First report on mild insecticide resistance in newly established Aegean Aedes albopictus populations of Turkey

The invasive nature of Aedes albopictus, a competent vector of dengue, zika, yellow fever, and chikungunya viruses, has spread to many parts of the world. To date, there have been no report regarding the insecticide resistance status of Aedes albopictus populations along the Aegean coasts of Turkey. This study aims to confirm the occurrence of Aedes albopictus populations in the Aegean region of Turkey and test their susceptibility against different insecticide classes. Bioassay for susceptibility to Dikloro difenil trikloroetan (DDT) (4%), propoxur (0.1%), fenitrothion (1%), bendiocarb (0.1%), permethrin (0.75%), and deltamethrin (0.05%) of each population was assessed through the World Health Organization (WHO) standard bioassay test. A total of 675 adult Aedes albopictus samples were analysed from four populations in addition to control group and laboratory population. Results showed that all of the populations were resistant or at least possible resistant to DDT. In addition to that, all of the populations showed susceptibility against bendiocarb, propoxur, and fenitrothion except the Didim population, which is a possible resistant to propoxur and fenitrothion and the Bodrum population which is a possible resistant to fenitrothion. Results also indicated reduced mortality against permethrin in the Kuşadası and Güzelçamlı populations, while all of the populations were susceptible to deltamethrin. This study might help public health authorities to choose proper insecticide in control activities before insecticide resistance spread other populations and fix in these populations.

___

  • Aizoun N, Osse R, Azondekon R, Alia R, Oussou O et al. (2013). Comparison of the standard WHO susceptibility tests and the CDC bottle bioassay for the determination of insecticide susceptibility in malaria vectors and their correlation with biochemical and molecular biology assays in Benin, West Africa. Parasit Vectors 6:147.
  • Akıner MM (2019). Asya Kaplan sivrisineği ve sarıhumma sivrisineğinin Türkiye’deki durumu. In: Şaylan DÜ (editor). Meraklısına Bilim. 1st ed. İstanbul, Türkiye: Doğan Egmont Yayıncılık ve Yapımcılık, p. 179. (in Turkish).
  • Akiner MM, Demirci B, Babuadze G, Robert V, Schaffner F (2016). Spread of the Invasive Mosquitoes Aedes aegypti and Aedes albopictus in the Black Sea Region Increases Risk of Chikungunya, Dengue, and Zika Outbreaks in Europe. Plos Neglected Tropical Diseases 10 (4): e0004664.
  • Akıner MM, Demirci B, Bedir H, Öztürk M, Demirtaş R et al. (2018). Surveillance and control of invasive Aedes species in the Eastern Black Sea area of Turkey. Türk Hijyen ve Deneysel Biyoloji Dergisi 75 (3): 225-238.
  • Arslan A, Rathor HR, Mukhtar MU, Mushtaq S, Bhatti A, Asif M, Arshad I, Ahmad JF (2016). Spatial distribution and insecticide susceptibility status of Aedes aegypti and Aedes albopictus in dengue affected urban areas of Rawalpindi, Pakistan. Journal of Vector Borne Diseases 53 (2):136–143.
  • Balaska S, Fotakis EA, Kioulos I, Grigoraki L, Mpellou S, Chaskopoulou A, Vontas J (2020). Bioassay and molecular monitoring of insecticide resistance status in Aedes albopictus populations from Greece, to support evidence-based vector control. Parasites & vectors 13 (1): 328.
  • Becker N, Petric D, Zgomba M, Boase C, Madon M, Dahl C, Kaiser A (2003). Mosquitoes and Their Control. New York: Kluwer Academic/Plenum Publishers, pp. 498.
  • Benedict MQ, Levine RS, Hawley WA, Lounibos LP (2007). Spread of the tiger: global risk of invasion by the mosquito Aedes albopictus. Vector Borne Zoonotic Diseases 7:76–85.
  • Bengoa M, Eritja R, Delacour S, Miranda MÁ, Sureda A, Lucientes J (2017) First data on resistance to pyrethroids in wild populations of Aedes albopictus from Spain. J Am Mosquito Contr 33:246–249.
  • Bharati M, Rai P, Saha, D (2019). Insecticide resistance in Aedes albopictus Skuse from sub-Himalayan districts of West Bengal, India. Acta tropica 192: 104–111.
  • Brengues, C, Hawkes NJ, Chandre F, McCarroll L, Duchon S, Guillet P, Manguin S, Morgan J.C, Hemingway J (2003). Pyrethroid and DDT cross-resistance in Aedes aegypti is correlated with novel mutations in the voltage-gated sodium channel gene. Medical and veterinary entomology 17(1): 87–94.
  • Caminade C, Medlock JM, Ducheyne E, McIntyre KM, Leach S, Baylis M (2012). Suitability of European climate for the Asian tiger mosquito Aedes albopictus: recent trends and future scenarios. Journal of the Royal Society Interface 9:2708–17.
  • Caraballo H (2014). Emergency Department Management of Mosquito-Borne Illness: Malaria, Dengue, and West Nile Virus. Emergency Medicine Practice 16(5):1–23.
  • Centers for Disease Control and Prevention (2017). Chikungunya virus in the united states. Atlanta.
  • Centers for Disease Control and Prevention (2020). CDC Yellow Book 2020. Health information for International Travel. Editor in Chief: Gary W. Brunette, Jeffrey B. Nemhauser.
  • Chevillon C, Raymond M, Guillemaud T, Lenormand T, Pasteur N (1999). Population genetics of insecticide resistance in the mosquito Culex pipiens. Biological Journal of the Linnean Society 68(1):147–57.
  • European Centre for Disease Preventation and Control (2019) (b). Factsheet: Aedes albopictus. Stockholm.
  • European Centre for Disease Prevention and Control (2019) (a) Zika. In: ECDC. Annual epidemiological report for 2018. Stockholm.
  • European Centre for Disease Prevention and Control (2019) (c). Aedes albopictus, Current known distribution: January 2019. Stockholm.
  • Fotakis EA, Giantsis IA, Avgerinou A, Kourtidis S, Agathaggelidou E, Kapoula C (2019). Identification of Leishmania species in naturally infected sand flies from refugee camps, Greece. Emerging Infectious Disease journal 25(2):361–364.
  • Franklinos LHV, Jones KE, Redding DW, Abubakar I (2019). The effect of global change on mosquito-borne disease. The Lancet Infectious Diseases 19(9): e302-e12.
  • Gratz NG (2004). Critical review of the vector status of Aedes albopictus. Medical and Veterinary Entomology 18: 215–27.
  • Hemingway J, Hawkes NJ, Mc Carroll L, Ranson H (2004). The molecular basis of insecticide resistance in mosquitoes. Insect Biochemistry and Molecular Biology 34: 653–665.
  • Ishak IH, Jaal Z, Ranson H, Wondji CS (2015). Contrasting patterns of insecticide resistance and knockdown resistance (kdr) in the dengue vectors Aedes aegypti and Aedes albopictus from Malaysia. Parasites & Vectors 8:181.
  • Kawada H, Maekawa Y, Abe M, Ohashi K, Ohba S, Takagi M (2010). Spatial distribution and pyrethroid susceptibility of mosquito larvae collected from catch basins in parks in Nagasaki City, Nagasaki, Japan. Jpn J Infect Dis 63:19–24.
  • Kolankaya D. (2006). Organochlorine pesticide reidues and their toxic effects on the environment and organisms in Turkey. International Journal of Environmental Analytical Chemistry 86:147-160.
  • Kushwah RB, Mallick PK, Ravikumar H, Dev V, Kapoor N, Adak, TP, Singh OP (2015). Status of DDT and pyrethroid resistance in Indian Aedes albopictus and absence of knockdown resistance (kdr) mutation. J Vector Dis 52(1): 95-98.
  • Leta S, Beyene TJ, De Clercq EM, Amenu K, Kraemer MUG, Revie CW (2018). Global risk mapping for major diseases transmitted by Aedes aegypti and Aedes albopictus. International Journal of Infectious Disease 67: 25-35.
  • Li Y, Xu J, Zhong D, Zhang H, Yang W et al. (2017). Evidence for multiple-insecticide resistance in urban Aedes albopictus populations in southern China. Parasites & Vectors 11:4
  • Liu N (2015). Insecticide resistance in mosquitoes: impact, mechanisms, and research directions. Annu Review of Entomology 60:537-559.
  • Moyes CL, Vontas J, Martins AJ, Nig LC, Koou SY, Dusfour I, Raghavendra K, Pinto J, Corbel V, David JP, Weetman D (2017). Contemporary status of insecticide resistance in the major Aedes vectors of arboviruses infecting humans. PLoS Neglected Tropical Diseases 11(7): e0005625.
  • Ngoagouni C, Kamgang B, Brengues C, Yahouédo GA, Paupy C, Nakouné E, Kazanji M, Chandre F (2016). Susceptibility profile and metabolic mechanisms involved in Aedes aegypti and Aedes albopictus resistant to DDT and deltamethrin in the Central African Republic. Parasites & Vectors 9 (1): 599.
  • Oter K, Gunay F, Tuzer E, Linton YM, Bellini R, Alten B (2013). First record of Stegomyia albopicta in Turkey determined by active ovitrap surveillance and DNA barcoding. Vector Borne Zoonotic Diseases 13 (10): 753-61.
  • Paaijmans K, Brustollin M, Aranda C, Eritja R, Talavera S et al (2019). Phenotypic insecticide resistance in arbovirus mosquito vectors in Catalonia and its capital Barcelona (Spain). PLoS ONE 14(7): e0217860.
  • Pichler V, Bellini R, Veronesi R, Arnoldi D, Rizzoli A et al. (2018). First evidence of resistance to pyrethroid insecticides in Italian Aedes albopictus populations 26years after invasion. Pest management science 74 (6): 1319-1327 .
  • Pichler V, Malandruccolo C, Serini P, Bellini R, Severini F et al. (2019). Phenotypic and genotypic pyrethroid resistance of Aedes albopictus, with focus on the 2017 chikungunya outbreak in Italy. Pest management science 75 (10): 2642-2651.
  • Ramasamy R, Surendran SN, Jude PJ, Dharshini S, Vinobaba M (2011) Larval Development of Aedes aegypti and Aedes albopictus in Peri-Urban Brackish Water and Its Implications for Transmission of Arboviral Diseases. PLoS Neglected Tropical Diseases 5(11): e1369.
  • Şakacı Z (2021). Contribution to mosquito (Diptera: Culicidae) fauna of Sakarya province and the first record of the invasive vector Aedes albopictus (Skuse, 1894) for Kocaeli province . Balıkesir Üniversitesi Fen Bilimleri Enstitüsü Dergisi 23 (1): 10-21.
  • Schaffner E, Angel G, Geoffroy B, Hervy JP, et al.(2001). The Mosquitoes of Europe [CD-ROM]. Paris: IRD Edition.
  • Scholte EJ, Schaffner F (2007). Emerging pests and vector-borne diseases in Europe. Wageningen Academic Publishers, Wageningen.
  • Somboon P, Prapanthadara L, Suwonkerd W (2003). Insecticide susceptibility tests of Anopheles minimus s.l., Aedes aegypti, Aedes albopictus, and Culex quinquefasciatus in northern Thailand. The Southeast Asian Journal of Tropical Medicine Public Health 34: 87-93.
  • Stanaway JD, Shepard DS, Undurraga EA, Halasa YA, Coffeng LE et al. (2016). The global burden of dengue: An analysis from the Global Burden of Disease Study 2013. Lancet Infectious Diseases 16: 712-723.
  • Statsoft. 2013. STATISTICA, release 12.0. Tulsa, OK, USA, Statsoft Inc.
  • Suter T, Crespo M, Oliveira MF, Oliveira TS, Melo-Santos MA, Oliveira CD, Ayres C, Barbosa R, Araújo AP, Regis L, Flacio E, Engeler L, Müller P, Silva-Filha MH (2017). Insecticide susceptibility of Aedes albopictus and Ae. aegypti from Brazil and the Swiss-Italian border region. Parasites & Vectors 10: 431.
  • Torun H (2017). Herbisitler ve Türkiye’deki Ruhsatlı Herbisitlerin Güncel Durumu. Turkish Journal of Weed Science 20 (2): 61-68.
  • Turgut C, Cutright TJ, Mermer S, Atatanır L, Turgut N et al. (2013). The Source of DDT and its metabolites contamination in Turkish agricultural soils. Environment Monitoring and Assessment 185:1087-1093.
  • Türkozan S (2019). Türkiye’de Aedes (Stegomyia) albopictus (Skuse, 1894)’un populasyon genetiği ve ekolojik niş modellemesi. Yüksek lisans tezi. Aydın Adnan Menderes Üniversitesi Fen Bilimleri Enstitüsü. Aydın, Türkiye.
  • Whitehorn J, Yacoub S (2019). Global warming and arboviral infections. Clinical Medicine Journal (Lond) 19 (2): 149-52.
  • World Health Organization (2016). Test procedures for insecticide resistance monitoring in malaria vector mosquitoes, 2nd edition, Geneva.
  • Yavaşoğlu S (2019). Akdeniz ve Ege Bölgesi’nin vektör sivrisinek türlerinde insektisit direncinin moleküler ve biyokimyasal tekniklerle belirlenmesi. Doktora tezi. Aydın Adnan Menderes Üniversitesi Fen Bilimleri Enstitüsü. Aydın, Türkiye.
Turkish Journal of Zoology-Cover
  • ISSN: 1300-0179
  • Yayın Aralığı: Yılda 6 Sayı
  • Yayıncı: TÜBİTAK