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Using MALDI-TOF MS to identify mosquitoes collected in Mali and their blood meals

Published online by Cambridge University Press:  07 February 2018

Fatalmoudou Tandina ,
Sirama Niaré ,
Maureen Laroche ,
Abdoulaye K Koné ,
Adama Z Diarra ,
Abdoulaye Ongoiba ,
Jean Michel Berenger ,
Ogobara K Doumbo ,
Didier Raoult  and
Philippe Parola
Fatalmoudou Tandina
Affiliation:
Aix Marseille Univ, IRD, AP-HM, IHU-Méditerranée Infection, SSA, VITROME, Marseille, France Department of Epidemiology of Parasitic Diseases, Malaria Research and Training Center, University of Science, Techniques and Technologies of Bamako, Mali
Sirama Niaré
Affiliation:
Aix Marseille Univ, IRD, AP-HM, IHU-Méditerranée Infection, SSA, VITROME, Marseille, France Department of Epidemiology of Parasitic Diseases, Malaria Research and Training Center, University of Science, Techniques and Technologies of Bamako, Mali
Maureen Laroche
Affiliation:
Aix Marseille Univ, IRD, AP-HM, IHU-Méditerranée Infection, SSA, VITROME, Marseille, France
Abdoulaye K Koné
Affiliation:
Department of Epidemiology of Parasitic Diseases, Malaria Research and Training Center, University of Science, Techniques and Technologies of Bamako, Mali
Adama Z Diarra
Affiliation:
Aix Marseille Univ, IRD, AP-HM, IHU-Méditerranée Infection, SSA, VITROME, Marseille, France Department of Epidemiology of Parasitic Diseases, Malaria Research and Training Center, University of Science, Techniques and Technologies of Bamako, Mali
Abdoulaye Ongoiba
Affiliation:
Department of Epidemiology of Parasitic Diseases, Malaria Research and Training Center, University of Science, Techniques and Technologies of Bamako, Mali
Jean Michel Berenger
Affiliation:
Aix Marseille Univ, IRD, AP-HM, IHU-Méditerranée Infection, SSA, VITROME, Marseille, France
Ogobara K Doumbo
Affiliation:
Department of Epidemiology of Parasitic Diseases, Malaria Research and Training Center, University of Science, Techniques and Technologies of Bamako, Mali
Didier Raoult
Affiliation:
Aix Marseille Univ, IRD, AP-HM, IHU-Méditerranée Infection, SSA, VITROME, Marseille, France
Philippe Parola*
Affiliation:
Aix Marseille Univ, IRD, AP-HM, IHU-Méditerranée Infection, SSA, VITROME, Marseille, France
*
Author for correspondence: Philippe Parola, Email: [email protected]
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Abstract

Matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF MS) has been recently described as an innovative and effective tool for identifying arthropods and mosquito blood meal sources. To test this approach in the context of an entomological survey in the field, mosquitoes were collected from five ecologically distinct areas of Mali. We successfully analysed the blood meals from 651 mosquito abdomens crushed on Whatman filter paper (WFPs) in the field using MALDI-TOF MS. The legs of 826 mosquitoes were then submitted for MALDI-TOF MS analysis in order to identify the different mosquito species. Eight mosquito species were identified, including Anopheles gambiae Giles, Anopheles coluzzii, Anopheles arabiensis, Culex quinquefasciatus, Culex neavei, Culex perexiguus, Aedes aegypti and Aedes fowleri in Mali. The field mosquitoes for which MALDI-TOF MS did not provide successful identification were not previously available in our database. These specimens were subsequently molecularly identified. The WFP blood meal sources found in this study were matched against human blood (n = 619), chicken blood (n = 9), cow blood (n = 9), donkey blood (n = 6), dog blood (n = 5) and sheep blood (n = 3). This study reinforces the fact that MALDI-TOF MS is a promising tool for entomological surveys.

Keywords

MALDI-TOF MSmosquitofieldblood mealsWhatmanMali
Type
Research Article
Information
Parasitology , Volume 145 , Issue 9 , August 2018 , pp. 1170 - 1182
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Copyright
Copyright © Cambridge University Press 2018 

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References

Anosike, JC, Nwoke, BE, Ajayi, EG, Onwuliri, CO, Okoro, OU, Oku, EE, Asor, JE, Amajuoyi, OU, Ikpeama, CA, Ogbusu, FI and Meribe, CO (2005) Lymphatic filariasis among the Ezza people of Ebonyi state, Eastern Nigeria. Annals of Agricultural and Environnemental Medicine 12, 181–186.Google Scholar
Bass, C, Williamson, MS, Wilding, CS, Donnelly, MJ and Field, LM (2007) Identification of the main malaria vectors in the Anopheles gambiae species complex using a TaqMan real-time PCR assay. Malaria Journal 6, 155.Google Scholar
Becker, N, Petriæ, D, Zgomba, M, Boase, C, Dahl, C, Madon, M and Kaiser, A (2010) Mosquitoes and Their Control, 2nd Edn. Heidelberg, Germany: Springer.Google Scholar
Brasil, P, Zalis, MG, de Pina-Costa, A, Siqueira, AM, Junior, CB, Silva, S, Areas, ALL, Pelajo-Machado, M, de Alvarenga, DAM, da Silva Santelli, ACF, Albuquerque, HG, Cravo, P, Santos de Abreu, FV, Peterka, CL, Zanini, GM, Suarez Mutis, MC, Pissinatti, A, Lourenco-de-Oliveira, R, de Brito, CFA, de Fatima Ferreira-da-Cruz, , Culleton, R and Daniel-Ribeiro, CT (2017) Outbreak of human malaria caused by Plasmodium simium in the Atlantic forest in Rio de Janeiro: a molecular epidemiological investigation. Lancet Global Health 5, 1038–1046.Google Scholar
Caglioti, C, Lalle, E, Castilletti, C, Carletti, F, Capobianchi, MR and Bordi, L (2013) Chikungunya virus infection: an overview. New Microbiology 36, 211–227.Google Scholar
de Wispelaere, M, Despres, P and Choumet, V (2017) European Aedes albopictus and Culex pipiens Are competent vectors for Japanese encephalitis virus. PLoS Neglected Tropical Diseases 11, e0005294.Google Scholar
Dieme, C, Yssouf, A, Vega-Rua, A, Berenger, JM, Failloux, AB, Raoult, D, Parola, P and Almeras, L (2014) Accurate identification of Culicidae at aquatic developmental stages by MALDI-TOF MS profiling. Parasites &Vectors 7, 544.Google Scholar
Fall, G, Diallo, M, Loucoubar, C, Faye, O and Sall, AA (2014) Vector competence of Culex neavei and Culex quinquefasciatus (Diptera: Culicidae) from Senegal for lineages 1, 2, koutango and a putative new lineage of west Nile virus. American Journal of Tropical Medicine and Hygiene 90, 747–754.Google Scholar
Fanello, C, Santolamazza, F and della, TA, (2002) Simultaneous identification of species and molecular forms of the Anopheles gambiae complex by PCR-RFLP. Medical and Veterinary Entomology 16, 461–464.Google Scholar
Folmer, O, Black, M, Hoeh, W, Lutz, R and Vrijenhoek, R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.Google Scholar
Fyodorova, MV, Savage, HM, Lopatina, JV, Bulgakova, TA, Ivanitsky, AV, Platonova, OV and Platonov, AE (2006) 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. Journal of Medical Entomology 43, 552–563.Google Scholar
Gardner, CL and Ryman, KD (2010) Yellow fever: a reemerging threat. Clinics in Laboratory Medicine 30, 237–260.Google Scholar
Gillies, MT and Coetzee, M (1987) A supplement to the Anophelinae of Africa south of the Sahara. South African Institute for Medical Research 55, 143p.Google Scholar
Gomes, B, Sousa, CA, Vicente, JL, Pinho, L, Calderon, I, Arez, E, Almeida, AP, Donnelly, MJ and Pinto, J (2013) Feeding patterns of molestus and pipiens forms of Culex pipiens (Diptera: Culicidae) in a region of high hybridization. Parasites & Vectors 6, 93.Google Scholar
Gould, E, Pettersson, J, Higgs, S, Charrel, R and de Lamballerie, X (2017) Emerging arboviruses: why today? One Health 4, 1–13.Google Scholar
Jupp, PG, McIntosh, BM and Blackburn, NK (1986) Experimental assessment of the vector competence of Culex (Culex) neavei theobald with west Nile and sindbis viruses in South Africa. Transactions of the Royal Society of Tropical Medicine and Hygiene 80, 226–230.Google Scholar
Komar, N (2003) West Nile virus: epidemiology and ecology in North America. Advances in Virus Research 61, 185–234.Google Scholar
Kumsa, B, Laroche, M, Almeras, L, Mediannikov, O, Raoult, D and Parola, P (2016) Morphological, molecular and MALDI-TOF mass spectrometry identification of ixodid tick species collected in Oromia, Ethiopia. Parasitology Research 115, 4199–4210.Google Scholar
Lafri, I, Almeras, L, Bitam, I, Caputo, A, Yssouf, A, Forestier, CL, Izri, A, Raoult, D and Parola, P (2016) Identification of Algerian field-caught phlebotomine sand Fly vectors by MALDI-TOF MS. PLoS Neglected Tropical Diseases 10, e0004351.Google Scholar
Lo, CI, Fall, B, Sambe-Ba, B, Diawara, S, Gueye, MW, Mediannikov, O, Sokhna, C, Faye, N, Dieme, Y, Wade, B, Raoult, D and Fenollar, F (2015) MALDI-TOF Mass spectrometry: a powerful tool for clinical microbiology at hopital principal de Dakar, Senegal (West Africa). PLoS ONE 10, e0145889.Google Scholar
Muturi, EJ, Mwangangi, JM, Beier, JC, Blackshear, M, Wauna, J, Sang, R and Mukabana, WR (2013) Ecology and behavior of Anopheles arabiensis in relation to agricultural practices in central Kenya. Journal of the American Mosquito Control Association 29, 222–230.Google Scholar
Nebbak, A, Willcox, AC, Bitam, I, Raoult, D, Parola, P and Almeras, L (2016) Standardization of sample homogenization for mosquito identification using an innovative proteomic tool based on protein profiling. Proteomics 16, 3148–3160.Google Scholar
Nebbak, A, Koumare, S, Willcox, AC, Raoult, D, Almeras, L and Parola, P (2017) Field application of MALDI-TOF MS on mosquito larvae identification. Parasitology 3, 1–11.Google Scholar
Niare, S, Berenger, JM, Dieme, C, Doumbo, O, Raoult, D, Parola, P and Almeras, L (2016) Identification of blood meal sources in the main African malaria mosquito vector by MALDI-TOF MS. Malariar Journal 15, 87.Google Scholar
Niare, S, Almeras, L, Tandina, F, Yssouf, A, Bacar, A, Toilibou, A, Doumbo, O, Raoult, D and Parola, P (2017) MALDI-TOF MS identification of Anopheles gambiae giles blood meal crushed on Whatman filter papers. PLoS One 12, e0183238.Google Scholar
Nikolay, B, Diallo, M, Faye, O, Boye, CS and Sall, AA (2012) Vector competence of Culex neavei (Diptera: Culicidae) for usutu virus. American Journal of Tropical Medicine and Hygiene 86, 993–996.Google Scholar
Onder, O, Shao, W, Kemps, BD, Lam, H and Brisson, D (2013) Identifying sources of tick blood meals using unidentified tandem mass spectral libraries. Nature Communication 4, 1746.Google Scholar
Raharimalala, FN, Andrianinarivomanana, TM, Rakotondrasoa, A, Collard, JM and Boyer, S (2017) Usefulness and accuracy of MALDI-TOF mass spectrometry as a supplementary tool to identify mosquito vector species and to invest in development of international database. Medical and Veterinary Entomology 31, 289–298.Google Scholar
Sambou, M, Aubadie-Ladrix, M, Fenollar, F, Fall, B, Bassene, H, Almeras, L, Sambe-Ba, B, Perrot, N, Chatellier, S, Faye, N, Parola, P, Wade, B, Raoult, D and Mediannikov, O (2015) 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. Journal of Clinical Microbiology 53, 410–418.Google Scholar
Schaffner, F, Kaufmann, C, Pfluger, V and Mathis, A (2014) Rapid protein profiling facilitates surveillance of invasive mosquito species. Parasites & Vectors 7, 142.Google Scholar
Smith, JL and Fonseca, DM (2004) Rapid assays for identification of members of the Culex (Culex) pipiens complex, their hybrids, and other sibling species (Diptera: Culicidae). American Journal of Tropical Medicine and Hygiene 70, 339–345.Google Scholar
Sogoba, N, Doumbia, S, Vounatsou, P, Baber, I, Keita, M, Maiga, M, Traore, SF, Toure, A, Dolo, G, Smith, T and Ribeiro, JM (2007) Monitoring of larval habitats and mosquito densities in the Sudan Savanna of Mali: implications for malaria vector control. American Journal of Tropical Medicine and Hygiene 77, 82–88.Google Scholar
Vasilakis, N, Cardosa, J, Hanley, KA, Holmes, EC and Weaver, SC (2011) Fever from the forest: prospects for the continued emergence of sylvatic dengue virus and its impact on public health. Nature Reviews Microbiology 9, 532–541.Google Scholar
WHO (1992) Entomological Field Techniques for Malaria Control. Part I, Learners Guide. Geneva: World Health Organization.Google Scholar
WHO (2016) World Malaria Report 2016. Geneva: World Health Organization.Google Scholar
Yssouf, A, Socolovschi, C, Flaudrops, C, Ndiath, MO, Sougoufara, S, Dehecq, JS, Lacour, G, Berenger, JM, Sokhna, CS, Raoult, D and Parola, P (2013) Matrix-assisted laser desorption ionization–time of flight mass spectrometry: an emerging tool for the rapid identification of mosquito vectors. PLoS ONE 8, e72380.Google Scholar
Yssouf, A, Parola, P, Lindstrom, A, Lilja, T, L'Ambert, G, Bondesson, U, Berenger, JM, Raoult, D and Almeras, L (2014a) Identification of European mosquito species by MALDI-TOF MS. Parasitology Research 113, 2375–2378.Google Scholar
Yssouf, A, Socolovschi, C, Leulmi, H, Kernif, T, Bitam, I, Audoly, G, Almeras, L, Raoult, D and Parola, P (2014b) Identification of flea species using MALDI-TOF/MS. Comparative Immunology, Microbiology and Infectious Diseases 37, 153–157.Google Scholar
Yssouf, A, Almeras, L, Berenger, JM, Laroche, M, Raoult, D and Parola, P (2015) Identification of tick species and disseminate pathogen using hemolymph by MALDI-TOF MS. Ticks and Tick-Borne Diseases 6, 579–586.Google Scholar
Yssouf, A, Almeras, L, Raoult, D and Parola, P (2016) Emerging tools for identification of arthropod vectors. Future Microbiology 11, 549–566.Google Scholar