alleles are not specifically affected by dwindling parasite biomass or interventions against the vectors.

Allelic recombination was common in An. arabiensis and An. coluzzii as previously shown [4, 11, 12], and consistently higher overtime in the high transmission setting than the low transmission setting. High recombination events in An. gambiae TEP1 gene was suggested to promote higher infection prevalence relative to homozygote TEP1r allele [11]. The relatively higher TEP1 heterozygous genotypes observed in An. arabiensis and An. coluzzii in the higher transmission setting could possibly be a factor for better vector competence in both vectors. However, lack of enough studies linking genetic diversity to vector competence in this setting hampers the interpretation of this finding. Nevertheless, sporozoite rates were recently reported higher in these vectors than An. gambiae s.s. in this setting [16]. A future study investigating the transmission efficiency of the vector species with the identified TEP1 alleles would better explain these results.

The temporal distribution of TEP1 alleles was consistent across the transmission settings in all vector populations. However, the consistent increase in TEP1s in An. coluzzii in both settings also prompts further phenotypic interrogations designed to determine the effect of these alleles in vector competence and malaria prevalence.

This study was limited by the inability to determine sporozoite infection rates in the vector population due to lack of adequate samples. Also, low number of specimens from some years and regions hampered the power to statistically compare the distribution of variants and malaria rates across the country and by specific year. However, the observed vector composition and densities were consistent with the previous studies, where vectors are relatively more abundant in the high than low transmission setting [16, 17, 21].


This study presented baseline data on TEP1 allelic variants of An. gambiae in The Gambia. Eight variants were identified at consistently similar pattern in both transmission settings and overtime. The susceptible allele was common in most vector species and transmission setting. These findings open opportunities for further studies to understand genetic changes in vectors populations that could be driving the current transmission pattern in The Gambia and implication for consideration of TEP1 for malaria control strategy such as gene drive systems in this setting.

Availability of data and materials

All relevant data are within the paper. No supporting Information is available.



Thioester-containing Protein 1


Deoxyribonucleic acid


Indoor residual spraying


Long-lasting insecticidal net


Polymerase chain reaction


  1. WHO. World Malaria Report. Geneva: World Health Organization; 2022.

    Google Scholar 

  2. Clayton AM, Dong Y, Dimopoulos G. The Anopheles innate immune system in the defense against malaria infection. J Innate Immun. 2014;6:169–81.

    Article  CAS  PubMed  Google Scholar 

  3. Dimopoulos G, Seeley D, Wolf A, Kafatos FC. Malaria infection of the mosquito Anopheles gambiae activates immune-responsive genes during critical transition stages of the parasite life cycle. EMBO J. 1998;17:6115–23.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Eldering M, Morlais I, van Gemert GJ, van de Vegte-Bolmer M, Graumans W, Siebelink-Stoter R, et al. Variation in susceptibility of African Plasmodium falciparum malaria parasites to TEP1 mediated killing in Anopheles gambiae mosquitoes. Sci Rep. 2016;6:20440.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Kwon H, Arends BR, Smith RC. Late-phase immune responses limiting oocyst survival are independent of TEP1 function yet display strain specific differences in Anopheles gambiae. Parasit Vectors. 2017;10:369.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Blandin S, Shiao SH, Moita LF, Janse CJ, Waters AP, Kafatos FC, Levashina EA. Complement-like protein TEP1 is a determinant of vectorial capacity in the malaria vector Anopheles gambiae. Cell. 2004;116:661–70.

    Article  CAS  PubMed  Google Scholar 

  7. Blandin SA, Marois E, Levashina EA. Antimalarial responses in Anopheles gambiae: from a complement-like protein to a complement-like pathway. Cell Host Microbe. 2008;3:364–74.

    Article  CAS  PubMed  Google Scholar 

  8. Blandin SA, Wang-Sattler R, Lamacchia M, Gagneur J, Lycett G, Ning Y, et al. Dissecting the genetic basis of resistance to malaria parasites in Anopheles gambiae. Science. 2009;326:147–50.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Harris C, Lambrechts L, Rousset F, Abate L, Nsango SE, Fontenille D, Morlais I, Cohuet A. Polymorphisms in Anopheles gambiae immune genes associated with natural resistance to Plasmodium falciparum. PLoS Pathog. 2010;6: e1001112.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Levashina EA, Moita LF, Blandin S, Vriend G, Lagueux M, Kafatos FC. Conserved role of a complement-like protein in phagocytosis revealed by dsRNA knockout in cultured cells of the mosquito. Anopheles gambiae Cell. 2001;104:709–18.

    Article  CAS  PubMed  Google Scholar 

  11. Obbard DJ, Callister DM, Jiggins FM, Soares DC, Yan G, Little TJ. The evolution of TEP1, an exceptionally polymorphic immunity gene in Anopheles gambiae. BMC Evol Biol. 2008;8:274.

    Article  PubMed  PubMed Central  Google Scholar 

  12. White BJ, Lawniczak MK, Cheng C, Coulibaly MB, Wilson MD, Sagnon N, et al. Adaptive divergence between incipient species of Anopheles gambiae increases resistance to Plasmodium. Proc Natl Acad Sci USA. 2011;108:244–9.

    Article  CAS  PubMed  Google Scholar 

  13. Mwesigwa J, Achan J, Di Tanna GL, Affara M, Jawara M, Worwui A, et al. Residual malaria transmission dynamics varies across The Gambia despite high coverage of control interventions. PLoS ONE. 2017;12: e0187059.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Mwesigwa J, Okebe J, Affara M, Di Tanna GL, Nwakanma D, Janha O, et al. On-going malaria transmission in The Gambia despite high coverage of control interventions: a nationwide cross-sectional survey. Malar J. 2015;14:314.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Wu L, Mwesigwa J, Affara M, Bah M, Correa S, Hall T, et al. Sero-epidemiological evaluation of malaria transmission in The Gambia before and after mass drug administration. BMC Med. 2020;18:331.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Hamid-Adiamoh M, Nwakanma D, Assogba BS, Ndiath MO, D’Alessandro U, Afrane YA, et al. Influence of insecticide resistance on the biting and resting preferences of malaria vectors in the Gambia. PLoS ONE. 2021;16: e0241023.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Opondo KO, Weetman D, Jawara M, Diatta M, Fofana A, Crombe F, et al. Does insecticide resistance contribute to heterogeneities in malaria transmission in The Gambia? Malar J. 2016;15:166.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Caputo B, Nwakanma D, Jawara M, Adiamoh M, Dia I, Konate L, et al. Anopheles gambiae complex along The Gambia river, with particular reference to the molecular forms of An. gambiae s. s. Malar J. 2008;7:182.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Jawara M, Pinder M, Drakeley CJ, Nwakanma DC, Jallow E, Bogh C, et al. Dry season ecology of Anopheles gambiae complex mosquitoes in The Gambia. Malar J. 2008;7:156.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Majambere S, Fillinger U, Sayer DR, Green C, Lindsay SW. Spatial distribution of mosquito larvae and the potential for targeted larval control in The Gambia. Am J Trop Med Hyg. 2008;79:19–27.

    Article  PubMed  Google Scholar 

  21. Opondo KO, Jawara M, Cham S, Jatta E, Jarju L, Camara M, et al. Status of insecticide resistance in Anopheles gambiae (s.l.) of The Gambia. Parasit Vectors. 2019;12:287.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Betson M, Jawara M, Awolola TS. Status of insecticide susceptibility in Anopheles gambiae s.l. from malaria surveillance sites in the Gambia. Malar J. 2009;8:187.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Scott JA, Brogdon WG, Collins FH. Identification of single specimens of the Anopheles gambiae complex by the polymerase chain reaction. Am J Trop Med Hyg. 1993;49:520–9.

    Article  CAS  PubMed  Google Scholar 

  24. Fanello C, Santolamazza F, della Torre A. Simultaneous identification of species and molecular forms of the Anopheles gambiae complex by PCR-RFLP. Med Vet Entomol. 2002;16:461–4.

    Article  CAS  PubMed  Google Scholar 

  25. Onyango SA, Ochwedo KO, Machani MG, Olumeh JO, Debrah I, Omondi CJ, et al. Molecular characterization and genotype distribution of thioester-containing protein 1 gene in Anopheles gambiae mosquitoes in western Kenya. Malar J. 2022;21:235.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Sougoufara S, Sokhna C, Diagne N, Doucouré S, Sembène PM, Harry M. The implementation of long-lasting insecticidal bed nets has differential effects on the genetic structure of the African malaria vectors in the Anopheles gambiae complex in Dielmo. Senegal Malar J. 2017;16:337.

    Article  PubMed  Google Scholar 

  27. Russell TL, Govella NJ, Azizi S, Drakeley CJ, Kachur SP, Killeen GF. Increased proportions of outdoor feeding among residual malaria vector populations following increased use of insecticide-treated nets in rural Tanzania. Malar J. 2011;10:80.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Pinder M, Jawara M, Jarju LB, Salami K, Jeffries D, Adiamoh M, et al. Efficacy of indoor residual spraying with dichlorodiphenyltrichloroethane against malaria in Gambian communities with high usage of long-lasting insecticidal mosquito nets: a cluster-randomised controlled trial. Lancet. 2015;385:1436–46.

    Article  CAS  PubMed  Google Scholar 

  29. Tangena JA, Adiamoh M, D’Alessandro U, Jarju L, Jawara M, Jeffries D, et al. Alternative treatments for indoor residual spraying for malaria control in a village with pyrethroid- and DDT-resistant vectors in the Gambia. PLoS ONE. 2013;8: e74351.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Wesolowski A, Eagle N, Tatem AJ, Smith DL, Noor AM, Snow RW, Buckee CO. Quantifying the impact of human mobility on malaria. Science. 2012;338:267–70.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Pradhan N, Tarai R, Hazra RK. Vector dynamics predicts transmission dynamics: a simple, realistic and sensible approach for measuring malaria endemicity. Bull Entomol Res. 2020;110:379–87.

    Article  PubMed  Google Scholar 

  32. Mafwele BJ, Lee JW. Relationships between transmission of malaria in Africa and climate factors. Sci Rep. 2022;12:14392.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Stresman GH. Beyond temperature and precipitation: ecological risk factors that modify malaria transmission. Acta Trop. 2010;116:167–72.

    Article  PubMed  Google Scholar 

  34. Molina-Cruz A, DeJong RJ, Ortega C, Haile A, Abban E, Rodrigues J, Jaramillo-Gutierrez G, Barillas-Mury C. Some strains of Plasmodium falciparum, a human malaria parasite, evade the complement-like system of Anopheles gambiae mosquitoes. Proc Natl Acad Sci USA. 2012;109:E1957–62.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references


We thank Mr Moussa Diallo and all field workers for their assistance in the field work for respective studies analysed for this study.


The study was supported with funding from PAMGEN (H3A/18/002) given to AAN.

Author information

Authors and Affiliations



MHA conceived study, analysed data and drafted manuscript. AJ performed laboratory work, analysed data and drafted manuscript. KOO, MON and BSA revised manuscript. AAN supervised the study and revised manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Majidah Hamid-Adiamoh.

Ethics declarations

Ethics approval and concept to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors have declared that no competing interests exist.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit The Creative Commons Public Domain Dedication waiver ( applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hamid-Adiamoh, M., Jabang, A.M.J., Opondo, K.O. et al. Distribution of Anopheles gambiae thioester-containing protein 1 alleles along malaria transmission gradients in The Gambia. Malar J 22, 89 (2023).

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: