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Malaria Journal
Published in: Malaria Journal 1/2016

Open Access 01-12-2016 | Research

Identification of blood meal sources in the main African malaria mosquito vector by MALDI-TOF MS

Authors: Sirama Niare, Jean-Michel Berenger, Constentin Dieme, Ogobara Doumbo, Didier Raoult, Philippe Parola, Lionel Almeras

Published in: Malaria Journal | Issue 1/2016

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Abstract

Background

The identification of blood meal sources in malaria vectors is critical to better understanding host/vector interactions and malaria epidemiology and control. Currently, the identification of mosquito blood meal origins is based on time-consuming and costly techniques such as precipitin tests, ELISA and molecular tools. Although these tools have been validated to identify the blood meal and trophic preferences of female Anopheles mosquitoes, they present several limitations. Recently, matrix-assisted, laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF MS) was successfully used as a quick and accurate tool for arthropod identification, including mosquitoes. The aim of the present work was to test whether MALDI-TOF MS could also be applied to identification of blood meal sources from engorged mosquitoes.

Methods

Abdomen proteins extracted from Anopheles gambiae (stricto sensu, S molecular form) that were either unengorged or artificially engorged on seven distinct types of vertebrate blood (human, horse, sheep, rabbit, mouse, rat, dog) were submitted for MALDI-TOF MS.

Results

The comparison of mass spectrometry (MS) spectra from mosquito abdomens collected 1 h post-feeding, were able to discriminate blood meal origins. Moreover, using Aedes albopictus specimens, abdominal protein MS spectra from engorged mosquitoes were found specific to host blood source and independent of the mosquito species. A sequential analysis revealed stability of mosquito abdominal protein spectra up to 24 h post-feeding.

Conclusions

These results indicate that MALDI-TOF MS could determine feeding patterns of freshly engorged mosquitoes up to 24 h post-blood meal. The MALDI-TOF MS technique appears to be an efficient tool for large epidemiological surveillance of vector-borne diseases and outbreak source identification.
Literature
1.
WHO. World malaria report 2014. Geneva: World Health Organization; 2014.
2.
Raghavendra K, Barik TK, Reddy BP, Sharma P, Dash AP. Malaria vector control: from past to future. Parasitol Res. 2011;108:757–79.CrossRefPubMed
3.
Bass C, Williamson MS, Wilding CS, Donnelly MJ, Field LM. Identification of the main malaria vectors in the Anopheles gambiae species complex using a TaqMan real-time PCR assay. Malar J. 2007;6:155.PubMedCentralCrossRefPubMed
4.
Githeko AK, Service MW, Mbogo CM, Atieli FK, Juma FO. Origin of blood meals in indoor and outdoor resting malaria vectors in western Kenya. Acta Trop. 1994;58:307–16.CrossRefPubMed
5.
Hervy JP, Le Goff G, Geoffroy B, Herv JP, Manga L, Brunhes J. Les Anopheles de la Région Afro-tropicale, Logiciel d’identification et d’enseignement, Collection Didactique, version ORSTOM. IRD. 1998.
6.
Zapata MA, Cienfuegos AV, Quiros OI, Quinones ML, Luckhart S, Correa MM. Discrimination of seven Anopheles species from San Pedro de Uraba, Antioquia, Colombia, by polymerase chain reaction-restriction fragment length polymorphism analysis of its sequences. Am J Trop Med Hyg. 2007;77:67–72.PubMed
7.
Kaufmann C, Schaffner F, Ziegler D, Pfluger V, Mathis A. Identification of field-caught Culicoides biting midges using matrix-assisted laser desorption/ionization time of flight mass spectrometry. Parasitology. 2012;139:248–58.CrossRefPubMed
8.
Yssouf A, Flaudrops C, Drali R, Kernif T, Socolovschi C, Berenger JM, et al. Matrix-assisted laser desorption ionization-time of flight mass spectrometry for rapid identification of tick vectors. J Clin Microbiol. 2013;51:522–8.PubMedCentralCrossRefPubMed
9.
Yssouf A, Socolovschi C, Flaudrops C, Ndiath MO, Sougoufara S, Dehecq JS, et al. Matrix-assisted laser desorption ionization–time of flight mass spectrometry: an emerging tool for the rapid identification of mosquito vectors. PLoS One. 2013;8:e72380.PubMedCentralCrossRefPubMed
10.
Yssouf A, Parola P, Lindstrom A, Lilja T, L’Ambert G, Bondesson U, et al. Identification of European mosquito species by MALDI-TOF MS. Parasitol Res. 2014;113:2375–8.CrossRefPubMed
11.
Suter T, Flacio E, Farina BF, Engeler L, Tonolla M, Muller P. First report of the invasive mosquito species Aedes koreicus in the Swiss-Italian border region. Parasit Vectors. 2015;8:402.PubMedCentralCrossRefPubMed
12.
Dieme C, Yssouf A, Vega-Rua A, Berenger JM, Failloux AB, et al. Accurate identification of Culicidae at aquatic developmental stages by MALDI-TOF MS profiling. Parasit Vectors. 2014;7:544.PubMedCentralCrossRefPubMed
13.
Molaei G, Andreadis TG, Armstrong PM, Diuk-Wasser M. Host-feeding patterns of potential mosquito vectors in Connecticut, USA: molecular analysis of bloodmeals from 23 species of Aedes, Anopheles, Culex, Coquillettidia, Psorophora, and Uranotaenia. J Med Entomol. 2008;45:1143–51.CrossRefPubMed
14.
Muturi EJ, Mwangangi JM, Beier JC, Blackshear M, Wauna J, Sang R, et al. Ecology and behavior of Anopheles arabiensis in relation to agricultural practices in central Kenya. J Am Mosq Control Assoc. 2013;29:222–30.CrossRefPubMed
15.
Fyodorova MV, Savage HM, Lopatina JV, Bulgakova TA, Ivanitsky AV, Platonova OV, et al. Evaluation of potential West Nile virus vectors in Volgograd region, Russia, 2003 (Diptera: Culicidae): species composition, bloodmeal host utilization, and virus infection rates of mosquitoes. J Med Entomol. 2006;43:552–63.CrossRefPubMed
16.
Tempelis CH. Host-feeding patterns of mosquitoes, with a review of advances in analysis of blood meals by serology. J Med Entomol. 1975;11:635–53.CrossRefPubMed
17.
Kent RJ. Molecular methods for arthropod bloodmeal identification and applications to ecological and vector-borne disease studies. Mol Ecol Resour. 2009;9:4–18.CrossRefPubMed
18.
Gomes B, Sousa CA, Vicente JL, Pinho L, Calderon I, Arez E, et al. Feeding patterns of molestus and pipiens forms of Culex pipiens (Diptera: Culicidae) in a region of high hybridization. Parasit Vectors. 2013;6:93.PubMedCentralCrossRefPubMed
19.
Ngo KA, Kramer LD. Identification of mosquito bloodmeals using polymerase chain reaction (PCR) with order-specific primers. J Med Entomol. 2003;40:215–22.CrossRefPubMed
20.
Martinez-de la Puente J, Ruiz S, Soriguer R, Figuerola J. Effect of blood meal digestion and DNA extraction protocol on the success of blood meal source determination in the malaria vector Anopheles atroparvus. Malar J. 2013;12:109.PubMedCentralCrossRefPubMed
21.
Oshaghi MA, Chavshin AR, Vatandoost H, Yaaghoobi F, Mohtarami F, Noorjah N. Effects of post-ingestion and physical conditions on PCR amplification of host blood meal DNA in mosquitoes. Exp Parasitol. 2006;112:232–6.CrossRefPubMed
22.
Good clinical laboratory pratice (World Health Organization) 2009.
23.
Awono-Ambene HP, Diawara L, Robert V. Comparison of direct and membrane feeding methods to infect Anopheles arabiensis with Plasmodium falciparum. Am J Trop Med Hyg. 2001;64:32–4.PubMed
24.
Townzen JS, Brower AV, Judd DD. Identification of mosquito bloodmeals using mitochondrial cytochrome oxidase subunit I and cytochrome b gene sequences. Med Vet Entomol. 2008;22:386–93.CrossRefPubMed
25.
Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol. 1994;3:294–9.PubMed
26.
27.
Muller P, Pfluger V, Wittwer M, Ziegler D, Chandre F, Simard F, et al. Identification of cryptic Anopheles mosquito species by molecular protein profiling. PLoS One. 2013;8:e57486.PubMedCentralCrossRefPubMed
28.
Schaffner F, Kaufmann C, Pfluger V, Mathis A. Rapid protein profiling facilitates surveillance of invasive mosquito species. Parasit Vectors. 2014;7:142.PubMedCentralCrossRefPubMed
29.
Massebo F, Balkew M, Gebre-Michael T, Lindtjorn B. Blood meal origins and insecticide susceptibility of Anopheles arabiensis from Chano in South-West Ethiopia. Parasit Vectors. 2013;6:44.PubMedCentralCrossRefPubMed
30.
Mwangangi JM, Mbogo CM, Nzovu JG, Githure JI, Yan G, Beier JC. Blood-meal analysis for anopheline mosquitoes sampled along the Kenyan coast. J Am Mosq Control Assoc. 2003;19:371–5.PubMed
31.
Onder O, Shao W, Kemps BD, Lam H, Brisson D. Identifying sources of tick blood meals using unidentified tandem mass spectral libraries. Nat Commun. 2013;4:1746.PubMedCentralCrossRefPubMed
32.
Wickramasekara S, Bunikis J, Wysocki V, Barbour AG. Identification of residual blood proteins in ticks by mass spectrometry proteomics. Emerg Infect Dis. 2008;14:1273–5.PubMedCentralCrossRefPubMed
33.
Kaufmann C, Steinmann IC, Hegglin D, Schaffner F, Mathis A. Spatio-temporal occurrence of Culicoides biting midges in the climatic regions of Switzerland, along with large scale species identification by MALDI-TOF mass spectrometry. Parasit Vectors. 2012;5:246.PubMedCentralCrossRefPubMed
34.
WHO. World malaria report 2010. Geneva: World Health Organization; 2010.
35.
Sambou M, Aubadie-Ladrix M, Fenollar F, Fall B, Bassene H, Almeras L, et al. Comparison of matrix-assisted laser desorption ionization-time of flight mass spectrometry and molecular biology techniques for identification of Culicoides (Diptera: ceratopogonidae) biting midges in Senegal. J Clin Microbiol. 2015;53:410–8.PubMedCentralCrossRefPubMed
36.
Mathis A, Depaquit J, Dvorak V, Tuten H, Banuls AL, Halada P. Identification of phlebotomine sand flies using one MALDI-TOF MS reference database and two mass spectrometer systems. Parasit Vectors. 2015;8:266.PubMedCentralCrossRefPubMed
37.
Yssouf A, Socolovschi C, Leulmi H, Kernif T, Bitam I, Audoly G, et al. Identification of flea species using MALDI-TOF/MS. Comp Immunol Microbiol Infect Dis. 2014;37:153–7.CrossRefPubMed
38.
Fotso FA, Mediannikov O, Diatta G, Almeras L, Flaudrops C, Parola P, et al. MALDI-TOF mass spectrometry detection of pathogens in vectors: the Borrelia crocidurae/Ornithodoros sonrai paradigm. PLoS Negl Trop Dis. 2014;8:e2984.CrossRef
39.
Yssouf A, Almeras L, Terras J, Socolovschi C, Raoult D, Parola P. Detection of Rickettsia spp in ticks by MALDI-TOF MS. PLoS Negl Trop Dis. 2015;9:e0003473.PubMedCentralCrossRefPubMed
40.
Yssouf A, Almeras L, Berenger JM, Laroche M, Raoult D, Parola P. Identification of tick species and disseminate pathogen using hemolymph by MALDI-TOF MS. Ticks Tick Borne Dis. 2015;6:579–86.CrossRefPubMed
Metadata
Title
Identification of blood meal sources in the main African malaria mosquito vector by MALDI-TOF MS
Authors
Sirama Niare
Jean-Michel Berenger
Constentin Dieme
Ogobara Doumbo
Didier Raoult
Philippe Parola
Lionel Almeras
Publication date
01-12-2016
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2016
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-016-1152-6

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