期刊论文详细信息
Particle and Fibre Toxicology
Contrasting Plasmodium infection rates and insecticide susceptibility profiles between the sympatric sibling species Anopheles parensis and Anopheles funestus s.s: a potential challenge for malaria vector control in Uganda
Charles S Wondji2  Josephine Birungi1  Louis G Mukwaya1  Jacob M Riveron2  Helen Irving2  Charles Mulamba1 
[1]Uganda Virus Research Institute, Entebbe, Uganda
[2]Vector Biology Department, Liverpool School of Tropical Medicine, Pembroke Place, Liverpool L3 5QA, UK
关键词: Uganda;    Vector control;    Insecticide resistance;    Malaria;    An. funestus;    An. parensis;   
Others  :  813957
DOI  :  10.1186/1756-3305-7-71
 received in 2013-10-25, accepted in 2014-02-10,  发布年份 2014
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【 摘 要 】

Background

Although the An. funestus group conceals one of the major malaria vectors in Africa, little is known about the dynamics of members of this group across the continent. Here, we investigated the species composition, infection rate and susceptibility to insecticides of this species group in Uganda.

Methods

Indoor resting blood-fed Anopheles adult female mosquitoes were collected from 3 districts in Uganda. Mosquitoes morphologically belonging to the An. funestus group were identified to species by PCR. The sporozoite infection rates were determined by TaqMan and a nested PCR. Susceptibility to major insecticides was assessed using WHO bioassays. The potential role of four candidate resistance genes was assessed using qRT-PCR.

Results

An. funestus s.s. and An. parensis, were the only members of the An. funestus group identified. Both species were sympatric in Masindi (North-West), whereas only An. parensis was present in Mityana (Central) and Ntungamo (South-West). The Plasmodium falciparum infection detected in An. parensis (4.2%) by TaqMan could not be confirmed by nested PCR, whereas the 5.3% infection in An. funestus s.s. was confirmed. An. parensis was susceptible to most insecticides, however, a moderate resistance was observed against deltamethrin and DDT. In the sympatric population of Masindi, resistance was observed to pyrethroids (permethrin and deltamethrin) and DDT, but all the resistant mosquitoes belonged to An. funestus s.s. No significant over-expression was observed for the four P450 candidate genes CYP6M7, CYP9K1, CYP6P9 and CYP6AA4 between deltamethrin resistant and control An. parensis. However, when compared with the susceptible FANG An. funestus s.s strain, the CYP9K1 is significantly over-expressed in An. parensis (15-fold change; P < 0.001), suggesting it could play a role in the deltamethrin resistance.

Conclusion

The contrasting infection rates and insecticide susceptibility profiles of both species highlights the importance of accurate species identification for successful vector control programs.

【 授权许可】

   
2014 Mulamba et al.; licensee BioMed Central Ltd.

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【 参考文献 】
  • [1]Yeka A, Gasasira A, Mpimbaza A, Achan J, Nankabirwa J, Nsobya S, Staedke SG, Donnelly MJ, Wabwire-Mangen F, Talisuna A, Dorsey G, Kamya MR, Rosenthal PJ: Malaria in Uganda: challenges to control on the long road to elimination: I. Epidemiology and current control efforts. Acta Trop 2012, 121:184-195.
  • [2]Morgan JC, Irving H, Okedi LM, Steven A, Wondji CS: Pyrethroid resistance in an Anopheles funestus population from Uganda. PLoS One 2010, 5:e11872.
  • [3]Cohuet A, Simard F, Toto JC, Kengne P, Coetzee M, Fontenille D: Species identification within the Anopheles funestus group of malaria vectors in Cameroon and evidence for a new species. Am J Trop Med Hyg 2003, 69:200-205.
  • [4]Gillies MT, Coetzee M: A supplement to the Anophelinae of Africa south of the Sahara (Afrotropical region). Johannesburg: South African Institute for Medical Research; 1987.
  • [5]Gillies MT, De Meillon B: The anophelinae of Africa South of the Sahara. Johannesburg: The South African Institute for Medical Research; 1968.
  • [6]Harbach RE: The classification of genus Anopheles (Diptera: Culicidae): a working hypothesis of phylogenetic relationships. Bull Entomol Res 2004, 94:537-553.
  • [7]Spillings BL, Brooke BD, Koekemoer LL, Chiphwanya J, Coetzee M, Hunt RH: A new species concealed by Anopheles funestus Giles, a major malaria vector in Africa. Am J Trop Med Hyg 2009, 81:510-515.
  • [8]Coetzee M, Koekemoer LL: Molecular systematics and insecticide resistance in the major African malaria vector Anopheles funestus. Annu Rev Entomol 2013, 58:393-412.
  • [9]Dia I, Guelbeogo MW, Ayala D: Advances and Perspectives in the Study of the Malaria Mosquito Anopheles funestus. In Anopheles mosquitoes - New insights into malaria vectors. Edited by Manguin S. In Tech Publisher; 2013:197-220.
  • [10]Wilkes TJ, Matola YG, Charlwood JD: Anopheles rivulorum, a vector of human malaria in Africa. Med Vet Entomol 1996, 10:108-110.
  • [11]Okello PE, Van Bortel W, Byaruhanga AM, Correwyn A, Roelants P, Talisuna A, D’Alessandro U, Coosemans M: Variation in malaria transmission intensity in seven sites throughout Uganda. Am J Trop Med Hyg 2006, 75:219-225.
  • [12]De Meillon B, Van Eeden G, Coetzee L, Coetzee M, Meiswinkel R, Du Toit C, Hansford C: Observations on a species of the Anopheles funestus subgroup, a suspected exophilic vector of malaria parasites in northeastern Transvaal, South Africa. Mosq News 1977, 37:657-661.
  • [13]Coetzee M, Fontenille D: Advances in the study of Anopheles funestus, a major vector of malaria in Africa. Insect Biochem Mol Biol 2004, 34:599-605.
  • [14]Cuamba N, Morgan JC, Irving H, Steven A, Wondji CS: High level of pyrethroid resistance in an Anopheles funestus population of the Chokwe District in Mozambique. PLoS One 2010, 5:e11010.
  • [15]Livak KJ: Organization and mapping of a sequence on the Drosophila melanogaster X and Y chromosomes that is transcribed during spermatogenesis. Genetics 1984, 107:611-634.
  • [16]Koekemoer LL, Kamau L, Hunt RH, Coetzee M: A cocktail polymerase chain reaction assay to identify members of the Anopheles funestus (Diptera: Culicidae) group. Am J Trop Med Hyg 2002, 66:804-811.
  • [17]Bass C, Nikou D, Blagborough AM, Vontas J, Sinden RE, Williamson MS, Field LM: PCR-based detection of Plasmodium in Anopheles mosquitoes: a comparison of a new high-throughput assay with existing methods. Malar J 2008, 7:177-177. BioMed Central Full Text
  • [18]Snounou G, Viriyakosol S, Zhu XP, Jarra W, Pinheiro L, do Rosario VE, Thaithong S, Brown KN: High sensitivity of detection of human malaria parasites by the use of nested polymerase chain reaction. Mol Biochem Parasitol 1993, 61:315-320.
  • [19]WHO: Test procedures for insecticide resistance montoring in malaria vectors, bio-efficacy and persistence of insecticides on treated surfaces. Geneva, Switzerland: World Health Organization; 1998.
  • [20]Riveron JM, Irving H, Ndula M, Barnes KG, Ibrahim SS, Paine MJ, Wondji CS: Directionally selected cytochrome P450 alleles are driving the spread of pyrethroid resistance in the major malaria vector Anopheles funestus. Proc Natl Acad Sci U S A 2013, 110:252-257.
  • [21]Jones CM, Machin C, Mohammed K, Majambere S, Ali AS, Khatib BO, McHa J, Ranson H, Kelly-Hope LA: Insecticide resistance in Culex quinquefasciatus from Zanzibar: implications for vector control programmes. Parasit Vectors 2012, 5:78. BioMed Central Full Text
  • [22]Schmittgen TD, Livak KJ: Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 2008, 3:1101-1108.
  • [23]Irving H, Riveron JM, Ibrahim SS, Lobo NF, Wondji CS: Positional cloning of rp2 QTL associates the P450 genes CYP6Z1, CYP6Z3 and CYP6M7 with pyrethroid resistance in the malaria vector Anopheles funestus. Heredity 2012, 109:383-392.
  • [24]Echodu R, Okello-Onen J, Lutwama J, Enyaru J, Ocan R, Asaba R, Ajuga F, Rubaire-Akiiki C, Bradley D, Mutero C: Heterogeneity of anopheles mosquitoes in Nyabushozi County, Kiruhura district, Uganda. J Parasitol Vect Biol 2010, 2:28-34.
  • [25]Kamau L, Koekemoer LL, Hunt RH, Coetzee M: Anopheles parensis: the main member of the Anopheles funestus species group found resting inside human dwellings in Mwea area of central Kenya toward the end of the rainy season. J Am Mosq Control Assoc 2003, 19:130-133.
  • [26]Mouatcho JC, Hargreaves K, Koekemoer LL, Brooke BD, Oliver SV, Hunt RH, Coetzee M: Indoor collections of the Anopheles funestus group (Diptera: Culicidae) in sprayed houses in northern KwaZulu-Natal, South Africa. Malar J 2007, 6:30. BioMed Central Full Text
  • [27]Gillies MT, Furlong M: An investigation into the behaviour of Anopheles parensis Gillies at Malindi on the Kenya coast. Bull Entomol Res 1964, 55:1-16.
  • [28]Molineaux L, Gramiccia G: The Garki project: research on the epidemiology and control of malaria in the Sudan savanna of West Africa. Geneva ; Albany, N.Y: World Health Organization; WHO Publications Centre USA distributor; 1980.
  • [29]Awolola TS, Oyewole IO, Koekemoer LL, Coetzee M: Identification of three members of the Anopheles funestus (Diptera: Culicidae) group and their role in malaria transmission in two ecological zones in Nigeria. Trans R Soc Trop Med Hyg 2005, 99:525-531.
  • [30]Hargreaves K, Koekemoer LL, Brooke BD, Hunt RH, Mthembu J, Coetzee M: Anopheles funestus resistant to pyrethroid insecticides in South Africa. Med Vet Entomol 2000, 14:181-189.
  • [31]Brooke BD, Kloke G, Hunt RH, Koekemoer LL, Temu EA, Taylor ME, Small G, Hemingway J, Coetzee M: Bioassay and biochemical analyses of insecticide resistance in southern African Anopheles funestus (Diptera: Culicidae). Bull Entomol Res 2001, 91:265-272.
  • [32]Djouaka R, Irving H, Tukur Z, Wondji CS: Exploring mechanisms of multiple insecticide resistance in a population of the malaria vector anopheles funestus in Benin. PLoS One 2011, 6:e27760.
  • [33]Okoye PN, Brooke BD, Koekemoer LL, Hunt RH, Coetzee M: Characterisation of DDT, pyrethroid and carbamate resistance in Anopheles funestus from Obuasi, Ghana. Trans R Soc Trop Med Hyg 2008, 102:591-598.
  • [34]Wondji CS, Coleman M, Kleinschmidt I, Mzilahowa T, Irving H, Ndula M, Rehman A, Morgan J, Barnes KG, Hemingway J: Impact of pyrethroid resistance on operational malaria control in Malawi. Proc Natl Acad Sci U S A 2012, 109:19063-19070.
  • [35]Nwane P, Etang J, Chouasmall Yi UM, Toto JC, Koffi A, Mimpfoundi R, Simard F: Multiple insecticide resistance mechanisms in Anopheles gambiae s.l. populations from Cameroon, Central Africa. Parasit Vectors 2013, 6:41. BioMed Central Full Text
  • [36]Witzig C, Parry M, Morgan JC, Irving H, Steven A, Cuamba N, Kerah-Hinzoumbe C, Ranson H, Wondji CS: Genetic mapping identifies a major locus spanning P450 clusters associated with pyrethroid resistance in kdr-free Anopheles arabiensis from Chad. Heredity 2013, 110:389-397.
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