| Particle and Fibre Toxicology | |
| Pyriproxyfen for mosquito control: female sterilization or horizontal transfer to oviposition substrates by Anopheles gambiae sensu stricto and Culex quinquefasciatus | |
| Ulrike Fillinger1  Steven W Lindsay2  Oscar Mbare1  | |
| [1] Disease Control Department, London School of Hygiene & Tropical Medicine, WC1E 7HT London, United Kingdom;School of Biological and Biomedical Sciences, Durham University, DH1 3LE Durham, United Kingdom | |
| 关键词: Auto-dissemination; Sterilization; Pyriproxyfen; Insect growth regulator; Vector control; Culex quinquefasciatus; Anopheles gambiae; | |
| Others : 804040 DOI : 10.1186/1756-3305-7-280 |
|
| received in 2014-04-30, accepted in 2014-06-16, 发布年份 2014 | |
PDF
|
|
【 摘 要 】
Background
The use of gravid mosquitoes as vehicles to auto-disseminate larvicides was recently demonstrated for the transfer of pyriproxyfen (PPF) by container-breeding Aedes mosquitoes and presents an appealing idea to explore for other disease vectors. The success of this approach depends on the female’s behaviour, the time of exposure and the amount of PPF that can be carried by an individual. We explore the effect of PPF exposure at seven time points around blood feeding on individual Anopheles gambiae sensu stricto and Culex quinquefasciatus fecundity and ability to transfer in laboratory assays.
Method
Mosquitoes were exposed to 2.6 mg PPF per m2 at 48, 24 and 0.5 hours before and after a blood meal and on the day of egg-laying. The proportion of exposed females (N = 80-100) laying eggs, the number of eggs laid and hatched was studied. Transfer of PPF to oviposition cups was assessed by introducing 10 late instar insectary-reared An. gambiae s.s. larvae into all the cups and monitored for adult emergence inhibition.
Results
Exposure to PPF between 24 hours before and after a blood meal had significant sterilizing effects: females of both species were 6 times less likely (Odds ratio (OR) 0.16, 95% confidence interval (CI) 0.10-0.26) to lay eggs than unexposed females. Of the few eggs laid, the odds of an egg hatching was reduced 17 times (OR 0.06, 95% CI 0.04-0.08) in Anopheles but only 1.2 times (OR 0.82, 95% CI 0.73-0.93) in Culex. Adult emergence inhibition from larvae introduced in the oviposition cups was observed only from cups in which eggs were laid. When females were exposed to PPF close to egg laying they transferred enough PPF to reduce emergence by 65-71% (95% CI 62-74%).
Conclusion
PPF exposure within a day before and after blood feeding affects egg-development in An. gambiae s.s. and Cx. quinquefasciatus and presents a promising opportunity for integrated control of vectors and nuisance mosquitoes. However, sterilized females are unlikely to visit an oviposition site and therefore do not transfer lethal concentrations of PPF to aquatic habitats. This suggests that for successful auto-dissemination the optimum contamination time is close to oviposition.
【 授权许可】
2014 Mbare et al.; licensee BioMed Central Ltd.
【 预 览 】
| Files | Size | Format | View |
|---|---|---|---|
| 20140708052946473.pdf | 424KB | ||
| Figure 2. | 75KB | Image | |
| Figure 1. | 35KB | Image |
【 图 表 】
Figure 1.
Figure 2.
【 参考文献 】
- [1]Soper FL: Paris green in the eradication of Anopheles gambiae: Brazil, 1940; Egypt, 1945. Mosq News 1966, 26:470-476.
- [2]Killeen GF, Fillinger U, Kiche I, Gouagna LC, Knols BG: Eradication of Anopheles gambiae from Brazil: lessons for malaria control in Africa? Lancet Infec Dis 2002, 2:618-627.
- [3]Tusting LS, Thwing J, Sinclair D, Fillinger U, Gimnig J, Bonner KE, Bottomley C, Lindsay SW: Mosquito larval source management for controlling malaria. Cochrane Database Syst Rev 2013, 8:CD008923.
- [4]Walker K, Lynch M: Contributions of Anopheles larval control to malaria suppression in tropical Africa: review of achievements and potential. Med Vet Entomol 2007, 21:2-21.
- [5]White MT, Griffin JT, Churcher TS, Ferguson NM, Basáñez M, Ghani AC: Modelling the impact of vector control interventions on Anopheles gambiae population dynamics. Parasit Vectors 2011, 4:153.
- [6]Fillinger U, Kannady K, William G, Vanek MJ, Dongus S, Nyika D, Geissbuhler Y, Chaki PP, Govella NJ, Mathenge EM, Singer BH, Mshinda H, Lindsay SW, Tanner M, Mtasiwa D, de Castro MC, Killeen GF: A tool box for operational mosquito larval control: preliminary results and early lessons from the Urban Malaria Control Programme in Dar es Salaam, Tanzania. Malar J 2008, 7:20.
- [7]Chaki PP, Govella NJ, Shoo B, Hemed A, Tanner M, Fillinger U, Killeen GF: Achieving high coverage of larval-stage mosquito surveillance: challenges for a community-based mosquito control programme in urban Dar es Salaam, Tanzania. Malar J 2009, 8:311.
- [8]Vanek MJ, Shoo B, Mtasiwa D, Kiama M, Lindsay SW, Fillinger U, Kannady K, Tanner M, Killeen GF: Community-based surveillance of malaria vector larval habitats: a baseline study in urban Dar es Salaam, Tanzania. BMC Public Health 2006, 6:154.
- [9]Devine GJ, Killeen GJ: The potential of a new larviciding method for the control of malaria vectors. Malar J 2010, 9:142.
- [10]Fillinger U, Lindsay SW: Larval source management for malaria control in Africa: myths and reality. Malar J 2011, 10:353.
- [11]Caputo B, Lenco A, Cianci D, Pombi M, Petrarca V, Baseggio A, Devine GJ, della Torre A: The “auto-dissemination” approach: a novel concept to fight Aedes albopictus in urban areas. PLoS One 2012, 6:e1793.
- [12]Devine GJ, Perea EZ, Killeen GF, Stancil JD, Clark SJ, Morrison AC: Using adult mosquitoes to transfer insecticides to Aedes aegypti larval habitats. Proc Natl Acad Sci U S A 2009, 106:11530-11534.
- [13]Itoh T, Kawada H, Abe A, Eshita Y, Rongsriyam Y, Igarashi A: Utilization of bloodfed females of Aedes aegypti as a vehicle for the transfer of the insect growth regulator pyriproxyfen to larval habitats. J Am Mosq Control Assoc 1994, 10:344-347.
- [14]Yapabandara AM, Curtis CF: Control of vectors and incidence of malaria in an irrigated settlement scheme in Sri Lanka by using the insect growth regulator pyriproxyfen. J Am Mosq Control Assoc 2004, 20:395-400.
- [15]Sihuincha M, Zamora-Perea E, Orellana-Rios W, Stancil JD, Lopez-Sifuentes V, Vidal-Ore C, Devine GJ: Potential use of pyriproxyfen for control of Aedes aegypti (Diptera: Culicidae) in Iquitos, Peru. J Med Entomol 2005, 42:620-630.
- [16]Mbare O, Lindsay SW, Fillinger U: Dose–response tests and semi-field evaluation of lethal and sub-lethal effects of slow release pyriproxyfen granules (Sumilarv®0.5G) for the control of the malaria vectors Anopheles gambiae sensu lato. Malar J 2013, 12:94.
- [17]Harris C, Lweitoijera DW, Dongus S, Matowo NS, Lorenz LM, Devine GJ, Majambere S: Sterilising effects of pyriproxyfen on Anopheles arabiensis and its potential use in malaria control. Parasit Vectors 2013, 6:144.
- [18]Mulligan FS III, Schaefer CH: Efficacy of a juvenile hormone mimic, pyriproxyfen (S-31183) for mosquito control in dairy waste water lagoons. J Am Mosq Control Assoc 1990, 6:89-92.
- [19]Yapabandara AM, Curtis CF, Wickramasinghe MB, Fernando WP: Control of malaria vectors with the insect growth regulator pyriproxyfen in a gem-mining area in Sri Lanka. Acta Trop 2001, 80:265-276.
- [20]World Health Organization: Guidelines for drinking water quality. [http://www.who.int/water_sanitation_health/dwq/chemicals/Pyriproxyfensum.pdf webcite]
- [21]Yapabandara AM, Curtis CF: Laboratory and field comparisons of pyriproxyfen, polystyrene beads and other larvicidal methods against malaria vectors in Sri Lanka. Acta Trop 2002, 81:211-223.
- [22]Vythilingam I, Luz BM, Hanni R, Beng TS, Huat TC: Laboratory and field evaluation of the insect growth regulator pyriproxyfen (Sumilarv 0.5G) against dengue vectors. J Am Mosq Control Assoc 2005, 21:296-300.
- [23]Chavasse DC, Lines JD, Ichimori K, Majala AR, Minjas JN, Marijani J: Mosquito control in Dar es Salaam. II. Impact of expanded polystyrene beads and pyriproxyfen treatment of breeding sites on Culex quinquefasciatus densities. Med Vet Entomol 1995, 9:147-154.
- [24]Kamal HA, Khater EIM: The biological effects of the insect growth regulators; pyriproxyfen and diflubenzuron on the mosquito Aedes aegypti. J Egypt Soc Parasitol 2010, 40:565-574.
- [25]Loh PY, Yap HH: Laboratory studies on the efficacy and sublethal effects of an insect growth regulator, pyriproxyfen (S-31183) against Aedes aegypti (Linnaeus). Trop Biomed 1989, 6:7-12.
- [26]Dell Chism B, Apperson CS: Horizontal transfer of the insect growth regulator pyriproxyfen to larval microcosms by gravid Aedes albopictus and Ochlerotatus triseriatus mosquitoes in the laboratory. Med Vet Entomol 2003, 17:211-220.
- [27]Itoh T: Utilization of blood fed females of Aedes aegypti as a vehicle for the transfer of the insect growth regulator, pyriproxyfen, to larval habitats. J Am Mosq Control Assoc 1994, 10:344-347.
- [28]Ohba SY, Ohashi K, Pujiyati E, Higa Y, Kawada H, Mito N, Takagi M: The effect of pyriproxyfen as a “population growth regulator” against Aedes albopictus under semi-field conditions. PLoS One 2013, 8:e67045.
- [29]Lounibos LP, Lima DC, Lourenco-de-Oliveira R, Escher RL, Nishimura N: Egg maturation in neotropical malaria vectors: one blood meal is usually enough. J Vector Ecol 1998, 23:195-201.
- [30]Aiku AO, Yates A, Rowland M: Laboratory evaluation of pyriproxifen treated bednets on mosquito fertility and fecundity. A preliminary study. West Afr J Med 2006, 25:22-26.
- [31]Miller JE: Can pyriproxifen (an insect growth regulator) be used to prevent selection of permethrin resistance by impregnated bednets? Trans R Soc Trop Med Hyg 1993, 18:281.
- [32]Ohashi K, Nakada K, Miyaguchi J, Shono Y, Lucas JR, Mito N: Efficacy of pyriproxyfen-treated nets in sterilizing and shortening the longevity of Anopheles gambiae (Diptera: Culicidae). J Med Entomol 2012, 49:1052-1058.
- [33]Ngufor C, N’Guessan R, Fagbohoun J, Odjo A, Malone D, Akogbeto M, Rowland M: Olyset Duo(R) (a pyriproxyfen and permethrin mixture net): an experimental hut trial against pyrethroid resistant Anopheles gambiae and Culex quinquefasciatus in Southern Benin. PLoS One 2014, 9:e93603.
- [34]Ramaiah KD, Pani SP, Balakrishnan N, Sadanandane C, Das LK, Mariappan T, Rajavel AR, Vanamail P, Subramanian S: Prevalence of bancroftian filariasis & its control by single course of diethyl carbamazine in a rural area in Tamil Nadu. Indian J Med Res 1989, 89:184-191.
- [35]Ramaiah KD, Das PK, Dhanda V: Estimation of permissible levels of transmission of bancroftian filariasis based on some entomological and parasitological results of a 5-year vector control programme. Acta Trop 1994, 56:89-96.
- [36]David MR, Ribeiro GS, Freitas RM: Bionomics of Culex quinquefasciatus within urban areas of Rio de Janeiro, Southeastern Brazil. Rev Saude Publica 2012, 46:858-865.
- [37]Dossou-yovo J, Doannio J, Riviere F, Chauvancy G: Urbanization and establishment of Culex quinquefasciatus in a west African rural area. Acta Trop 1995, 59:251-253.
- [38]Mosqueira B, Duchon S, Chandre F, Hougard JM, Carnevale P, Mas-Coma S: Efficacy of an insecticide paint against insecticide-susceptible and resistant mosquitoes - part 1: laboratory evaluation. Malar J 2010, 9:340.
- [39]Mukabana WR, Takken W, Coe R, Knols BG: Host-specific cues cause differential attractiveness of Kenyan men to the African malaria vector Anopheles gambiae. Malar J 2002, 1:17.
- [40]de Jong R, Knols BG: Olfactory responses of host-seeking Anopheles gambiae s.s. Giles (Diptera: Culicidae). Acta Trop 1995, 59:333-335.
- [41]Boreman PFL, Port GR: The distribution and movement of engorged females of Anopheles gambiae Giles (Diptera: Culicidae) in a Gambian village. Bull Ent Res 1982, 72:489-495.
- [42]Smith A, Obudho WO, Esozed S: Resting patterns of Anopheles gambiae in experimental huts treated with malathion. Trans R Soc Trop Med Hyg 1966, 60:401-408.
- [43]Fillinger U, Sonye G, Killeen GF, Knols BG, Becker N: The practical importance of permanent and semipermanent habitats for controlling aquatic stages of Anopheles gambiae sensu lato mosquitoes: operational observations from a rural town in western Kenya. Trop Med Int Health 2004, 9:1274-1289.
- [44]Robert V, Awono-Ambene HP, Thioulouse J: Ecology of larval mosquitoes, with special reference to Anopheles arabiensis (Diptera: Culicidae) in market-garden wells in urban Dakar, Senegal. J Med Entomol 1998, 35:948-955.
- [45]Muturi EJ, Mwangangi J, Shililu J, Jacob BG, Mbogo C, Githure J, Novak RJ: Environmental factors associated with the distribution of Anopheles arabiensis and Culex quinquefasciatus in a rice agro-ecosystem in Mwea, Kenya. J Vector Ecol 2008, 33:56-63.
- [46]Dejenie T, Yohannes M, Assmelash T: Characterization of mosquito breeding sites in and in the vicinity of tigray microdams. Ethiop J Health Sci 2011, 21:57-66.
- [47]Ndenga BA, Simbauni JA, Mbugi JP, Githeko AK: Physical, chemical and biological characteristics in habitats of high and low presence of anopheline larvae in Western Kenya Highlands. PLoS One 2012, 7:e47975.
- [48]Munga S, Minakawa N, Zhou G, Mushinzimana E, Barrack OOJ, Githeko AK, Yan G: Association between land cover and habitat productivity of malaria vectors in Western Kenya highlands. Am J Trop Med Hyg 2006, 74:69-75.
- [49]Mutuku FM, Bayoh NM, Gimnig JE, Vulule JM, Kamau L, Walker ED, Kabiru E, Hawley WA: Pupal habitat productivity of Anopheles gambiae complex mosquitoes in a rural village in Western Kenya. Am J Trop Med Hyg 2006, 74:54-61.
- [50]Araujo MS, Gil LHS, E-Silva AA: Larval food quantity affects development time, survival and adult biological traits that influence the vectorial capacity of Anopheles darlingi under laboratory conditions. Malar J 2012, 11:261.
- [51]Abbott WS: A method of computing the effectiveness of an insecticide. J Am Mosq Control Assoc 1987, 3:302-303.
- [52]Kweka EJ, Zhou G, Beilhe LB, Dixit A, Afrane Y, Gilbreath TM, 3rd Munga S, Nyindo M, Githeko AK, Yan G: Effects of co-habitation between Anopheles gambiae s.s. and Culex quinquefasciatus aquatic stages on life history traits. Parasit Vectors 2012, 5:33.
- [53]Gillies MT, Wilkes TJ: A study of the age-composition of populations of Anopheles gambiae Giles and A. funestus Giles in North-Eastern Tanzania. Bull Entomol Res 1965, 56:237-262.
- [54]Quinones ML, Lines JD, Thomson MC, Jawara M, Morris J, Greenwood BM: Anopheles gambiae gonotrophic cycle duration, biting and exiting behaviour unaffected by permethrin-impregnated bednets in The Gambia. Med Vet Entomol 1997, 11:71-78.
- [55]Begum MN, Ahmed TU, E-Khoda M: Gonotrophic cycle of Culex quinquefasciatus Say (Diptera: Culicidae) in Dhaka. Bangladesh J Zool 1985, 14:111-115.
- [56]Garcia-Rejon JE, Farfan-Ale JA, Ulloa A, Flores-Flores LF, Rosado-Paredes E, Baak-Baak C, Lorono-Pino MA, Fernandez-Salas I, Beaty BJ: Gonotrophic cycle estimate for Culex quinquefasciatus in Merida, Yucatan, Mexico. J Am Mosq Control Assoc 2008, 24:344-348.
- [57]Subra R: Biology and control of Culex pipiens quinquefasciatus Say 1823 (Diptera, Culicidae) with special reference to Africa. Insect Sci Application 1981, 4:319-338.
- [58]McHugh CP: Survivorship and gonotrophic cycle length of Culex tarsalis (Diptera: Culicidae) near Sheridan, Placer County, California. J Med Entomol 1990, 27:1027-1030.
- [59]Gaugler R, Suman D, Wang Y: An autodissemination station for the transfer of an insect growth regulator to mosquito oviposition sites. Med Vet Entomol 2012, 26:37-45.
- [60]Itoh K: Control of DF/DHF vector, Aedes mosquito, with insecticides. Trop Med 1993, 35:259-267.
- [61]Vezzani D: Review: artificial container-breeding mosquitoes and cemeteries: a perfect match. Trop Med Int Health 2007, 12:299-313.
- [62]Bartlett-Healy K, Unlu I, Obenauer P, Hughes T, Healy S, Crepeau T, Farajollahi A, Kesavaraju B, Fonseca D, Schoeler G, Gaugler R, Stickman D: Larval mosquito habitat utilization and community dynamics of Aedes albopictus and Aedes japonicus (Diptera: Culicidae). J Med Entomol 2012, 49:813-824.
- [63]Burkot TR, Handzel T, Schmaedick MA, Tufa J, Roberts JM, Graves PM: Productivity of natural and artificial containers for Aedes polynesiensis and Aedes aegypti in four American Samoan villages. Med Vet Entomol 2007, 21:22-29.
- [64]Chadee DD: The diel oviposition periodicity of Aedes aegypti (L.) (Diptera: Culicidae) in Trinidad, West Indies: effects of forced egg retention. Bull Entemol Res 2010, 100:599-603.
- [65]Colton YM, Chadee DD, Severson DW: Natural skip oviposition of the mosquito Aedes aegypti indicated by codominant genetic markers. Med Vet Entomol 2003, 17:195-204.
- [66]Mackay AJ, Amador M, Barrera R: An improved autocidal gravid ovitrap for the control and surveillance of Aedes aegypti. Parasit Vectors 2013, 6:225.
- [67]Barrera R, Mackay AJ, Amador M: A novel autocidal ovitrap for the surveillance and control of Aedes aegypti. J Am Mosq Control Assoc 2013, 29:293-296.
- [68]Rapley LP, Johnson PH, Williams CR, Silcock RM, Larkman M, Long SA, Russell RC, Ritchie SA: A lethal ovitrap-based mass trapping scheme for dengue control in Australia: II. Impact on populations of the mosquito Aedes aegypti. Med Vet Entomol 2009, 23:303-316.
- [69]Gimnig JE, Ombok M, Kamau L, Hawley WA: Characteristics of larval anopheline (Diptera: Culicidae) habitats in western Kenya. J Med Entomol 2001, 38:282-288.
- [70]Majambere S, Fillinger U, Sayer DR, Green C, Lindsay SW: Spatial distribution of mosquito larvae and the potential for targeted larval control in the Gambia. Am J Trop Med Hyg 2008, 79:19-27.
- [71]Majambere S, Pinder M, Fillinger U, Ameh D, Conway DJ, Green C, Jeffries D, Jawara M, Milligan PJ, Hutchinson R, Lindsay SW: Is mosquito larval source management appropriate for reducing malaria in areas of extensive flooding in the Gambia? A cross-over intervention trial. Am J Trop Med Hyg 2010, 82:176-184.
- [72]Ndenga BA, Simbauni JA, Mbugi JP, Githeko AK, Fillinger U: Productivity of malaria vectors from different habitat types in the western Kenya highlands. PLoS 2011, 6:e19473.
- [73]Mala AO, Irungu LW: Factors influencing differential larval habitat productivity of Anopheles gambiae complex mosquitoes in a western Kenyan village. J Vector Borne Dis 2011, 48:52-57.
- [74]Chen H, Minakawa N, Cui L, Yan G: Conspecific sharing of breeding sites by anopheline female mosquitoes (Diptera: Culicidae) inferred from microsatellite markers. J Insect Behav 2008, 21:24-33.
- [75]Chen H, Fillinger U, Yan G: Oviposition behavior of female Anopheles gambiae in western Kenya inferred from microsatellite markers. Am J Trop Med Hyg 2006, 75:246-250.
- [76]Herrera-Varela M, Lindh J, Lindsay SW, Fillinger U: Habitat discrimination by gravid Anopheles gambiae sensu lato - a push-pull system. Malar J 2014, 13:133.
- [77]Judson CL, de Lumen HZ: Some effects of juvenile hormone and analogues on the ovarian follicles of the mosquito Aedes aegypti (Diptera: Culicidae). J Med Entomol 1976, 13:197-201.
- [78]Bai H, Gelman DB, Palli SR: Mode of action of methoprene in affecting female reproduction in the African malaria mosquito, Anopheles gambiae. Pest Manag Sci 2011, 66:936-943.
- [79]Matowo NS, Moore J, Mapua S, Madumla EP, Moshi IR, Kaindoa EW, Mwangungulu SP, Kavishe DR, Sumaye RD, Lweitoijera DW, Okumu FO: Using a new odour-baited device to explore options for luring and killing outdoor-biting malaria vectors: a report on design and field evaluation of the mosquito landing box. Parasit Vectors 2013, 6:137.
- [80]Snetselaar J, Andriessen R, Suer RA, Osinga AJ, Knols BG, Farenhorst M: Development and evaluation of a novel contamination device that targets multiple life-stages of Aedes aegypti. Parasit Vectors 2014, 7:200.
- [81]World Health Organization: Launch of the global plan for insecticide resistance management in malaria. Event report. Geneva; 2012.
PDF