Phenotypic and genotypic pyrethroid resistance of Aedes albopictus, with focus on the 2017 chikungunya outbreak in Italy.
Europe
arbovirus vector
insecticide resistance
mosquito
Journal
Pest management science
ISSN: 1526-4998
Titre abrégé: Pest Manag Sci
Pays: England
ID NLM: 100898744
Informations de publication
Date de publication:
Oct 2019
Oct 2019
Historique:
received:
11
10
2018
revised:
31
12
2018
accepted:
02
02
2019
pubmed:
8
2
2019
medline:
18
12
2019
entrez:
8
2
2019
Statut:
ppublish
Résumé
The highly invasive mosquito species Aedes albopictus has become a major health concern in temperate areas due to its role as vector of exotic arboviruses. Pyrethroid insecticides represent the main tools for limiting the circulation of such mosquito-borne viruses. The present work aim to extend previous reports on phenotypic pyrethroid-resistance in European Ae. albopictus, to identify its genetic basis and to monitor the geographical distribution of resistant genotypes, with a particular focus on sites experiencing the 2017 chikungunya outbreak in Italy. Bioassays, performed according to World Health Organization protocols, showed full susceptibility to deltamethrin (concentration = 0.05%) and varying levels of resistance to permethrin (0.75%) and/or α-cypermethrin (0.05%) across Italy, with highest levels in the core of the 2017 chikungunya outbreak. Partial genotyping of the VSSC gene revealed widespread distribution of V1016G mutation and confirmed its association with pyrethroid resistance. The results obtained show that the condition for the spread of pyrethroid resistance in Ae. albopictus in Europe exists under strong selective pressure due to intensive insecticide spraying to control exotic arbovirus outbreak or high levels of nuisance. The results draw attention to the need for an evidence-based implementation of mosquito nuisance control, taking insecticide resistance management into consideration. © 2019 Society of Chemical Industry.
Sections du résumé
BACKGROUND
BACKGROUND
The highly invasive mosquito species Aedes albopictus has become a major health concern in temperate areas due to its role as vector of exotic arboviruses. Pyrethroid insecticides represent the main tools for limiting the circulation of such mosquito-borne viruses. The present work aim to extend previous reports on phenotypic pyrethroid-resistance in European Ae. albopictus, to identify its genetic basis and to monitor the geographical distribution of resistant genotypes, with a particular focus on sites experiencing the 2017 chikungunya outbreak in Italy.
RESULTS
RESULTS
Bioassays, performed according to World Health Organization protocols, showed full susceptibility to deltamethrin (concentration = 0.05%) and varying levels of resistance to permethrin (0.75%) and/or α-cypermethrin (0.05%) across Italy, with highest levels in the core of the 2017 chikungunya outbreak. Partial genotyping of the VSSC gene revealed widespread distribution of V1016G mutation and confirmed its association with pyrethroid resistance.
CONCLUSION
CONCLUSIONS
The results obtained show that the condition for the spread of pyrethroid resistance in Ae. albopictus in Europe exists under strong selective pressure due to intensive insecticide spraying to control exotic arbovirus outbreak or high levels of nuisance. The results draw attention to the need for an evidence-based implementation of mosquito nuisance control, taking insecticide resistance management into consideration. © 2019 Society of Chemical Industry.
Substances chimiques
Nitriles
0
Pyrethrins
0
cypermethrin
1TR49121NP
decamethrin
2JTS8R821G
Permethrin
509F88P9SZ
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
2642-2651Informations de copyright
© 2019 Society of Chemical Industry.
Références
WHO, A Global Brief on Vector-Borne Diseases, WHO Press, Geneva 27, Switzerland pp. 1-56 (2014).
Goubert C, Minard G, Vieira C and Boulesteix M, Population genetics of the Asian tiger mosquito Aedes albopictus, an invasive vector of human diseases. Heredity (Edinb) 117:125-134 (2016).
Kraemer MUG, Sinka ME, Duda KA, Mylne A, Shearer FM, Barker CM et al., The global distribution of the arbovirus vectors Aedes aegypti and Ae. albopictus. Elife 4:e08347 (2015).
Medlock JM, Hansford KM, Schaffner F, Versteirt V, Hendrickx G, Zeller H et al., A review of the invasive mosquitoes in Europe: ecology, public health risks, and control options. Vector Borne Zoonotic Dis 12:435-447 (2012).
Medlock JM, Hansford KM, Versteirt V, Cull B, Kampen H, Fontenille D et al., An entomological review of invasive mosquitoes in Europe. Bull Entomol Res 105:1-27 (2015).
Benedict MQ, Levine RS, Hawley WA and Lounibos LP, Spread of the tiger: global risk of invasion by the mosquito Aedes albopictus. Vector Borne Zoonotic Dis 7:76-85 (2007).
Schaffner F, Medlock JM and Van Bortel W, Public health significance of invasive mosquitoes in Europe. Clin Microbiol Infect 19:685-692 (2013).
Succo T, Leparc-Goffart I, Ferré J, Roiz D, Broche B, Maquart M et al., Autochthonous dengue outbreak in Nimes, South of France, July to September 2015. Eurosurveillance 21:1-7 (2016).
Gjenero-Margan I, Aleraj B, Krajcar D, Lesnikar V, Klobučar A, Pem-Novosel I et al., Autochthonous dengue fever in Croatia, August-September 2010. Eurosurveillance 16:19805 (2011).
Angelini R, Finarelli AC, Angelini P, Po C, Petropulacos K, Macini P et al., Chikungunya in north-eastern Italy: a summing up of the outbreak. Eurosurveillance Euro Surveill. 2007 Nov 22;12:E071122.2.
Rezza G, Nicoletti L, Angelini R, Romi R, Finarelli A, Panning M et al., Infection with chikungunya virus in Italy: an outbreak in a temperate region. Lancet 370:1840-1846 (2007).
ECDC, Clusters of Autochthonous Chikungunya Cases in Italy. European Centre for Disease Prevention and Control. Rapid Risk Assessment [Online] (2017). Available: https://ecdc.europa.eu/sites/portal/files/documents/RRA-chikungunya-Italy-update-9-Oct-2017.pdf [accessed 9 October 2017].
Venturi G, Di Luca M, Fortuna C, Remoli ME, Riccardo F, Severini F et al., Detection of a chikungunya outbreak in Central Italy, August to September 2017. Euro Surveill 22:17-00646 (2017).
Moyes CL, Vontas J, Martins AJ, Ng LC, Koou SY, Dusfour I et al., Contemporary status of insecticide resistance in the major Aedes vectors of arboviruses infecting humans. PLoS Negl Trop Dis 7:e0005625 (2017).
Ranson H, N'Guessan R, Lines J, Moiroux N, Nkuni Z, Corbel V. Pyrethroid resistance in African anopheline mosquitoes: what are the implications for malaria control? Trends Parasitol 2011;27(2):91-98.
Ranson H and Lissenden N, Insecticide resistance in African Anopheles mosquitoes: a worsening situation that needs urgent action to maintain malaria control. Trends Parasitol 32:187-196 (2016).
World Health Organization. Control of Communicable Diseases. (1998). Test procedures for insecticide resistance monitoring in malaria vectors, bio-efficacy and persistence of insecticides on treated surfaces : report of the WHO informal consultation, Geneva, 28-30 September 1998. Geneva : World Health Organization. (2018). http://www.who.int/iris/handle/10665/64879.
WHO. Global Plan for Insecticide Resistance Management in Malaria Vectors. 2012. Geneva, Switzerland, 15 May 2012 WHO Global Malaria Programme.
World Health Organization. (2016). Test procedures for insecticide resistance monitoring in malaria vector mosquitoes, 2nd ed.. World Health Organization. http://www.who.int/iris/handle/10665/250677.
EU Directive 528/2012. Biocidal Products Regulation 528/2012. Regulation (EU) No 528/2012 of the European Parliament and of the Council of 22 May 2012 concerning the making available on the market and use of biocidal products Text with EEA relevance. ELI: http://data.europa.eu/eli/reg/2012/528/oj.
EU Directive 98/8. Biocidal Products Directive 98/8. Directive 98/8/EC of the European Parliament and of the Council of 16 February 1998 concerning the placing of biocidal products on the market. ELI: http://data.europa.eu/eli/dir/1998/8/oj.
WHO-EMCA. Guidelines for the Control of Mosquitoes of Public Health Importance in Europe. European Mosquito Control Association (EMCA) in collaboration the Word Health Organization Copenhagen 2013.
Ranson H, Burhani J, Lumjuan N and Iv WCB, Insecticide resistance in dengue vectors. TropIKA.net 1:1-12 (2010).
Vontas J, Kioulos E, Pavlidi N, Morou E, della Torre A and Ranson H, Insecticide resistance in the major dengue vectors Aedes albopictus and Aedes aegypti. Pestic Biochem Physiol 104:126-131 (2012).
Chuaycharoensuk T, Juntarajumnong W, Boonyuan W, Bangs MJ, Akratanakul P, Thammapalo S et al., Frequency of pyrethroid resistance in Aedes aegypti and Aedes albopictus (Diptera: Culicidae) in Thailand. J Vector Ecol 36:204-212 (2011).
Ishak IH, Jaal Z, Ranson H and Wondji CS, Contrasting patterns of insecticide resistance and knockdown resistance (kdr) in the dengue vectors Aedes aegypti and Aedes albopictus from Malaysia. Parasit Vectors 8:181 (2015).
Lee RML, Choong CTH, Goh BPL, Ng LC and Lam-Phua SG, Bioassay and biochemical studies of the status of pirimiphos-methyl and cypermethrin resistance in Aedes (Stegomyia) aegypti and Aedes (Stegomyia) albopictus (Diptera: Culicidae) in Singapore. Trop Biomed 31:670-679 (2014).
Thanispong K, Sathantriphop S, Malaithong N, Bangs MJ and Chareonviriyaphap T, Establishment of diagnostic doses of five pyrethroids for monitoring physiological resistance in Aedes albopictus in Thailand. J Am Mosq Control Assoc 31:346-352 (2015).
Arslan A, Rathor HR, Mukhtar MU, Mushtaq S, Bhatti A, Asif M, et al. Spatial distribution and insecticide susceptibility status of Aedes aegypti and Aedes albopictus in dengue affected urban areas of Rawalpindi, Pakistan. J Vector Borne Dis 2016;53:136-143.
Kushwah RBS, Mallick PK, Ravikumar H, Dev V, Kapoor N, Adak T et al., Status of DDT and pyrethroid resistance in Indian Aedes albopictus and absence of knockdown resistance (kdr) mutation. J Vector Borne Dis 52:95-98 (2015).
Sivan A, Shriram AN, Sunish IP and Vidhya PT, Studies on insecticide susceptibility of Aedes aegypti (Linn) and Aedes albopictus (Skuse) vectors of dengue and chikungunya in Andaman and Nicobar Islands, India. Parasitol Res 114:4693-4702 (2015).
Kamgang B, Marcombe S, Chandre F, Nchoutpouen E, Nwane P, Etang J et al., Insecticide susceptibility of Aedes aegypti and Aedes albopictus in Central Africa. Parasit Vectors 4:79 (2011).
Ngoagouni C, Kamgang B, Brengues C, Yahouedo G, Paupy C, Nakouné E et al., Susceptibility profile and metabolic mechanisms involved in Aedes aegypti and Aedes albopictus resistant to DDT and deltamethrin in the Central African Republic. Parasit Vectors 9:599 (2016).
Kamgang B, Yougang AP, Tchoupo M, Riveron JM and Wondji C, Temporal distribution and insecticide resistance profile of two major arbovirus vectors Aedes aegypti and Aedes albopictus in Yaoundé, the capital city of Cameroon. Parasit Vectors 10:469 (2017).
Romi R, Toma L, Severini F and Di Luca M, Susceptibility of Italian populations of Aedes albopictus to temephos and to other insecticides. J Am Mosq Control Assoc 19:419-423 (2003).
Suter T, Crespo MM, De Oliveira MF, De Oliveira TSA, De Melo-Santos MAV, De Oliveira CMF et al., Insecticide susceptibility of Aedes albopictus and Ae. aegypti from Brazil and the Swiss-Italian border region. Parasit Vectors 10:1-11 (2017).
Bengoa M, Eritja R, Delacour S, Miranda MÁ, Sureda A and Lucientes J, First data on resistance to pyrethroids in wild populations of Aedes albopictus from Spain. J Am Mosq Control Assoc 33:246-249 (2017).
Pichler V, Bellini R, Veronesi R, Arnoldi D, Rizzoli A, Lia RP, et al. First evidence of resistance to pyrethroid insecticides in Italian Aedes albopictus populations 26 years after invasion. Pest Manag Sci 2018;74(6):1319-1327.
Richards SL, Balanay JAG, Fields M, Vandock K and Eisen L, Baseline insecticide susceptibility screening against six active ingredients for Culex and Aedes (Diptera: Culicidae) Mosquitoes in the United States. J Med Entomol 54:682-695 (2017).
Richards SL, Anne J, Balanay G, White AV, Hope J, Vandock K et al., Insecticide susceptibility screening against Culex and Aedes (Diptera: Culicidae) mosquitoes from the United States. J Med Entomol 55:398-407 (2018).
Kasai S, Komagata O, Itokawa K, Shono T, Ng LC, Kobayashi M et al., Mechanisms of pyrethroid resistance in the dengue mosquito vector, Aedes aegypti: target site insensitivity, penetration, and metabolism. PLoS Negl Trop Dis 8:e2948 (2014).
Ishak IH, Kamgang B, Ibrahim SS, Riveron JM, Irving H and Wondji CS, Pyrethroid resistance in Malaysian populations of dengue vector Aedes aegypti is mediated by CYP9 family of cytochrome P450 genes. PLoS Negl Trop Dis 11:e0005302 (2017).
Ishak IH, Riveron JM, Ibrahim SS, Stott R, Longbottom J, Helen I et al., The cytochrome P450 gene CYP6P12 confers pyrethroid resistance in kdr-free Malaysian populations of the dengue vector Aedes albopictus. Sci Rep 6:1-13 (2016).
Soderlund DM, Molecular mechanisms of pyrethroid insecticide neurotoxicity: recent advances. Arch Toxicol 86:165-181 (2012).
Hemingway J, Hawkes NJ, McCarroll L and Ranson H, The molecular basis of insecticide resistance in mosquitoes. Insect Biochem Mol Biol 34:653-665 (2004).
Hemingway J and Ranson H, Insecticide resistance in insect vectors of human disease. Annu Rev Entomol 45:371-391 (2000).
Smith LB, Kasai S and Scott JG, Pyrethroid resistance in Aedes aegypti and Aedes albopictus: important mosquito vectors of human diseases. Pestic Biochem Physiol 133:1-12 (2016).
Auteri M, La Russa F, Blanda V and Torina A, Insecticide resistance associated with kdr mutations in Aedes albopictus : an update on worldwide evidences. Biomed Res Int 2018:3098575 (2018).
Kasai S, Ng LC, Lam-phua SG and Tang CS, First detection of a putative knockdown resistance gene in major mosquito vector, Aedes albopictus. Jpn J Infect Dis 64:217-221 (2011).
Chen H, Li K, Wang X, Yang X, Lin Y, Cai F, et al. First identification of kdr allele F1534S in VGSC gene and its association with resistance to pyrethroid insecticides in Aedes albopictus populations from Haikou City, Hainan Island, China. Infect Dis Poverty 2016;5(31).
Xu J, Bonizzoni M, Zhong D, Zhou G, Cai S, Yan G et al., Multi-country survey revealed prevalent and novel F1534S mutation in voltage-gated sodium channel (VGSC) gene in Aedes albopictus. PLoS Negl Trop Dis 10:e0004696 (2016).
Aguirre-Obando OA, Martins AJ and Navarro-Silva MA, First report of the Phe1534Cys kdr mutation in natural populations of Aedes albopictus from Brazil. Parasit Vectors 10:160 (2017).
Marcombe S, Farajollahi A, Healy SP, Clark GG and Fonseca DM, Insecticide resistance status of United States populations of Aedes albopictus and mechanisms involved. PLoS One 9:e101992 (2014).
ECDC. Guidelines for the Surveillance of Invasive Mosquitoes in Europe. 2012. European Centre for Disease Prevention and Control. Stockholm.
Ministero della Salute. Piano Nazionale di sorveglianza e risposta alle arbovirosi trasmesse da zanzare invasive (Aedes sp.) con particolare riferimento ai virus Chikungunya, Dengue e Zika. 2018. Circolare 18 maggio 2018 Ministero della Salute, Italia.
WHO, Monitoring and Managing Insecticide Resistance in Aedes Mosquito Populations. Interim Guidance for Entomologists (2016). Available: http://apps.who.int/iris/bitstream/10665/204588/2/WHO_ZIKV_VC_16.1_eng.pdf.WHO/ZIKV/VC/16.12016-03-08T09:10:47Z.
Corbel V, Fonseca DM, Weetman D, Pinto J, Achee NL, Chandre F, et al. International workshop on insecticide resistance in vectors of arboviruses, December 2016, Rio de Janeiro, Brazil. Parasit Vectors 2017;10(1):278.
Corbel V, Dusfour I, David J, Corbel V, Achee NL, Chandre F et al., Tracking insecticide resistance in mosquito vectors of arboviruses: the worldwide insecticide resistance network (WIN). PLoS Negl Trop Dis 10:e0005054 (2016).
Farajollahi A, Healy SP, Unlu I, Gaugler R and Fonseca DM, Effectiveness of ultra-low volume nighttime applications of an adulticide against diurnal Aedes albopictus, a critical vector of dengue and chikungunya viruses. PLoS One 7:e49181 (2012).
Fonseca DM, Unlu I, Crepeau T, Farajollahi A, Healy SP, Bartlett-Healy K, et al. Area-wide management of Aedes albopictus. Part 2: Gauging the efficacy of traditional integrated pest control measures against urban container mosquitoes. Pest Manag Sci 2013;69(12):1351-1361.
Manica M, Cobre P, Rosà R and Caputo B, Not in my backyard: effectiveness of outdoor residual spraying from hand-held sprayers against the mosquito Aedes albopictus in Rome, Italy. Pest Manag Sci 73:138-145 (2017).
Caputo B, Manica M, D'Alessandro A, Bottà G, Filipponi F, Protano C et al., Assessment of the effectiveness of a seasonal-long insecticide-based control strategy against Aedes albopictus nuisance in an urban area. PLoS Negl Trop Dis 10:e0004463 (2016).
Ministero della Salute. Piano nazionale integrato di sorveglianza e risposta ai virus West Nile e Usutu. 27 giugno 2018 Ministero della Salute Italia.
Velo E, Kadriaj P, Mersini K, Shukullari A, Manxhari B, Simaku A, et al. Enhancement of Aedes albopictus collections by ovitrap and sticky adult trap. Parasit Vectors 2016;9(1):1-5.
Severini F, Toma L, Luca D and Romi R, Le zanzare italiane: Generalità e identificazione degli adulti (Diptera, Culicidae). Fragm Entomol 41:213-372 (2009).
Wan-norafikah O, Ahmad W, Lim H and Zainol-ariffin P, Susceptibility of Aedes albopictus Skuse (Diptera: Culicidae) to permethrin in Kuala Lumpur, Malaysia. Asian Biomed 7:51-62 (2013).
Pocquet N, Darriet F, Zumbo B, Milesi P, Thiria J, Bernard V, et al. Insecticide resistance in disease vectors from Mayotte: an opportunity for integrated vector management. Parasit Vectors 2014;7:299.
R Development Core Team, R: A Language and Environment for Statistical Computing, ed. by R Foundation for Statistical Computing. R Foundation for Statistical Computing, (2011). p. 409. (R Foundation for Statistical Computing; vol. 1) [Online]. Available: http://www.r-project.org.
Giraldo-Calderón GI, Emrich SJ, MacCallum RM, Maslen G, Dialynas E, Topalis P, et al. VectorBase: an updated bioinformatics resource for invertebrate vectors and other organisms related with human diseases. Nucleic Acids Research 43(Database issue):D707-13 (2015).
Veronesi R, Gentile G, Carrieri M, Maccagnani B, Stermieri L and Bellini R, Seasonal pattern of daily activity of Aedes caspius, Aedes detritus, Culex modestus, and Culex pipiens in the Po Delta of northern Italy and significance for vector-borne disease risk assessment. J Vector Ecol 37:49-61 (2012). doi: 10.1111/j.1948-7134.2012.00199.x.
Srisawat R, Komalamisra N, Eshita Y, Zheng M, Ono K, Itoh TQ, et al. Point mutations in domain II of the voltage-gated sodium channel gene in deltamethrin-resistant Aedes aegypti (Diptera: Culicidae). Appl Entomol Zool 2010;45(2):275-282.
Hirata K, Komagata O, Itokawa K, Yamamoto A, Tomita T and Kasai S, A single crossing-over event in voltage-sensitive Na+channel genes may cause critical failure of dengue mosquito control by insecticides. PLoS Negl Trop Dis 8:e3085 (2014).
Dusfour I, Zorrilla P, Guidez A, Issaly J, Girod R, Guillaumot L et al., Deltamethrin resistance mechanisms in Aedes aegypti populations from three French overseas territories worldwide. PLoS Negl Trop Dis 9:1-17 (2015).
Italian Ministery of Health, Istituto Superiore della Sanità, Italy: Autochtonous Cases of Chikungunya Virus [Online] (updated 21 December 2017). (2017). Available: http://www.salute.gov.it/portale/temi/documenti/chikungunya/bollettino_chikungunya_ULTIMO.pdf 27 dicembre 2017.
WHO. Handbook for Integrated Vector Management. 2012. World Health Organization. (2012). Handbook for integrated vector management. Geneva : World Health Organization. http://www.who.int/iris/handle/10665/44768 World Health Organization Avenue Appia 20, 1211 Geneva 27, Switzerland.
Stenhouse SA, Plernsub S, Yanola J, Lumjuan N and Dantrakool A, Detection of the V1016G mutation in the voltage-gated sodium channel gene of Aedes aegypti (Diptera: Culicidae) by allele-specific PCR assay , and its distribution and effect on deltamethrin resistance in Thailand. Parasit Vectors 6:1 (2013).