Back to the future: the sterile insect technique against mosquito disease vectors.

With the global burden of mosquito-borne diseases increasing, and some conventional vector control tools losing effectiveness, the sterile insect technique (SIT) is a potential new tool in the arsenal. Equipment and protocols have been developed and validated for efficient mass-rearing, irradiation and release of Aedines and Anophelines that could be useful for several control approaches. Assessment of male quality is becoming more sophisticated, and several groups are well advanced in pilot site selection and population surveillance. It will not be long before SIT feasibility has been evaluated in various settings. Until perfect sexing mechanisms exist, combination of Wolbachia-induced phenotypes, such as cytoplasmic incompatibility and pathogen interference, and irradiation may prove to be the safest solution for population suppression.

[1]  H. Bossin,et al.  Harnessing mosquito-Wolbachia symbiosis for vector and disease control. , 2014, Acta tropica.

[2]  R. Bellini,et al.  Mass Production Cage for Aedes albopictus (Diptera: Culicidae) , 2014, Journal of medical entomology.

[3]  H. Bossin,et al.  Open Release of Male Mosquitoes Infected with a Wolbachia Biopesticide: Field Performance and Infection Containment , 2012, PLoS neglected tropical diseases.

[4]  S. Dobson,et al.  Wolbachia strain wPip yields a pattern of cytoplasmic incompatibility enhancing a Wolbachia-based suppression strategy against the disease vector Aedes albopictus , 2012, Parasites & Vectors.

[5]  Dong-Jing Zhang,et al.  Standard operating procedures for standardized mass rearing of the dengue and chikungunya vectors Aedes aegypti and Aedes albopictus (Diptera: Culicidae) - II - Egg storage and hatching , 2015, Parasites & Vectors.

[6]  L. Alphey,et al.  Mass Production of Genetically Modified Aedes aegypti for Field Releases in Brazil , 2014, Journal of visualized experiments : JoVE.

[7]  R. Bellini,et al.  γ Ray Dosimetry and Mating Capacity Studies in the Laboratory on Aedes albopictus Males , 2010, Journal of medical entomology.

[8]  O. Duron,et al.  Cytoplasmic Incompatibility as a Means of Controlling Culex pipiens quinquefasciatus Mosquito in the Islands of the South-Western Indian Ocean , 2011, PLoS neglected tropical diseases.

[9]  D. Damiens,et al.  Standard operating procedures for standardized mass rearing of the dengue and chikungunya vectors Aedes aegypti and Aedes albopictus (Diptera: Culicidae) - I - egg quantification , 2015, Parasites & Vectors.

[10]  A. Mathis,et al.  Dengue and dengue vectors in the WHO European region: past, present, and scenarios for the future. , 2014, The Lancet. Infectious diseases.

[11]  D. Damiens,et al.  X-ray sterilization of the An. arabiensis genetic sexing strain 'ANO IPCL1' at pupal and adult stages. , 2014, Acta tropica.

[12]  H. Laven.  A possible model for speciation by cytoplasmic isolation in the Culex pipiens complex. , 1967, Bulletin of the World Health Organization.

[13]  Guoli Zhou,et al.  Wolbachia Invades Anopheles stephensi Populations and Induces Refractoriness to Plasmodium Infection , 2013, Science.

[14]  A. Zeb,et al.  Development of inexpensive and globally available larval diet for rearing Anopheles stephensi (Diptera: Culicidae) mosquitoes , 2013, Parasites & Vectors.

[15]  S. Ritchie,et al.  Dynamics of the “Popcorn” Wolbachia Infection in Outbred Aedes aegypti Informs Prospects for Mosquito Vector Control , 2011, Genetics.

[16]  A. Farajollahi,et al.  Climate Change and Range Expansion of the Asian Tiger Mosquito (Aedes albopictus) in Northeastern USA: Implications for Public Health Practitioners , 2013, PloS one.

[17]  R. Lees,et al.  Guidelines to site selection for population surveillance and mosquito control trials: a case study from Mauritius. , 2014, Acta tropica.

[18]  Peter A. Ryan,et al.  A Wolbachia Symbiont in Aedes aegypti Limits Infection with Dengue, Chikungunya, and Plasmodium , 2009, Cell.

[19]  K. Bourtzis,et al.  Wolbachia: more than just a bug in insects genitals. , 2010, Current opinion in microbiology.

[20]  Z. Premji,et al.  Understanding caretakers' dilemma in deciding whether or not to adhere with referral advice after pre-referral treatment with rectal artesunate , 2010, Malaria Journal.

[21]  B. Knols,et al.  Field site selection: getting it right first time around , 2009, Malaria Journal.

[22]  M. Benedict,et al.  An Inexpensive and Effective Larval Diet for Anopheles arabiensis (Diptera: Culicidae): Eat Like a Horse, a Bird, or a Fish? , 2012, Journal of medical entomology.

[23]  Guofa Zhou,et al.  Urbanization Increases Aedes albopictus Larval Habitats and Accelerates Mosquito Development and Survivorship , 2014, PLoS neglected tropical diseases.

[24]  R. Lees,et al.  Aedes albopictus (Skuse) males in laboratory and semi-field cages: release ratios and mating competitiveness. , 2014, Acta tropica.

[25]  L. Alphey,et al.  Genetic control of mosquitoes , 2016 .

[26]  G. Lempérière,et al.  Evidence of Multiple Inseminations in the Field in Aedes albopictus , 2012, PloS one.

[27]  D. Damiens,et al.  Different Blood and Sugar Feeding Regimes Affect the Productivity of Anopheles arabiensis Colonies (Diptera: Culicidae) , 2013, Journal of medical entomology.

[28]  B. Knols,et al.  Radiation-induced sterility for pupal and adult stages of the malaria mosquito Anopheles arabiensis , 2006, Malaria Journal.

[29]  A. James,et al.  The invasive mosquito species Aedes albopictus: current knowledge and future perspectives. , 2013, Trends in parasitology.

[30]  S. Ritchie,et al.  Ability for Aedes albopictus (Diptera: Culicidae) to Survive at the Climatic Limits of Its Potential Range in Eastern Australia , 2014, Journal of medical entomology.

[31]  R. Bellini,et al.  Validation of a New Larval Rearing Unit for Aedes albopictus (Diptera: Culicidae) Mass Rearing , 2014, PloS one.

[32]  E. McGraw,et al.  Beyond insecticides: new thinking on an ancient problem , 2013, Nature Reviews Microbiology.

[33]  Maurizio Calvitti,et al.  Use of the sterile insect technique against Aedes albopictus in Italy: First results of a pilot trial , 2007 .

[34]  C. Curtis,et al.  History of the Sterile Insect Technique , 2021, Sterile Insect Technique.

[35]  R. Moretti,et al.  Wolbachia Density and Cytoplasmic Incompatibility in Aedes albopictus: Concerns with Using Artificial Wolbachia Infection as a Vector Suppression Tool , 2015, PloS one.

[36]  H. Ranson,et al.  Insecticide resistance in dengue vectors , 2010 .

[37]  M. Bonsall,et al.  Modeling resistance to genetic control of insects. , 2011, Journal of theoretical biology.

[38]  R. Hunt,et al.  Field study site selection, species abundance and monthly distribution of anopheline mosquitoes in the northern Kruger National Park, South Africa , 2014, Malaria Journal.

[39]  A. James,et al.  Criteria for identifying and evaluating candidate sites for open-field trials of genetically engineered mosquitoes. , 2014, Vector borne and zoonotic diseases.

[40]  A. Robinson,et al.  Insect pest control using Wolbachia and/or radiation , 2006 .

[41]  M. Capurro,et al.  Towards mosquito sterile insect technique programmes: exploring genetic, molecular, mechanical and behavioural methods of sex separation in mosquitoes. , 2014, Acta tropica.

[42]  Ben L. Phillips,et al.  Stability of the wMel Wolbachia Infection following Invasion into Aedes aegypti Populations , 2014, PLoS neglected tropical diseases.

[43]  S. Halstead,et al.  Approaches to Refining Estimates of Global Burden and Economics of Dengue , 2014, PLoS neglected tropical diseases.

[44]  K. Bourtzis,et al.  Combining the Sterile Insect Technique with the Incompatible Insect Technique: I-Impact of Wolbachia Infection on the Fitness of Triple- and Double-Infected Strains of Aedes albopictus , 2015, PloS one.

[45]  M. Benedict,et al.  A New Larval Tray and Rack System for Improved Mosquito Mass Rearing , 2012, Journal of medical entomology.

[46]  Participation of irradiated Anopheles arabiensis males in swarms following field release in Sudan , 2014, Malaria Journal.

[47]  Controlled human malaria infection in Kenyan adults: A safe model that could accelerate assessment of novel drugs and vaccines in malaria endemic populations , 2014, Malaria Journal.

[48]  Mosquito Mass Rearing Technology: A Cold-Water Vortex Device for Continuous Unattended Separation of Anopheles arabiensis Pupae from Larvae , 2011, Journal of the American Mosquito Control Association.

[49]  F. Simard,et al.  Effect of three larval diets on larval development and male sexual performance of Anopheles gambiae s.s. , 2014, Acta tropica.

[50]  L. Alphey,et al.  Mosquito transgenesis: what is the fitness cost? , 2006, Trends in parasitology.

[51]  C. Rogier,et al.  The changes in mosquito vector behaviour and the emerging resistance to insecticides will challenge the decline of malaria. , 2013, Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases.

[52]  S. Dobson,et al.  Interspecific Hybridization Yields Strategy for South Pacific Filariasis Vector Elimination , 2008, PLoS neglected tropical diseases.

[53]  R. Paine.  The Introduction of Megarhinus Mosquitos into Fiji , 1934, Bulletin of Entomological Research.

[54]  R. Bellini,et al.  Efficiency of Three Diets for Larval Development in Mass Rearing Aedes albopictus (Diptera: Culicidae) , 2013, Journal of medical entomology.

[55]  H. Zeller,et al.  An entomological review of invasive mosquitoes in Europe , 2015, Bulletin of Entomological Research.

[56]  R. Bellini,et al.  Mating Competitiveness of Aedes albopictus Radio-Sterilized Males in Large Enclosures Exposed to Natural Conditions , 2013, Journal of medical entomology.

[57]  Jonathan Cox,et al.  Spatial and temporal distribution of the malaria mosquito Anopheles arabiensis in northern Sudan: influence of environmental factors and implications for vector control , 2009, Malaria Journal.

[58]  D. Focks,et al.  An improved separator for the developmental stages, sexes, and species of mosquitoes (Diptera: Culicidae). , 1980, Journal of medical entomology.

[59]  C. Oliva,et al.  X-Ray-Induced Sterility in Aedes albopictus (Diptera: Culicidae) and Male Longevity Following Irradiation , 2014, Journal of medical entomology.

[60]  N. Segata,et al.  Evidence of natural Wolbachia infections in field populations of Anopheles gambiae , 2014, Nature Communications.

[61]  A. Parker,et al.  Sterile Insect Quality , 2005 .

[62]  R. Bellini,et al.  Pilot Field Trials with Aedes albopictus Irradiated Sterile Males in Italian Urban Areas , 2013, Journal of medical entomology.

[63]  L. Singh,et al.  Effect of Gamma Radiation on Survival and Fertility of Male Anopheles stephensi Liston, Irradiated as Pharate Adults , 2010 .

[64]  G. Clark,et al.  Insecticide Resistance Status of United States Populations of Aedes albopictus and Mechanisms Involved , 2014, PloS one.

[65]  L. Gouagna,et al.  Wolbachia-Based Population Control Strategy Targeting Culex quinquefasciatus Mosquitoes Proves Efficient under Semi-Field Conditions , 2015, PloS one.

[66]  D. Chadee,et al.  Eliminating female Anopheles arabiensis by spiking blood meals with toxicants as a sex separation method in the context of the sterile insect technique , 2013, Parasites & Vectors.