Skip to main content
Top
Published in: Malaria Journal 1/2019

Open Access 01-12-2019 | Malaria | Research

Human exposure to Anopheles farauti bites in the Solomon Islands is not associated with IgG antibody response to the gSG6 salivary protein of Anopheles gambiae

Authors: Edgar J. M. Pollard, Catriona Patterson, Tanya L. Russell, Alan Apairamo, Jance Oscar, Bruno Arcà, Chris Drakeley, Thomas R. Burkot

Published in: Malaria Journal | Issue 1/2019

Login to get access

Abstract

Background

Mosquito saliva elicits immune responses in humans following mosquito blood feeding. Detection of human antibodies recognizing the Anopheles gambiae salivary gland protein 6 (gSG6) or the gSG6-P1 peptide in residents of Africa, South America and Southeast Asia suggested the potential for these antibodies to serve as a universal marker to estimate human biting rates. Validating the utility of this approach requires concurrent comparisons of anopheline biting rates with antibodies to the gSG6 protein to determine the sensitivity and specificity of the assay for monitoring changes in vector populations. This study investigated whether seroprevalence of anti-gSG6 antibodies in humans reflected the relative exposure to Anopheles farauti bites in the Solomon Islands as estimated from sympatric human landing catches.

Methods

Human biting rates by An. farauti were estimated by landing catches at 10 sampling sites in each of 4 villages during the wet and dry seasons. Human serum samples from these same villages were also collected during the wet and dry seasons and analysed for antibody recognition of the gSG6 antigen by the Luminex xMAP© platform. Antibody titres and prevalence were compared to HLCs at the sampling sites nearest to participants’ residences for utility of anti-gSG6 antibodies to estimate human exposure to anopheline bites.

Results

In this study in the Solomon Islands only 11% of people had very high anti-gSG6 antibody titres, while other individuals did not recognize gSG6 despite nightly exposures of up to 190 bites by An. farauti. Despite clear spatial differences in the human biting rates within and among villages, associations between anti-gSG6 antibody titres and biting rates were not found.

Conclusions

Few studies to date have concurrently measured anopheline biting rates and the prevalence of human antibodies to gSG6. The lack of association between anti-gSG6 antibody titres and concurrently measured human biting rates suggests that the assay for human anti-gSG6 antibodies lacks sufficient sensitivity to be a biomarker of An. farauti exposure at an epidemiologically relevant scale. These findings imply that an improvement in the sensitivity of serology to monitor changes in anopheline biting exposure may require the use of saliva antigens from local anophelines, and this may be especially true for species more distantly related to the African malaria vector An. gambiae.
Literature
1.
go back to reference Bousema T, Griffin JT, Sauerwein RW, Smith DL, Churcher TS, Takken W, et al. Hitting hotspots: spatial targeting of malaria for control and elimination. PLoS Med. 2012;9:e1001165.CrossRef Bousema T, Griffin JT, Sauerwein RW, Smith DL, Churcher TS, Takken W, et al. Hitting hotspots: spatial targeting of malaria for control and elimination. PLoS Med. 2012;9:e1001165.CrossRef
2.
go back to reference WHO. A framework for malaria elimination. Geneva: World Health Organization; 2017. WHO. A framework for malaria elimination. Geneva: World Health Organization; 2017.
3.
go back to reference Burkot TR, Graves PM, Cattan JA, Wirtz RA, Gibson FD. The efficiency of sporozoite transmission in the human malarias, Plasmodium falciparum and P. vivax. Bull World Health Organ. 1987;65:375–80. Burkot TR, Graves PM, Cattan JA, Wirtz RA, Gibson FD. The efficiency of sporozoite transmission in the human malarias, Plasmodium falciparum and P. vivax. Bull World Health Organ. 1987;65:375–80.
4.
go back to reference Tusting LS, Bousema T, Smith DL, Drakeley C. Measuring changes in Plasmodium falciparum transmission: precision, accuracy and costs of metrics. Adv Parasitol. 2014;84:151–208.CrossRef Tusting LS, Bousema T, Smith DL, Drakeley C. Measuring changes in Plasmodium falciparum transmission: precision, accuracy and costs of metrics. Adv Parasitol. 2014;84:151–208.CrossRef
5.
go back to reference Burkot TR, Bugoro H, Apairamo A, Cooper RD, Echeverry DF, Odabasi D, et al. Spatial-temporal heterogeneity in malaria receptivity is best estimated by vector biting rates in areas nearing elimination. Parasit Vectors. 2018;11:606.CrossRef Burkot TR, Bugoro H, Apairamo A, Cooper RD, Echeverry DF, Odabasi D, et al. Spatial-temporal heterogeneity in malaria receptivity is best estimated by vector biting rates in areas nearing elimination. Parasit Vectors. 2018;11:606.CrossRef
6.
go back to reference Lombardo F, Ronca R, Rizzo C, Mestres-Simòn M, Lanfrancotti A, Currà C, et al. The Anopheles gambiae salivary protein gSG6: an anopheline-specific protein with a blood-feeding role. Insect Biochem Mol Biol. 2009;39:457–66.CrossRef Lombardo F, Ronca R, Rizzo C, Mestres-Simòn M, Lanfrancotti A, Currà C, et al. The Anopheles gambiae salivary protein gSG6: an anopheline-specific protein with a blood-feeding role. Insect Biochem Mol Biol. 2009;39:457–66.CrossRef
7.
go back to reference 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.CrossRef 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.CrossRef
8.
go back to reference 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.CrossRef 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.CrossRef
9.
go back to reference Drame P, Machault V, Diallo A, Cornelie S, Poinsignon A, Lalou R, et al. IgG responses to the gSG6-P1 salivary peptide for evaluating human exposure to Anopheles bites in urban areas of Dakar region. Senegal Malar J. 2012;11:72.CrossRef Drame P, Machault V, Diallo A, Cornelie S, Poinsignon A, Lalou R, et al. IgG responses to the gSG6-P1 salivary peptide for evaluating human exposure to Anopheles bites in urban areas of Dakar region. Senegal Malar J. 2012;11:72.CrossRef
10.
go back to reference 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. 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.
11.
go back to reference 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. 2016;215:396–404.PubMedCentral 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. 2016;215:396–404.PubMedCentral
12.
go back to reference Idris ZM, Chan CW, Mohammed M, Kalkoa M, Taleo G, Junker K, et al. Serological measures to assess the efficacy of malaria control programme on Ambae Island. Vanuatu Parasit Vectors. 2017;10:204.CrossRef Idris ZM, Chan CW, Mohammed M, Kalkoa M, Taleo G, Junker K, et al. Serological measures to assess the efficacy of malaria control programme on Ambae Island. Vanuatu Parasit Vectors. 2017;10:204.CrossRef
13.
go back to reference McLaughlin K, Russell TL, Apairamo A, Bugoro H, Oscar J, Cooper RD, et al. Smallest Anopheles farauti occur during the peak transmission season in the Solomon Islands. Malar J. 2019;18:208.CrossRef McLaughlin K, Russell TL, Apairamo A, Bugoro H, Oscar J, Cooper RD, et al. Smallest Anopheles farauti occur during the peak transmission season in the Solomon Islands. Malar J. 2019;18:208.CrossRef
14.
go back to reference Russell TL, Beebe NW, Bugoro H, Apairamo A, Chow WK, Cooper RD, et al. Frequent blood feeding enables insecticide-treated nets to reduce transmission by mosquitoes that bite predominately outdoors. Malar J. 2016;15:156.CrossRef Russell TL, Beebe NW, Bugoro H, Apairamo A, Chow WK, Cooper RD, et al. Frequent blood feeding enables insecticide-treated nets to reduce transmission by mosquitoes that bite predominately outdoors. Malar J. 2016;15:156.CrossRef
15.
go back to reference Belkin JN. The mosquitoes of the South Pacific (Diptera, Culicidae). Berkeley and Los Angeles: University of California Press; 1962. Belkin JN. The mosquitoes of the South Pacific (Diptera, Culicidae). Berkeley and Los Angeles: University of California Press; 1962.
16.
go back to reference Beebe NW, Saul A. Discrimination of all members of the Anopheles punctulatus complex by polymerase chain reaction - restriction fragment length polymorphism analysis. Am J Trop Med Hyg. 1995;53:478–81.CrossRef Beebe NW, Saul A. Discrimination of all members of the Anopheles punctulatus complex by polymerase chain reaction - restriction fragment length polymorphism analysis. Am J Trop Med Hyg. 1995;53:478–81.CrossRef
17.
go back to reference Wu L, Hall T, Ssewanyana I, Oulton T, Patterson C, Vasileva H, et al. Optimisation and standardisation of a multiplex immunoassay of diverse Plasmodium falciparum antigens to assess changes in malaria transmission using sero-epidemiology. Wellcome Open Research. 2019;4:26.CrossRef Wu L, Hall T, Ssewanyana I, Oulton T, Patterson C, Vasileva H, et al. Optimisation and standardisation of a multiplex immunoassay of diverse Plasmodium falciparum antigens to assess changes in malaria transmission using sero-epidemiology. Wellcome Open Research. 2019;4:26.CrossRef
18.
go back to reference Charlwood J, Hall T, Nenhep S, Rippon E, Branca-Lopes A, Steen K, et al. Spatial repellents and malaria transmission in an endemic area of Cambodia with high mosquito net usage. MalariaWorld J. 2017;8. Charlwood J, Hall T, Nenhep S, Rippon E, Branca-Lopes A, Steen K, et al. Spatial repellents and malaria transmission in an endemic area of Cambodia with high mosquito net usage. MalariaWorld J. 2017;8.
19.
go back to reference 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.CrossRef 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.CrossRef
20.
go back to reference Rizzo C, Ronca R, Fiorentino G, Mangano V, Sirima S, Nebie I, et al. Wide cross-reactivity between Anopheles gambiae and Anopheles funestus SG6 salivary proteins supports exploitation of gSG6 as a marker of human exposure to major malaria vectors in tropical Africa. Malar J. 2011;10:206.CrossRef Rizzo C, Ronca R, Fiorentino G, Mangano V, Sirima S, Nebie I, et al. Wide cross-reactivity between Anopheles gambiae and Anopheles funestus SG6 salivary proteins supports exploitation of gSG6 as a marker of human exposure to major malaria vectors in tropical Africa. Malar J. 2011;10:206.CrossRef
21.
go back to reference 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.CrossRef 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.CrossRef
22.
go back to reference Arcà B, Lombardo F, Struchiner CJ, Ribeiro JMC. Anopheline salivary protein genes and gene families: an evolutionary overview after the whole genome sequence of sixteen Anopheles species. BMC Genomics. 2017;18:153.CrossRef Arcà B, Lombardo F, Struchiner CJ, Ribeiro JMC. Anopheline salivary protein genes and gene families: an evolutionary overview after the whole genome sequence of sixteen Anopheles species. BMC Genomics. 2017;18:153.CrossRef
23.
go back to reference Scarpassa VM, Debat HJ, Alencar RB, Saraiva JF, Calvo E, Arcà B, et al. An insight into the sialotranscriptome and virome of Amazonian anophelines. BMC Genomics. 2019;20:166.CrossRef Scarpassa VM, Debat HJ, Alencar RB, Saraiva JF, Calvo E, Arcà B, et al. An insight into the sialotranscriptome and virome of Amazonian anophelines. BMC Genomics. 2019;20:166.CrossRef
24.
go back to reference Schenone FH, Olea NA, Rojas SA, García DN. Malaria en Chile: 1913–2001. Revista Médica de Chile. 2002;130:1170–6.PubMed Schenone FH, Olea NA, Rojas SA, García DN. Malaria en Chile: 1913–2001. Revista Médica de Chile. 2002;130:1170–6.PubMed
25.
go back to reference González C, Sallum M. Anopheles (Nyssorhynchus) atacamensis (Diptera: Culicidae), a new species from Northern Chile. Mem Inst Oswaldo Cruz. 2010;105:13–24.CrossRef González C, Sallum M. Anopheles (Nyssorhynchus) atacamensis (Diptera: Culicidae), a new species from Northern Chile. Mem Inst Oswaldo Cruz. 2010;105:13–24.CrossRef
26.
go back to reference Burkot TR, Graves PM, Paru R, Wirtz RA, Heywood PF. Human malaria transmission studies in the Anopheles punctulatus Complex in Papua New Guinea: sporozoite rates, inoculation rates, and sporozoite densities. Am J Trop Med Hyg. 1988;39:135–44.CrossRef Burkot TR, Graves PM, Paru R, Wirtz RA, Heywood PF. Human malaria transmission studies in the Anopheles punctulatus Complex in Papua New Guinea: sporozoite rates, inoculation rates, and sporozoite densities. Am J Trop Med Hyg. 1988;39:135–44.CrossRef
Metadata
Title
Human exposure to Anopheles farauti bites in the Solomon Islands is not associated with IgG antibody response to the gSG6 salivary protein of Anopheles gambiae
Authors
Edgar J. M. Pollard
Catriona Patterson
Tanya L. Russell
Alan Apairamo
Jance Oscar
Bruno Arcà
Chris Drakeley
Thomas R. Burkot
Publication date
01-12-2019
Publisher
BioMed Central
Keyword
Malaria
Published in
Malaria Journal / Issue 1/2019
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-019-2975-8

Other articles of this Issue 1/2019

Malaria Journal 1/2019 Go to the issue