The call for malaria control, over the last century, marked a new epoch in the history of this disease. Many control strategies targeting either the Plasmodium parasite or the Anopheles vector were shown to be effective. Yet, the emergence of drug resistant parasites and insecticide resistant mosquito strains, along with numerous health, environmental, and ecological side effects of many chemical agents, highlighted the need to develop alternative tools that either complement or substitute conventional malaria control approaches. The use of biological means is considered a fundamental part of the recently launched malaria eradication program and has so far shown promising results, although this approach is still in its infancy. This review presents an overview of the most promising biological control tools for malaria eradication, namely fungi, bacteria, larvivorous fish, parasites, viruses and nematodes.
References
[1]
World Health Organization Regional Office for South-East Asia. Anopheline Species Complexes in South and South-East; World Health Organization Regional Office for South-East Asia: New Delhi, India, 2007; p. 102.
[2]
Murray, C.J.L.; Rosenfeld, L.C.; Lim, S.S.; Andrews, K.G.; Foreman, K.J.; Haring, D.; Fullman, N.; Mohsen, N.; Rafael, L.; Lopez, A.D. Global malaria mortality between 1980 and 2010: A systematic analysis. Lancet 2012, 379, 413–431, doi:10.1016/S0140-6736(12)60034-8.
[3]
Anopheles. Available online: http://en.wikipedia.org/wiki/Anopheles (accessed on 10 May 2012).
[4]
Oaks, S.C.; Mitchell, V.S.; Pearson, G.W. Malaria: Obstacles and Opportunities; Carpenter, C.C.J., Ed.; National Academy: Washington, WA, USA, 1991.
[5]
Bronner, U.; Divis, P.C.; Farnert, A.; Singh, B. Swedish Traveller with Plasmodium Knowlesi Malaria After Visiting Malaysian Borneo. Malar. J. 2009, 8, 15, doi:10.1186/1475-2875-8-15.
[6]
Harrison, G. Mosquitoes, Malaria and Man. A history of Hostilities since 1880; Murray, J., Ed.; Dutton: New York, NY, USA, 1978; p. 314.
[7]
World Health Organization. Implementation of the Global Malaria Control Strategy; Technical Report Series, No. 839; World Health Organization: Geneva, Switzerland, 1993; pp. 1–62.
[8]
Raghavendra, K.; Subbarao, S.K. Chemical Insecticides in Malaria Vector Control in India. ICMR Bull 2002, 32, 93–99.
[9]
Hassall, K.A. The Chemistry of Pesticide: Their Metabolism, Mode of Action, and Uses in Crop Protections; Chemie, V., Ed.; Weinheim: Deerfield Beach, FL, USA, 1982; p. 372.
[10]
D’Alessandro, U.; Olaleye, B.O.; McGuire, W.; Thomson, M.C.; Langerock, P.; Bennett, S.; Greenwood, B.M. A comparison of the efficacy of insecticide-treated and untreated bed nets in preventing malaria in Gambian children. Trans. R. Soc. Trop. Med. Hyg. 1995, 89, 596–598, doi:10.1016/0035-9203(95)90401-8.
[11]
Trigg, P.I.; Kondrachine, A.V. Commentary: Malaria Control in the 1990s. Bull. World Health Organ. 1998, 76, 11–16.
[12]
Shiff, C. Integrated approach to malaria control. Clin. Microbiol. Rev. 2002, 15, 278–293, doi:10.1128/CMR.15.2.278-293.2002.
[13]
Mabaso, M.L.H.; Sharp, B.; Lengeler, C. Historical review of malarial control in Southern African with emphasis on the use of indoor residual house-spraying. Trop. Med. Int. Health 2004, 9, 846–856, doi:10.1111/j.1365-3156.2004.01263.x.
[14]
Wakabi, W. Africa counts greater successes against malaria. Lancet 2007, 370, 1895–1896, doi:10.1016/S0140-6736(07)61796-6.
[15]
Pant, C.P. Malaria Vector Control: Imagociding. In Malaria: Principles and Practicie of Malariology; Wernsdorfer, W.H., McGregor, I.A., Eds.; Churchill Livingstone: Edinburgh, UK, 1988; pp. 1173–1212.
[16]
Rozendaal, J.A. Vector Control: Methods for Use by Individuals and Communities; World Health Organization: Geneva, Switzerland, 1997; pp. 1–412.
[17]
Gratz, N.G.; Pal, R. Malaria Vector Control: Larviciding. In Malaria: Principle and Practices of Malariology; Wernsdorfer, W.H., McGregor, I.A., Eds.; Churchill Livingstone: Edinburgh, UK, 1988; pp. 1213–1226.
[18]
Raghavendra, K.; Barik, T.K.; Niranjan Reddy, B.P.; Sharma, P.; Dash, A.P. Malaria vector control: From past to future. Parasitol. Res. 2011, 108, 757–779, doi:10.1007/s00436-010-2232-0.
[19]
Kumar, A.; Sharma, V.P.; Sumodan, P.K.; Thavaselvan, D.; Kamat, R.H. Malaria control utilizing Bacillus sphaericus against Anopheles stephensi breeding in construction sites and abandoned overhead tanks with Bacillus thuringiensis var. israelensis. J. Am. Mosq. Control Assoc. 1994, 11, 86–89.
[20]
Gopaul, R. Entomological surveillance in mauritius. Sante 1995, 5, 401–405.
[21]
Parvez, S.D.; Al-Wahaibi, S.S. Comparison of three larviciding options for malaria vector control. East Mediterr. Health J. 2003, 9, 627–636.
[22]
National malaria eradication programme, Directorate General of Health Services. Epidemiology and Control of Malaria in India; World Health Organization: New Delhi, India, 1996; p. 251.
[23]
Global Malaria Programme. Available online: http://www.who.int/malaria/en/ (accessed on 20 April 2012).
[24]
Brown, A.W. Laboratory Studies on the Behaviouristic Resistance of Anopheles albimanus in Panama. Bull. World Health Organ. 1958, 19, 1053–1061.
[25]
Beier, J.C. Malaria control in the highlands of burundi: An important success story. Am. J. Trop. Med. Hyg. 2008, 79, 1–2.
[26]
Fang, W.; Vega-Rodríguez, J.; Ghosh, A.K.; Jacobs-Lorena, M.; Kang, A.; St Leger, R.J. Development of transgenic fungi that kill human malaria parasites in mosquitoes. Science 2011, 331, 1074–1077, doi:10.1126/science.1199115.
[27]
Orduz, S.; Restrepo, N.; Pati？o, M.M.; Rojas, W. Transfer of toxin genes to alternate bacterial hosts for mosquito control. Mem. Inst. Oswaldo Cruz. 1995, 90, 97–107, doi:10.1590/S0074-02761995000100020.
[28]
Scholte, E.J.; Knols, B.G.J.; Samson, R.A.; Takken, W. Entomopathogenic fungi for mosquito control: A review. J. Insect Sci. 2004, 4, 24.
Scholte, E.J.; Knols, B.G.J.; Samson, R.A.; Takken, W. Infection of the malaria mosquito Anopheles gambiae with the entomopathogenic fungus Metarhizium anisopliae reduces blood feeding and fecundity. J. Invertebr. Pathol. 2006, 91, 43–49, doi:10.1016/j.jip.2005.10.006.
[34]
Charles, J.F.; Nielsen-LeRoux, C. Mosquitocidal bacterial toxins: Diversity, mode of action and resistance phenomena. Mem. Inst. Oswaldo Cruz. 2002, 95, 201–206.
[35]
Unep, I.L.O. Bacillus Thuringiensis: Environmental Health Criteria; Series No. 217; World Health Organization: Geneva, Switzerland, 1999.
[36]
Becker, N. The use of Bacillus thuringiensis subsp. israelensis (Bti) against mosquitoes, with special emphasis on the ecological impact. Isr. J. Entomol. 1998, 32, 63–69.
[37]
Guillet, P.; Kurstak, D.; Philippon, B.; Meyer, R. Use of Bacillus thuringiensis israelensis for Onchocerciasis Control in West Africa. In Bacterial Control of Mosquitoes and Blackflies; de Barjac, H., Sutherland, D.J., Eds.; Rutgers University Press: New Brunswick, NJ, USA, 1990; pp. 187–199.
[38]
Majori, G.; Ali, A.; Sabatinelli, G. Laboratory and field efficacy of Bacillus thuringiensis var. israelensis and Bacillus sphaericus against Anopheles gambiae s.l. and Culex quinquefasciatus in Ouagadougou, Burkina Faso. J. Am. Mosq. Control Assoc. 1987, 3, 20–25.
[39]
Karch, S.; Manzambi, Z.A.; Salaun, J.J. Field trials with vectolex (Bacillus sphaericus) and vectobac (Bacillus thuringiensis (H-14)) against Anopheles gambiae and Culex quinquefasciatus Breeding in Zaire. J. Am. Mosq. Control Assoc. 1991, 7, 176–179.
[40]
Karch, S.; Asidi, N.; Manzambi, Z.M.; Salaun, J.J. Efficacy of Bacillus sphaericus against the malaria vector Anopheles gambiae and other mosquitoes in swamps and rice fields in Zaire. J. Am. Mosq. Control Assoc. 1992, 8, 376–380.
[41]
Ragoonanansingh, R.N.; Njunwa, K.J.; Curtis, C.F.; Becker, N. A field study of Bacillus sphaericus for the control of culicine and anopheline mosquito larvae in Tanzania. Bull. Soc. Vector Ecol. 1992, 17, 45–50.
[42]
Ravoahangimalala, O.; Thiery, I.; Sinegre, G. Rice field efficacy of deltamethrin and Bacillus thuringiensis israelensis formulations on Anopheles gambiae s.s. the Anjiro region of Madagascar. Bull. Soc. Vector Ecol. 1994, 19, 169–174.
[43]
Seyoum, A.; Abate, D. Larvicidal efficacy of Bacillus thuringiensis var. israelensis and Bacillus sphaericus on Anopheles arabiensis in Ethiopia. World J. Microbiol. Biotechnol. 1997, 13, 21–24, doi:10.1007/BF02770802.
[44]
Skovmand, O.; Sanogo, E. Experimental formulations of Bacillus sphaericus and Bacillus thuringiensis israelensis against Culex quinquefasciatus and Anopheles gambiae (Diptera: Culicidae) in Burkina Faso. J. Med. Entomol. 1999, 36, 62–67.
[45]
Barbazan, P.; Baldet, T.; Darriet, F.; Escaffre, H.; Djoda, D.H.; Hougard, J.M. Control of Culex quinquefasciatus (Diptera: Culicidae) with Bacillus sphaericus in Maroua, Cameroon. J. Am. Mosq. Control Assoc. 1997, 13, 263–269.
[46]
Barbazan, P.; Baldet, T.; Darriet, F.; Escaffre, H.; Djoda, D.H.; Hougard, J.M. Impact of treatments with Bacillus sphaericus on Anopheles populations and the transmission of malaria in Maroua, a Large City in a Savannah region of Cameroon. J. Am. Mosq. Control Assoc. 1998, 14, 33–39.
[47]
Das, P.K.; Amalraj, D.D. Biological control of malaria vectors. Indian J. Med. Res. 1997, 106, 174–197.
[48]
Chouaia, B.; Rossi, P.; Montagna, M.; Ricci, I.; Crotti, E.; Damiani, C.; Epis, S.; Faye, I.; Sagnon, N.; Alma, A.; et al. Molecular evidence for multiple infections as revealed by typing of Asaia bacterial symbionts of four mosquito species. Appl. Environ. Microbiol. 2010, 76, 7444–7450, doi:10.1128/AEM.01747-10.
[49]
Damiani, C.; Ricci, I.; Crotti, E.; Rossi, P.; Rizzi, A.; Scuppa, P.; Capone, A.; Ulissi, U.; Epis, S.; Genchi, M.; et al. Mosquito-bacteria symbiosis: the case of Anopheles gambiae and Asaia. Microb. Ecol. 2010, 60, 644–654, doi:10.1007/s00248-010-9704-8.
[50]
Favia, G.; Ricci, I.; Damiani, C.; Raddadi, N.; Crotti, E.; Marzorati, M.; Rizzi, A.; Urso, R.; Brusetti, L.; Borin, S.; et al. Bacteria of the genus Asaia stably associate with Anopheles stephensi, an Asian malarial mosquito vector. Proc. Natl. Acad. Sci. USA 2007, 104, 9047–9051.
[51]
Favia, G.; Ricci, I.; Marzorati, M.; Negri, I.; Alma, A.; Sacchi, L.; Bandi, C.; Daffonchio, D. Bacteria of the genus Asaia: A potential paratransgenic weapon against malaria. Adv. Exp. Med. Biol. 2008, 627, 49–59, doi:10.1007/978-0-387-78225-6_4.
[52]
Crotti, E.; Damiani, C.; Pajoro, M.; Gonella, E.; Rizzi, A.; Ricci, I.; Negri, I.; Scuppa, P.; Rossi, P.; Ballarini, P.; et al. Asaia, a versatile acetic acid bacterial symbiont, capable of cross-colonizing insects of phylogenetically distant genera and orders. Environ. Microbiol. 2009, 11, 3252–3264, doi:10.1111/j.1462-2920.2009.02048.x.
[53]
Kambris, Z.; Cook, P.E.; Phuc, H.K.; Sinkins, S.P. Immune activation by life shortening Wolbachia and reduced filarial competence in mosquitoes. Science 2009, 326, 134–136.
[54]
Hughes, G.L.; Koga, R.; Xue, P.; Fukatsu, T.; Rasgon, J.L. Wolbachia infections are virulent and inhibit the human malaria parasite Plasmodium falciparum in Anopheles gambiae. PLoS Pathog. 2011, 7, e1002043, doi:10.1371/journal.ppat.1002043.
[55]
Walker, K. A Review of Control Methods for African Malaria Vectors; Activity Report 108; Agency for International Development: Washington, WA, USA, 2002.
Yap, H.H. Biological control of mosquitoes, especially malaria vectors, Anopheles specie. Southeast Asian J. Trop. Med. Public Health 1985, 16, 163–172.
[58]
World Health Organization. Manual on Environmental Management for Mosquito Control with Special Emphasis on Malaria Vectors; WHO Offset Publication No. 66; World Health Organization: Geneva, Switzerland, 1982; pp. 1–276.
[59]
Rupp, H.R. Adverse assessments of Gambusia affinis: An alternate view for mosquito control practitioners. J. Am. Mos. Control Assoc. 1996, 12, 155–166.
[60]
Dua, V.K.; Sharma, S.K. Use of Guppy and Gambusia Fishes for Control of Mosquito Breeding at BHEL. Industrial Complex, Hardwar (U.P.). In Larvivorous Fishes of Inland Ecosystems; Sharma, V.P., Ghosh, A., Eds.; Malaria Research Centre: Delhi, India, 1994; pp. 35–42.
[61]
Wu, N.; Liao, G.; Li, D.; Luo, Y.; Zhong, G. The advantages of mosquito biocontrol by stocking edible fish in rice paddies. Southeast Asian J. Trop. Med. Public Health 1991, 22, 436–442.
[62]
Lacey, L.A.; Lacey, C.M. The medicinal importance of riceland mosquitoes and their control using alternatives to chemical insecticides. J. Am. Mosq. Control Assoc. 1990, 2, 1–93.
[63]
Victor, T.J.; Chandrasekaran, B.; Reuben, R. Composite fish culture for mosquito control in rice fields in Southern India. Southeast Asian J. Trop. Med. Public Health 1994, 25, 522–527.
[64]
Fletcher, M.; Teklehaimanot, A.; Yemane, G. Control of mosquito larvae in the port city of Assab by an indigenous larvivorous fish, Aphanius dispar. Acta Trop. 1992, 52, 155–166, doi:10.1016/0001-706X(92)90032-S.
[65]
Menon, P.K.B.; Rajagopalan, P.K. Control of mosquito breeding in wells by using Gambusia affinis and Aplocheilus blocki in Pondicherry town. Indian J. Med. Res. 1978, 68, 927–933.
[66]
Kumar, A.; Sharma, V.P.; Sumodan, P.K.; Thavaselvam, D. Field trials of biolarvicide Bacillus thuringiensis var. israelensis strain 164 and the larvivorous fish Aplocheilus blocki against Anopheles stephensi for malaria control in Goa, India. J. Am. Mos. Control Assoc. 1998, 14, 457–462.
[67]
Sabatinelli, G.; Blanchy, S.; Majori, G.; Papakay, M. Impact de L’utilisations du poisson larvivore Poecilia reticulata Sur la transmission du paludisme en RFI des comores. Ann. Parasitol. Hum. Comp. 1991, 66, 84–88.
[68]
Gupta, D.K.; Bhatt, R.M.; Sharma, R.C.; Gautam, A.S. Rajnikant. Intradomestic mosquito breeding sources and their management. Indian J. Malariol. 1992, 29, 41–46.
[69]
Rajnikant, D.; Bhatt, R.M.; Gupta, D.K.; Sharma, R.C.; Srivastava, H.C.; Gautam, A.S. Observations on mosquito breeding in wells and its control. Indian J. Malariol. 1993, 20, 215–220.
[70]
Kusumawathie, P.H.D.; Wickremasinghe, A.R.; Karunaweera, N.D.; Wijeyaratne, M.J.S. Larvivorous potential of the Guppy, Poecilia reticulata, in Anopheline mosquito control in riverbed pools below the Kotmale Dam, Sri Lanka. Asia Pac. J. Public Health 2008, 20, 56–63, doi:10.1177/1010539507308507.
[71]
Shililu, J.; Ghebremeskel, T.; Seulu, F.; Mengistu, S.; Fekadu, H.; Zerom, M.; Asmelash, G.E.; Sintasath, D.; Mbogo, C.; Githure, J.; et al. Seasonal abundance, vector behavior, and malaria parasite transmission in Eritrea. J. Am. Mosq. Control Assoc. 2004, 20, 155–164.
[72]
Lyimo, E.O.; Koella, J.C. Relationship between body size of adult Anopheles gambiae s.l. and infection with the malaria parasite Plasmodium falciparum. Parasitology 1992, 104, 233–237, doi:10.1017/S0031182000061667.
[73]
Ameneshewa, B.; Service, M.W. The relationship between female body size and survival rates of the malaria vector Anopheles arabiensis in Ethiopia. Med. Vet. Entomol. 1996, 10, 170–172, doi:10.1111/j.1365-2915.1996.tb00724.x.
[74]
Bano, L. Partial inhibitory effect of Plistophora culicis on the Sporogonic cycle of Plasmodium cynomolgi in Anopheles Stephensi. Nature 1958, 181, 430, doi:10.1038/181430a0.
[75]
Fox, R.M.; Weiser, J. A microsporidian parasite of Anopheles gambiae in Liberia. J. Parasitol. 1959, 45, 21–30, doi:10.2307/3274782.
[76]
Gajanana, A.; Tewari, S.C.; Reuben, R.; Rajagopalan, P.K. Partial suppression of malaria parasites in Aedes aegypti and Anopheles stephensi doubly infected with Nosema algerae and Plasmodium. Indian J. Med. Res. 1979, 70, 417–423.
[77]
Hulls, R.H. The adverse effects of a microsporidian on the sporogony and infectivity of Plasmodium berghei. Trans. R. Soc. Trop. Med. Hyg. 1971, 65, 412–423, doi:10.1016/0035-9203(71)90033-2.
[78]
Schenker, W.; Maier, W.A.; Seitz, H.M. The Effects of Nosema algerae on the Development of Plasmodium yoelii nigeriensis in Anopheles stephensi. Parasitol Res. 1992, 78, 56–59, doi:10.1007/BF00936182.
[79]
Koella, J.C.; Agnew, P. Blood-feeding success of the mosquito Aedes aegypti depends on the transmission route of its parasite Edhazardia aedis. Oikos 1997, 78, 311–316, doi:10.2307/3546298.
[80]
Koella, J.C.; Lorenz, L.; Bargielowski, I. Microsporidians as evolution-proof agents of malaria control? Adv. Parasitol. 2009, 68, 315–327, doi:10.1016/S0065-308X(08)00612-X.
[81]
Ren, X.; Hoiczyk, E.; Rasgon, J.L. Viral paratransgenesis in the malaria vector Anopheles gambiae. PLoS Pathog. 2008, 4, 1–8.
[82]
Carlson, J.; Suchman, E.; Buchatsky, L. Densoviruses for control and genetic manipulation of mosquitoes. Adv. Virus Res. 2006, 68, 361–392, doi:10.1016/S0065-3527(06)68010-X.
[83]
Blackmore, M.S. Mermethid parasitism of adult mosquitoes in Sweden. Am. Midl. Nat. 1994, 312, 192–198, doi:10.2307/2426213.
[84]
Blackmore, M.S.; Berry, R.L.; Foster, W.A.; Walker, E.D.; Wilmot, T.R.; Craig, G.B., Jr. Records of mosquito parasitic mermithid nematodes in the northcentral United States. J. Am. Mosq. Control Assoc. 1993, 9, 338–343.
[85]
Trips, M.; Haufe, W.O.; Shemanchuk, J.A. Mermithid parasites of the mosquito Aedes vexans meigen in British Columbia. Can. J. Zool. 1968, 46, 1077–1079, doi:10.1139/z68-150.
[86]
Petersen, J.J.; Chapman, H.C.; Woodard, D.B. Preliminary observations on the incidence and biology of a mermithid nematode of Aedes sollicitans (walker) in Louisiana. Mosq. News 1967, 27, 493–498.
[87]
Pachecoa, R.P.; Hernándezb, C.R.; Reynab, J.L.; Belmontc, R.M.; Vegaa, J.R. Control of the mosquito Anopheles pseudopunctipennis (Diptera: Culicidae) with Romanomermis iyengari (Nematoda: Mermithidae) in Oaxaca, Mexico. Biol. Control 2005, 32, 137–142, doi:10.1016/j.biocontrol.2004.09.005.
[88]
Rojas, W.; Northup, J.; Gallo, O.; Montoya, A.E.; Montoya, F.; Restrepo, M.; Nimnich, G.; Arango, M.; Echavarria, M. Reduction of malaria prevalence after introduction of Romanomermis culicivorax (Mermithidae: Nematoda) in larval anopheles habitats in Colombia. Bull. World Health Org. 1987, 65, 331–337.
[89]
Howard, A.F.V.; Koenraadth, C.J.M.; Farenhorst, M.; Knols, B.G.J.; Takken, W. Pyrethroid resistance in Anopheles gambiae leads to increased susceptibility to the entomopathogenic fungi Metarhizium anisopliae and Beauveria bassiana.. Malar. J. 2010, 9, 168, doi:10.1186/1475-2875-9-168.
[90]
Farenhorst, M.; Knols, B.G.; Thomas, M.B.; Howard, A.F.; Takken, W.; Rowland, M.; N’Guessan, R. Synergy in efficacy of fungal entomopathogens and permethrin against West African insecticide-resistant Anopheles gambiae mosquitoes. PLoS One 2010, 11, 5.
[91]
Scholte, E.J.; Takken, W.; Knols, B.G.J. Pathogenicity of six East African entomopathogenic fungi to adult Anopheles gambiae s.s. (Diptera: Culicidae) mosquitoes. Proc. Exp. Appl. Entomol. 2003, 14, 25–29.
[92]
Read, A.F.; Lynch, P.A.; Thomas, M.B. How to make evolution-proof insecticides for malaria control. PLoS Biol. 2009, 7, e1000058.
[93]
Scholte, E.J.; Njiru, B.N.; Smallegange, R.C.; Takken, W.; Knols, B.G.J. Infection of malaria (Anopheles gambiae s.s.) and filariasis (Culex quinquefasciatus) vectors with the entomopathogenic fungus Metarhizium anisopliae. Malar. J. 2003, 2, 29, doi:10.1186/1475-2875-2-29.
Ferrari, J.; Muller, C.B.; Kraaijeveld, A.R.; Godfray, H.C.J. Clonal variation and covariation in Aphid resistance to parasitoids and a pathogen. Evolution 2001, 55, 1805–1814.
[99]
Thomas, M.B.; Blandford, S. Thermal biology in insect-Pathogen interactions. Trends Ecol. Evol. 2003, 18, 344–350, doi:10.1016/S0169-5347(03)00069-7.
[100]
Traniello, J.F.A.; Rosengaus, R.B.; Savoie, K. The development of immunity in a social insect: Evidence for the group facilitation of disease resistance. Proc. Natl. Acad. Sci. USA 2002, 99, 6838–6842, doi:10.1073/pnas.102176599.
[101]
Elliot, S.L.; Blandford, S.; Thomas, M.B. Host-pathogen interactions in a varying environment: temperature, behavioural fever and fitness. Proc. R. Soc. B 2002, 269, 1599–1607, doi:10.1098/rspb.2002.2067.
[102]
Partridge, L.; Barton, N.H. Optimality, mutation and evolution of ageing. Nature 1993, 362, 305–311, doi:10.1038/362305a0.
[103]
Boete, C.; Koella, J.C. Evolutionary ideas about genetically manipulated mosquitoes and malaria control. Trends Parasitol. 2003, 19, 32–38, doi:10.1016/S1471-4922(02)00003-X.
[104]
Riehle, M.M.; Markianos, K.; Niaré, O.; Xu, J.; Li, J.; Touré, AM.; Podiougou, B.; Oduol, F.; Diawara, S.; Diallo, M.; et al. Natural malaria infection in Anopheles gambiae is regulated by a single genomic control region. Science 2006, 312, 577–579, doi:10.1126/science.1124153.
[105]
Fillinger, U.; Knols, B.G.J.; Becker, N. Efficacy and efficiency of new Bacillus thuringiensis var. israelensis and Bacillus sphaericus formulations Afrotropical Anophelines in Western Kenya. Trop. Med. Int. Health 2003, 8, 37–47, doi:10.1046/j.1365-3156.2003.00979.x.
[106]
Consoli, R.A.; Santos, B.S.; Lamounier, M.A.; Secundino, N.F.; Rabinovitch, L.; Silva, C.M.; Alves, R.S.; Carneiro, N.F. Efficacy of a new formulation of Bacillus sphaericus 2362 against Culex quinquefasciatus (Diptera: Culicidae) in Montes Claros, Minas Gerais, Brazil. Mem. Inst. Oswaldo Cruz. 1997, 92, 571–573, doi:10.1590/S0074-02761997000400025.
[107]
Rodrigues, I.B.; Tadei, W.P.; Dias, J.M. Studies on the Bacillus sphaericus larvicidal activity against malarial vector species in Amazonia. Mem. Inst. Oswaldo Cruz. 1998, 93, 441–444, doi:10.1590/S0074-02761998000400005.
[108]
Rodrigues, I.B.; Tadei, W.P.; Dias, J.M. Larvicidal activity of Bacillus sphaericus 2362 against Anopheles nuneztovari, Anopheles darlingi and Anopheles braziliensis (Diptera, Culicidae). Rev. Inst. Med. Trop. Sao Paulo 1999, 41, 101–105.
[109]
Kroeger, A.; Dehlinger, U.; Burkhardt, G.; Atehortua, W.; Anaya, H.; Becker, N. Community based dengue control in Columbia: People’s knowledge and practice and the potential contribution of the biological larvicide Bti (Bacillus thuringiensis israelensis). Trop. Med. Parasitol. 1995, 46, 241–246.
[110]
Kroeger, A.; Horstick, O.; Riedl, C.; Kaiser, A.; Becker, N. The potential for malaria control with the biological larvicide Bacillus thuringiensis israelensis (Bti) in Peru and Ecuador. Acta Trop. 1995, 60, 47–57, doi:10.1016/0001-706X(95)00101-J.
[111]
Blanco Castro, S.D.; Martinez Arias, A.; Cano Velasquez, O.R.; Tello Granados, R.; Mendoza, I. Introduction of Bacillus sphaericus Strain-2362 (GRISELESF) for biological control of malaria vectors in Guatemala. Rev. Cubana. Med. Trop. 2000, 52, 37–43.
[112]
Regis, L.; Oliveira, C.M.; Silva-Filha, M.H.; Silva, S.B.; Maciel, A.; Furtado, A.F. Efficacy of Bacillus sphaericus in control of the filariasis vector Culex quinquefasciatus in an urban area of Olinda, Brazil. Trans. R. Soc. Trop. Med. Hyg. 2000, 94, 488–492, doi:10.1016/S0035-9203(00)90061-0.
[113]
Regis, L.; Silva, S.I.B.; Melo-Santos, M.A.V. The use of bacteria larvicides in mosquito and black fly control programmes in Brazil. Mem. Inst. Oswaldo Cruz. 2000, 95, 207–210, doi:10.1590/S0074-02762000000700035.
[114]
Porter, A.G.; Davidson, E.W.; Liu, J.W. Mosquitocidal toxins of Bacilli and their genetic manipulation for effective biological control of mosquitoes. Microbiologic. Rev. 1993, 57, 838–861.
[115]
Tianyun, S.; Mulla, M.S. Field evaluation of new waterdispersible granular formulations of Bacillus thuringiensis ssp. israelensis and Bacillus sphaericus against Culex mosquitoes in microcosms. J. Am. Mosq. Control Assoc. 1999, 15, 356–365.
[116]
Becker, N.; Zgomba, M.; Petric, D.; Beck, M.; Ludwig, M. Role of larval cadavers in recycling processes of Bacillus sphaericus. J. Am. Mosq. Control Assoc. 1995, 11, 329–334.
[117]
Pantuwatana, S.; Maneeroj, R.; Upatham, E.S. Long residual activity of Bacillus sphaericus 1593 against Culex quinquefasciatus larvae in artificial pools. Southeast Asian J. 1989, 20, 421–427.
[118]
Federici, B.A.; Park, H.W.; Bideshi, D.K.; Wirth, M.C.; Johnson, J.J. Review: Recombinant bacteria for mosquito control. J. Exp. Biol. 2003, 206, 3877–3885, doi:10.1242/jeb.00643.
[119]
Federici, B.A.; Park, H.W.; Bideshi, D.K.; Wirth, M.C.; Johnson, J.J.; Sakano, Y.; Tang, M. Developing recombinant bacteria for control of mosquito larvae. J. Am. Mosq. Control Assoc. 2007, 23, 164–175, doi:10.2987/8756-971X(2007)23[164:DRBFCO]2.0.CO;2.
[120]
Borovsky, D.; Carlson, D.A.; Griffin, P.R.; Shabanowitz, J.; Hunt, D.F. Sequence analysis, synthesis and characterization of Aedes aegypti trypsin oostatic factor (TMOF) and its analogs. Insect Biochem. Mol.Biol. 1993, 23, 703–712, doi:10.1016/0965-1748(93)90044-S.
[121]
Delécluse, A.; Rosso, M.L.; Ragni, A. Cloning and expression of a novel toxin gene from Bacillus thuringiensis subsp. jegathesan encoding a highly mosquitocidal protein. Appl. Environ. Microbiol. 1995, 61, 4230–4235.
[122]
Magesa, S.M.; Wilkes, T.J.; Mnzava, A.E.P.; Njunwa, K.J.; Myamba, J.; Kivuyo, M.D.P.; Hill, N.; Lines, J.D.; Curtis, C.F. Trial of pyrethroid impregnated bed nets in an area of Tanzania holoendemic for malaria, 2. Effects on the malaria vector population. Acta Trop. 1991, 49, 97–108, doi:10.1016/0001-706X(91)90057-Q.
[123]
Robert, V.; Carnevale, P. Influence of deltamethrin treatment of bed nets on malaria transmission in the Kou Valley, Burkina Faso. Bull. World Health Org. 1991, 69, 735–740.
[124]
Gimnig, J.E.; Kolczak, M.S.; Hightower, A.W.; Vulule, J.M.; Schoute, E.; Kamau, L.; Phillips-Howard, P.A.; Ter Kuile, F.O.; Nahlen, B.L.; Hawley, W.A. Effect of permethrin-treated bed nets on the spatial distribution of malaria vectors in Western Kenya. Am. J. Trop. Med. Hyg. 2003, 68, 115–120.
[125]
Service, M.W. Biological control of mosquitoes—has it a future? Mosq. News 1983, 43, 113.
[126]
Service, M.W. Importance of ecology in Aedes aegypti control. Southeast Asian J. Trop. Med. Public Health 1992, 23, 681–688.
[127]
Killeen, G.F.; Fillinger, U.; Knols, B.G.J. Advantages of larval control for African malaria vectors: Low mobility and behavioural responsiveness of immature mosquito stages allow high effective Coverage. Malar. J. 2002, 1, 1–7, doi:10.1186/1475-2875-1-1.
[128]
Hansen, M.H.H.; Koella, J.C. Evolution of tolerance: The genetic basis of a host’s resistance against parasite manipulation. Oikos 2003, 102, 309–317, doi:10.1034/j.1600-0706.2003.12537.x.
[129]
Riehle, M.A.; Moreira, C.K.; Lampe, D.; Lauzon, C.; Jacobs-Lorena, M. Using bacteria to express and display anti-Plasmodium molecules in the mosquito midgut. Int. J. Parasitol. 2007, 37, 595–603, doi:10.1016/j.ijpara.2006.12.002.
[130]
Daoust, R.A. Nematode Pathogens of Culicidae (Mosquitoes). In Bibligoraphy on Pathogens of Medically Important Arthropods; Robert, D.W., Daoust, R.A., Wraight, S.P., Eds.; World Health Organization: Geneva, Switzerland, 1983; pp. 102–118.
[131]
Washburn, J.O.; Anderson, J.R.; Egerter, D.E. Distribution and prevalence of Octomyomermis triglodytis (Nematoda: Mermithidae), a parasite of the Western tree hole mosquito, Aedes sierrensi. J. Am. Mosq. Control Assoc. 1986, 2, 341–346.
[132]
Nielsen, B.O. Mermithid Parasitism (Nematoda: Mermithidae) in Ochlerotatus cantans (Meigen) (Diptera: Culicidae) in Denmark. Available online: http://www.uel.ac.uk/mosquito/issue10/mermithids.htm (accessed on 23 May 2012).
[133]
Vythilingam, I.; Sidavong, B.; Chan, S.T.; Phonemixay, T.; Phompida, S.; Krishnasamy, M. First report of mermithid parasitism (Nematoda: Mermithidae) in mosquitoes (Diptera: Culicidae) from Lao PDR. Trop. Biomed. 2005, 22, 77–79.
[134]
World Health Organization. Vector Control for Malaria and Other Mosquito-Borne Diseases; WHO technical report series, No. 857; World Health Organization: Geneva, Switzerland, 1995; pp. 1–100.
