Journal of Global Infectious DiseasesOfficial Publishing of INDUSEM and OPUS 12 Foundation, Inc. Users online:203  
Print this pageEmail this pageSmall font sizeDefault font sizeIncrease font size     
Home About us Editors Ahead of Print Current Issue Archives Search Instructions Subscribe Advertise Login 
 


 
   Table of Contents     
ORIGINAL ARTICLE  
Year : 2012  |  Volume : 4  |  Issue : 2  |  Page : 114-119
Knockdown resistance, Rdl alleles, and the annual entomological Inoculation rate of wild mosquito populations from Lower Moshi, Northern Tanzania


1 Tropical Pesticides Research Institute, Mabogini Field Station, Moshi, Tanzania
2 Department of Preventive Medicine and Biometrics, Uniformed Services University of the Health Sciences, Bethesda, MD 20814-4799,USA; Unité d'entomologie médicale, Institut Pasteur de la Guyane, Cayenne Cedex, French Guiana
3 Poseidon Science Foundation, New York, USA
4 Division of Livestock and Human Diseases Vector Control, Mosquito Section, Tropical Pesticides Research Institute, Arusha, Tanzania

Click here for correspondence address and email

Date of Web Publication30-May-2012
 

   Abstract 

Aim: Understanding vector behavioral response due to ecological factors is important in the control of disease vectors. This study was conducted to determine the knockdown resistance (kdr) alleles, dieldrin resistance alleles, and entomological inoculation rates (EIRs) of malaria vectors in lower Moshi irrigation schemes for the mitigation of disease transmission. Materials and Methods: The study was longitudinal design conducted for 14 months. Mosquitoes were collected fortnightly by using a CDC miniature light trap in 20 houses. Mosquitoes were identified morphologically in the field, of which 10% of this population was identified to species level by using molecular techniques. Samples from this study population were taken for kdr and resistance to dieldrin (rdl) genes detection. Results: A total of 6220 mosquitoes were collected by using a light trap, of which 86.0% (n=5350) were Anopheles gambiae sensu lato and 14.0% (n=870) were Culex quinquefasciatus. Ten percent of the An. gambiae s.l. (n=535) collected were taken for species identification, of which 99.8% (n=534) were identified as An. arabiensis while 0.2% (n=1) were An. gambiae sensu stricto. Of the selected mosquitoes, 3.5% (n=19) were sporozoite positive. None of the mosquitoes tested had the kdr gene. The rdl resistant allele was detected at a frequency of 0.48 throughout the year. EIR was determined to be 0.54 ib/trap/year. Conclusion: The findings of this study suggest that the homozygous and the heterozygous resistance present in rdl genes demonstrated the effect of pesticide residues on resistance selection pressure in mosquitoes. A better insecticide usage protocol needs to be developed for farmers to use in order to avoid excessive use of pesticides. Key words: An. arabiensis, EIR, Knockdown mutation, Moshi, rdl locus, Tanzania

How to cite this article:
Mahande AM, Dusfour I, Matias JR, Kweka EJ. Knockdown resistance, Rdl alleles, and the annual entomological Inoculation rate of wild mosquito populations from Lower Moshi, Northern Tanzania. J Global Infect Dis 2012;4:114-9

How to cite this URL:
Mahande AM, Dusfour I, Matias JR, Kweka EJ. Knockdown resistance, Rdl alleles, and the annual entomological Inoculation rate of wild mosquito populations from Lower Moshi, Northern Tanzania. J Global Infect Dis [serial online] 2012 [cited 2019 Aug 24];4:114-9. Available from: http://www.jgid.org/text.asp?2012/4/2/114/96776



   Introduction Top


Insecticides have been the primary method of controlling disease vectors and agricultural pests for many decades. While insect resistance to pesticides has been described for decades as well, there has been a dramatic increase in resistance in recent years. [1] The relationship between resistance and insecticides has commonly been assumed to be a direct one. [1],[2],[3] In addition, the presence and persistence of chemical residues in soil and water have been detected and their impacts on aquatic fauna, including insecticide resistance of immature vector stages, have been documented. [4],[5] Recent studies corroborated these assumptions by demonstrating a strong relationship between the resistance level in Anopheles species and the pesticide uses in crops, especially in areas with cotton and vegetable production. [6],[7],[8] In addition, metabolic resistance due to the introduction of xenobiotics in aquatic larval habitats was documented in a strain of Aedes aegypti. [9]

The preferential breeding sites for Anopheles arabiensis are rice fields and the feeding behavior of this species is largely exophilic and zoophilic. [10] In northern Tanzania, a variety of pesticides and other chemicals are sprayed by pest control services in agriculture such as organochlorides such as Dichlorodiphenyltrichloroethane (DDT) and dieldrin and in public health and veterinary pyrethroid-based insecticides such as permethrin and deltamethrin. [11] These are applied in rice fields once every 3 months (i.e., January, April, July, and October) following the rice irrigation cycles. These applications rarely exceed 10 times a year for other crops. [11] The presence of dieldrin, γ-HCH (lindane), and DDT residues in water and in soil have been reported in northern Tanzania,[12] more specifically in the rice-irrigated areas of lower Moshi where low levels of the three compounds were found in both water and soil. [12] In contrast, malaria vector control in this area has relied exclusively on conventional insecticide treatments and long-lasting insecticide-treated nets impregnated with pyrethroids. This strategy seems to limit the development of resistance in Anopheles species [13] compared with insecticide spraying. [14] Pyrethroids are also used in the region for veterinary purposes against ticks and tsetse flies in livestock and other domesticated animals. [10]

A major concern on the use of pyrethroids, especially in long lasting insecticides treated bed nets (LLITNs) and conventionally insecticides treated bed nets (ITNs), [15],[16] is the lack of proper surveillance of the knockdown resistance (kdr) mutation that confers cross-resistance to both pyrethroids and DDT. The kdr mutations are known to exhibit seasonal variations throughout studies conducted in other parts of East Africa. [13],[17] These variations have been attributed to several factors including interaction of vector populations with insecticide residues within the ecosystem. In order to better implement vector control strategies, resistance levels in An. arabiensis from areas utilizing rice irrigation schemes in the lower Moshi area have been evaluated using WHO susceptibility tests [18] to monitor the presence of kdr mutations [19] and to evaluate the biochemical mechanisms of resistance. [20] The previous studies showed high susceptibility in Anopheles populations to pyrethroids, a low frequency of kdr mutation (0.16%) and highly elevated oxidases and beta-esterase enzymes. [18],[19],[20],[21] The kdr mutation was a substitution of a leucine by a phenylalanine in position 1014 of the sodium channel domain II segment 6 gene (L1014P). However, the most widespread kdr mutation in An. gambiae sensu stricto and An. arabiensis in East African populations is a substitution of a leucine by a serine in position 1014 (L1014S). [14],[22] The L1014P mutation also exists at low frequencies in Kenya [13] and Uganda. [17],[22]

The exposure of An. arabiensis to insecticides could occur at the larval stage where they come in contact with freshly sprayed or persistent molecules in the breeding sites and at the adult stage through contact with pesticides used in agriculture or during veterinary, medical, or domestic use. [2],[4] Therefore, this study aimed at utilizing longitudinal monitoring of kdr and rdl alleles due to a reported reduction in An. gambiae sensu lato susceptibility to permethrin and other pyrethroids [18],[21] and a low kdr frequency in a cross-sectional study in this study area. [19] Due to cyclodiene residues being found in soil and water within the lower Moshi area, the dieldrin (rdl) locus of the GABA receptor, the main target for cyclodiene compounds, was genotyped.


   Materials and Methods Top


Study area description

The study site was located in lower Moshi in the Kilimanjaro region of the northern Tanzania in an area utilizing a rice irrigation scheme (3°21′S, 37°21′E). A more detailed description of the study area can be found elsewhere. [23] Meteorological data were obtained from the Kilimanjaro International Airport Meteorological Station.

Species density variation

Mosquitoes were collected from 20 houses by using standard CDC-miniature light trap collections as described previously. [24] The collections were done fortnightly for 14 months from July 2005 to August 2006. Anopheles gambiae s.l. were identified morphologically by using the standard key. [25]

Sporozoite detection and entomological inoculation rate

Mosquito sporozoite detection utilized the enzyme-linked immunosorbent assay (ELISA) using the protocol of Wirtz et al. [26] The annual entomological inoculation rate (EIR) was calculated by using the formula published in a previous work [27] for light trap collections: 1.605 × (number of sporozoite-positive mosquitoes detected by ELISA/number of mosquitoes tested) × (number of mosquitoes collected/number of collections performed) × 365.

DNA extraction

DNA was extracted from legs of 535 individual mosquitoes by using DNA Easy Kit (Qiagen, Valencia, CA, USA) according to the manufacturer protocol for insects. DNA was eluted in a 200 μl volume.

Mosquito identification method

The polymerase chain reaction (PCR) protocol was used to perform the amplification of DNA for species identification and other molecular use. [28] Five microliters of DNA extract were amplified in a 25 μl PCR mix containing 1× Taq buffer (Qiagen, Valencia, CA, USA), 2 mM of MgCl 2 , 0.2 mM of each dNTP, 0.5 ng/μl of primer UN [5-GTG TGC CCC TTC CTC GAT GT-3′], 0.25 ng/μl of primer GA [5′-CTGGTTTGGTCGGCACGTTT-3′], 0.73 ng/μl of primer AR [5′-AAGTGTCCTTCTCCATCCTA-3′], 1 ng/μl primer QD [5′-CAGACCAAGATGGTTAGTAT-3′], 0.5ng/μl primer ME [5′-TGACCAACCCACTCCCTTGA-3′], and 0.05 U/μl HotstartTaq polymerase (Qiagen, Valencia, CA, USA). The PCR was carried out with an initial step of 10 min at 94°C to activate the DNA polymerase followed by 30 cycles, each consisting of 5 min denaturation at 94°C, 30 s annealing at 50°C, and 30 s extension at 72°C; the final cycle products were extended for 10 min at 72°C. Fragments were run through an ethidium bromide 2% agarose gel and photographed under ultraviolet light illumination.

Knockdown ( kd ) allele detection

This procedure was based on a developed PCR protocol for the detection of the kdr mutation (L1014S) in East African An. gambiae complex mosquitoes. [29] Five microliters of DNA extract were amplified in a 15 μl PCR mix containing 1× Taq buffer (Qiagen, Valencia, CA, USA), 2.5 mM of MgCl 2 , 0.2 mM of each dNTP, 0.3 ng/μl of primer Agd1 [5′-ATAGATTCCCCGACCATG-3′] and Agd2 [5'-AGACAAGGATGATGAACC-3'], 0.5 ng/μl of primer Agd4 [5′-CTGTAGTGATAGGAAATTTA-3′] and Agd5 [5′-TTTGCATTACTTACGACTG-3′], and 0.05 U/μl HotstartTaq polymerase (Qiagen, Valencia, CA, USA). PCR was carried out with an initial step of 10 min at 95°C to activate the DNA polymerase followed by 35 cycles, each consisting of 25 s denaturation at 94°C, 20 s annealing at 55°C, and 8 s extension at 72°C. The final cycle products were extended for 10 min at 72°C. Fragments were run through an ethidium bromide 2% agarose gel and photographed under ultraviolet light illumination. A total of 535 mosquitoes were tested.

Rdl mutation detection

This procedure was based on a developed PCR protocol. [30] Five microliters of DNA extract were amplified in a 25 μl PCR mix containing 1× Taq buffer (Qiagen, Valencia, CA, USA), 1.5 mM of MgCl 2 , 0.2 mM of each dNTP, 0.04 ng/μl of primer RdlF [5′-AGTTTGTACGTTCGATGGGTTA-3′], RdlR [5′-CCAGCAGACTGGCAAATACC-3], AARdl [5′-GCTACACCAGCACGTGATT-3′] and RdlSS [5′-CAAGACAGTAGTTACACCTAAAGC-3′], and 0.05U/μl HotstartTaq polymerase (Qiagen, Valencia, CA, USA). PCR was carried out with an initial step of 10 min at 95°C to activate the DNA polymerase followed by 35 cycles, each consisting of 45 s denaturation at 94°C, 45 s annealing at 53°C, and 45 s extension at 72°C; the final cycle products were extended for 10 min at 72°C. Fragments were run through an ethidium bromide 2% agarose gel and photographed under ultraviolet light illumination. A total of 535 mosquitoes were tested.

Ethical consideration

The ethical clearance was given by Kilimanjaro Christian Medical College of Tumaini University. Written consent was given to all participants whose houses were involved in this study for mosquitoes sampling by using CDC miniature light traps.


   Results Top


Species identification, density variation, and entomological inoculation rate

A total of 6220 mosquitoes were collected that comprised the following species: 5350 (86.0%) An. gambiae s.l. and 870 (14.0%) Culex spp. Out of 5350 An. gambiae s.l. collected, 10% (n=535) was randomly sampled each month and subjected to species identification. Within that population, 99.8% (n=534) were identified by PCR to be An. arabiensis and 0.2% (n=1) was identified as An. gambiae s.s. The population of mosquitoes sampled changed from 400 mosquitoes in July 2005 to 679 mosquitoes in August 2006 [Table 1]. The study started at the end of rainy season, resulting in the low numbers of mosquitoes at the beginning of the study. The mosquito numbers subsequently increased with the start of rice-growing season and the short rains that occurred in late November 2005 and long rains that started in late February 2006. Among 535 mosquitoes identified, 19 (3.5%) of the An. arabiensis were found to be circumsporozoite protein positive. This resulted in an annual EIR of 0.54 ib/trap/year.
Table 1: An. gambiae s.l. densities and circumsporozoite protein ELISA results throughout the study period

Click here to view


Yearly fluctuations in mutation point resistance

Mutation points were detected in 477 of the 534 An. arabiensis, which were successfully genotyped for kdr 1014S and rdl based on diagnostic PCR results. No samples tested positive for the knockdown resistance mutation L1014S of the sodium channel gene. However, the rdl locus mutation was found with a resistant allele frequency of 0.48 throughout the 14 months of study. In monthly assessments, the resistant allele frequencies dropped from 0.73 and 0.70 in July and August 2005, respectively, to 0.31 and 0.32 for the same period in 2006. During this 14-month period, heterozygote proportions (standard deviation) were 33.13% (19.9) for RR (homozygote resistant), 28.88% (18.15) for SS (homozygote susceptible), and 37.99% (10.37) for RS (heterozygote resistant). However, throughout the year, the rdl genotype proportions fluctuated. The proportion of homozygote-resistant genotype (RR) decreased from 57 and 48% in July and August 2005, respectively, to 15 and 12% during the same period in 2006. In contrast, homozygote-susceptible genotypes (SS) increased from 11 and 7% in July and August 2005 to 51 and 47% the following year. Heterozygote proportions (RS) showed a stable pattern varying from 31 and 45% to 34 and 40% between July/August 2005 and July/August 2006 [Figure 1]. No direct relationships were observed between these genotype fluctuations and climatic factors or insecticide use in rice fields. Among the 19 specimens found positive for Plasmodium falciparum circumsporozoite protein, 7 were RR, 4 were RS, and 8 were SS. In parallel evaluations, permethrin susceptibility among wild population of the An. arabiensis in this study area was monitored from January 2005 to August 2006 and seemed to have seasonal variation in mosquitoes' mortality and knockdown percentage [Figure 2].
Figure 1: The proportion of genotypes at the rdl locus from July 2005 to August 2006 among An. arabiensis

Click here to view
Figure 2: Variation in permethrin susceptibility among wild population of An. arabiensis in lower Moshi, 2005-2006

Click here to view



   Discussion Top


Although previous studies reported only An. arabiensis[31],[32] in this rice-growing region of lower Moshi, Tanzania, this report demonstrates that An. arabiensis and An. gambiae s.s. are both present in this region. This is the first observation that An. gambiae s.s. is also present in lower Moshi. It was not observed in previous studies, but arguably it might be due to climate change and land-use practice changes.

Finding rdl genes in mosquitoes shows that residues of insecticides are present in the environment and likely exposed the developmental stages, confirming a previous report. [12] In addition, the absence of the L1014S kdr mutation was confirmed, along with low EIRs as previously reported for this region. [19],[33],[34] The result of this study suggests the possibility that insecticide residues in soil may have either direct or indirect impact on the development of insecticide resistance documented in other sites. [2],[6]

In this same study site, metabolic resistance is known to be a major reason for reduced permethrin susceptibility among adult mosquitoes. [20] Variation of permethrin tolerance done in previous years [Figure 2] were shown to deviate within months of the years. Insecticides used for agricultural activities may have contributed to this resistance since our results show a significant increase in the mutated rdl allele along with yearly variations in the An. arabiensis population. This mutation is known to confer resistance to dieldrin, endosulfan, and lindane, all of which are used in agriculture and are found in water, sediment, and soil in the Moshi area. [12] In western Africa, a strong association was found between insecticide resistance in mosquitoes and the use of agricultural pesticides. [35] The resistant allele frequency at the rdl locus was found to decrease during the 14 months of the collection along with the genotype RR and an increase in genotype SS proportions. These findings suggest that the use of agricultural insecticides should be taken in consideration by public health disease vector control officials since pesticide residues in the soil contributes to the spread of resistance among disease vectors. The variations in rdl homozygote and heterozygote alleles have imparted a tolerance for dieldrin among mosquitoes in the rice-growing region in lower Moshi.

The Abuja declaration aims to cover 60% of the population living in malaria endemic areas of Africa with insecticide-treated bed nets by the end of 2010. [36] The absence of both West and East African kdr resistances in lower Moshi allows for longer performance time for pyrethroid-treated bed nets (conventionally made and/or industrially treated) and long-lasting insecticide-treated nets (LLITNs) to continue their ability to kill mosquitoes. ITNs and LLITNs show efficacy in most areas of Tanzania and other parts of Africa. [37] The active surveillance of the L1014P kdr mutation should be maintained in the years to come as part of the vector control program in lower Moshi and in similar agro-ecosystems. An. arabiensis is both zoophilic and exophilic in our study area. [10] The implementation of an active zoophylaxis is necessary as a complementary part of vector control to lower the EIR. It is therefore a viable vector control method to attract mosquitoes away from human dwellings to animals, resulting in an EIR lower than 0.54 ib/person/trap/year observed during the study.


   Conclusion Top


The findings of this study suggests that agricultural, veterinary, and public health workers need to minimize pesticide residues waste in soil to prevent contaminations of the mosquito larval habitats and subsequently the evolution of resistance in malaria vectors against pesticides used for public health that have similar ingredients to those used in agriculture and veterinary services.


   Acknowledgements Top


The authors wish to thank the villagers of lower Moshi who are residents in irrigation schemes for allowing mosquito sampling to be conducted in their homes. Belgium Technical Cooperation (BTC) in Tanzania is gratefully acknowledged for providing funds for the field activities. The vector control project at Kilimanjaro Christian Medical Centre is highly acknowledged for transport assistance. The authors wish to thank Mr. Charles Massenga and Mr. Augustine Mtui for their active participation in the collection and field identification of mosquitoes.

 
   References Top

1.Hemingway J, Field L, Vontas J. An overview of insecticide resistance. Science 2002; 298:96-7.  Back to cited text no. 1
    
2.Akogbéto M, Yakoubou S. Resistance of malaria vectors to pyrethrins used for impregnating mosquito nets in Benin, West Africa. Bull Soc Pathol Exot. 1999;92:123-30.  Back to cited text no. 2
    
3.Diabate A, Baldet T, Chandre F, Guiguemde RT, Brengues C, Guillet P, et al. First report of the kdr mutation in Anopheles gambiae M form from Burkina Faso, west Africa. Parassitologia 2002; 44:157-8.  Back to cited text no. 3
    
4.Jan MR, Shah J, Khawaja MA, Gul K. DDT residue in soil and water in and around abandoned DDT manufacturing factory. Environ Monit Assess 2009; 155:31-8.  Back to cited text no. 4
    
5.Mandocdoc M, David CP. Dieldrin contamination of the groundwater in a former US military base (Clark Air Base, Philippines). Clean Soil Air Water 2008; 36:870-4.  Back to cited text no. 5
    
6.Akogbeto MC, Djouaka R, Noukpo H. Use of agricultural insecticides in Benin. Bull Soc Pathol Exot 2005; 98:400-5.  Back to cited text no. 6
    
7.Chouaibou M, Etang J, Brevault T, Nwane P, Hinzoumbe CK, Mimpfoundi R, et al. Dynamics of insecticide resistance in the malaria vector Anopheles gambiae s.l. from an area of extensive cotton cultivation in Northern Cameroon. Trop Med Int Health 2008; 13:476-86.  Back to cited text no. 7
    
8.Dusfour I, Achee NL, Briceno I, King R, Grieco JP. Comparative data on the insecticide resistance of Anopheles albimanus in relation to agricultural practices in northern Belize, CA. J Pest Sci 2010; 83:41-6.  Back to cited text no. 8
    
9.Poupardin R, Reynaud S, Strode C, Ranson H, Vontas J, David JP. Cross-induction of detoxification genes by environmental xenobiotics and insecticides in the mosquito Aedes aegypti: impact on larval tolerance to chemical insecticides. Insect Biochem Mol Biol 2008;38:540-51.  Back to cited text no. 9
    
10.Mahande A, Mosha F, Mahande J, Kweka E. Feeding and resting behaviour of malaria vector, Anopheles arabiensis with reference to zooprophylaxis. Malar J 2007; 6:100.  Back to cited text no. 10
    
11.Ngowi AV, Mbise TJ, Ijani AS, London L, Ajayi OC. Pesticides use by smallholder farmers in vegetable production in Northern Tanzania. Crop Prot 2007; 26:1617-24.  Back to cited text no. 11
    
12.Kishimba MA, Henry L, Mwevura H, Mmochi AJ, Mihale M, Hellar H. The status of pesticide pollution in Tanzania. Talanta 2004; 64:48-53.  Back to cited text no. 12
    
13.Stump AD, Atieli FK, Vulule JM, Besansky NJ. Dynamics of the pyrethroid knockdown resistance allele in western Kenyan populations of Anopheles gambiae in response to insecticide-treated bed net trials. Am J Trop Med Hyg 2004; 70:591-6.  Back to cited text no. 13
    
14.Protopopoff N, Verhaeghen K, Van Bortel W, Roelants P, Marcotty T, Baza D, et al. A significant increase in kdr in Anopheles gambiae is associated with an intensive vector control intervention in Burundi highlands. Trop Med Int Health 2008; 13:1479-87.  Back to cited text no. 14
    
15.Czeher C, Labbo R, Arzika I, Duchemin JB. Evidence of increasing Leu-Phe knockdown resistance mutation in Anopheles gambiae from Niger following a nationwide long-lasting insecticide-treated nets implementation. Malar J 2008; 7:189.  Back to cited text no. 15
    
16.Dabire RK, Diabate A, Baldet T, Pare-Toe L, Guiguemde RT, Ouedraogo JB, et al. Personal protection of long lasting insecticide-treated nets in areas of Anopheles gambiae s.s. resistance to pyrethroids. Malar J 2006; 5:12.  Back to cited text no. 16
    
17.Verhaeghen K, Bortel WV, Roelants P, Okello PE, Talisuna A, Coosemans M. Spatio-temporal patterns in kdr frequency in permethrin and DDT resistant Anopheles gambiae s.s. from Uganda. Am J Trop Med Hyg 2010; 82:566-73.  Back to cited text no. 17
    
18.Mosha FW, Lyimo IN, Oxborough RM, Matowo J, Malima R, Feston E, et al. Comparative efficacies of permethrin-, deltamethrin-and alpha-cypermethrin-treated nets, against Anopheles arabiensis and Culex quinquefasciatus in northern Tanzania. Ann Trop Med Parasitol 2008; 102:367-76.  Back to cited text no. 18
    
19.Kulkarni MA, Rowland M, Alifrangis M, Mosha FW, Matowo J, Malima R, et al. Occurrence of the leucine-to-phenylalanine knockdown resistance (kdr) mutation in Anopheles arabiensis populations in Tanzania, detected by a simplified high-throughput SSOP-ELISA method. Malar J 2006; 5:56.  Back to cited text no. 19
    
20.Matowo J, Kulkarni MA, Mosha FW, Oxborough RM, Kitau JA, Tenu F, et al. Biochemical basis of permethrin resistance in Anopheles arabiensis from Lower Moshi, north-eastern Tanzania. Malar J 2010; 9:193.  Back to cited text no. 20
    
21.Kulkarni M, FW Mosha, Rowland M, Kweka E, Temu E, Rau M, et al. Reduced permethrin susceptibility of Anopheles arabiensis from an irrigated rice growing area in northern Tanzania [In Press].  Back to cited text no. 21
    
22.Verhaeghen K, Van Bortel W, Roelants P, Backeljau T, Coosemans M. Detection of the East and West African kdr mutation in Anopheles gambiae and Anopheles arabiensis from Uganda using a new assay based on FRET/Melt Curve analysis. Malar J 2006; 5:16.  Back to cited text no. 22
    
23.Kweka EJ, Mwang'onde BJ, Kimaro E, Msangi S, Massenga CP, Mahande AM. A resting box for outdoor sampling of adult Anopheles arabiensis in rice irrigation schemes of lower Moshi, northern Tanzania. Malar J 2009; 8:82.  Back to cited text no. 23
    
24.WHO: Manual on practical entomology in malaria. Part II. Methods and Techniques: Division of Malaria and Other Parasitic Diseases, Geneva: 1975.  Back to cited text no. 24
    
25.Gillies TM, Coetzee M. Supplement of the Anopheles of Africa South of Sahara (Afrotropical Region), vol. 55. Johannesburg Republic of South Africa Publication of The South Africa Institute of Medical Research; 1987.  Back to cited text no. 25
    
26.Wirtz RA, Burkot TR, Graves PM, Andre RG. Field evaluation of enzyme-linked immunosorbent assays for Plasmodium falciparum and Plasmodium vivax sporozoites in mosquitoes (Diptera: Culicidae) from Papua New Guinea. J Med Entomol 1987; 24:433-7.  Back to cited text no. 26
    
27.Lines JD, Curtis CF, Wilkes T, Njunwa T. Monitoring human biting mosquitoes in Tanzania with light traps hung beside mosquito nets. Bull Entomol Res 1991; 81:77-84.  Back to cited text no. 27
    
28.Scott JA, Brogdon WG, Collins FH. Identification of single specimens of the Anopheles gambiae complex by the polymerase chain reaction. Am J Trop Med Hyg 1993; 49:520-9.  Back to cited text no. 28
    
29.Ranson H, Jensen B, Wang X, Prapanthadara L, Hemingway J, Collins FH. Genetic mapping of two loci affecting DDT resistance in the malaria vector Anopheles gambiae. Insect Mol Biol 2000; 9:499-507.  Back to cited text no. 29
    
30.Wilkins EE, Howell PI, Benedict MQ. IMP PCR primers detect single nucleotide polymorphisms for Anopheles gambiae species identification, Mopti and Savanna rDNA types, and resistance to dieldrin in Anopheles arabiensis. Malar J 2006; 5:125.  Back to cited text no. 30
    
31.Mnzava AE, Kilama WL. Observations on the distribution of the Anopheles gambiae complex in Tanzania. Acta Trop 1986; 43:277-82.  Back to cited text no. 31
    
32.Temu EA, Minjas JN, Coetzee M, Hunt RH, Shift CJ. The role of four anopheline species (Diptera: Culicidae) in malaria transmission in coastal Tanzania. Trans R Soc Trop Med Hyg 1998;92:152-8.  Back to cited text no. 32
    
33.Ijumba JN, Mosha FW, Lindsay SW. Malaria transmission risk variations derived from different agricultural practices in an irrigated area of northern Tanzania. Med Vet Entomol 2002; 16:28-38.  Back to cited text no. 33
    
34.Kulkarni MA, Kweka E, Nyale E, Lyatuu E, Mosha FW, Chandramohan D, et al. Entomological evaluation of malaria vectors at different altitudes in Hai district, northeastern Tanzania. J Med Entomol 2006; 43:580-8.  Back to cited text no. 34
    
35.Yadouleton AW, Asidi A, Djouaka RF, Braima J, Agossou CD, Akogbeto MC. Development of vegetable farming: A cause of the emergence of insecticide resistance in populations of Anopheles gambiae in urban areas of Benin. Malar J 2009; 8:103.  Back to cited text no. 35
    
36.Rugemalila JB, Wanga CL, Kilama WL. Sixth Africa Malaria Day in 2006: How far have we come after the Abuja Declaration? Malar J 2006; 5:102.  Back to cited text no. 36
    
37.Malima RC, Magesa SM, Tungu PK, Mwingira V, Magogo FS, Sudi W, et al. An experimental hut evaluation of Olyset nets against anopheline mosquitoes after seven years use in Tanzanian villages. Malar J 2008; 7:38.  Back to cited text no. 37
    

Top
Correspondence Address:
Eliningaya J Kweka
Division of Livestock and Human Diseases Vector Control, Mosquito Section, Tropical Pesticides Research Institute, Arusha, Tanzania

Login to access the Email id

Source of Support: Belgium Technical Cooperation, Belgium Embassy Tanzania., Conflict of Interest: None


DOI: 10.4103/0974-777X.96776

Rights and Permissions


    Figures

  [Figure 1], [Figure 2]
 
 
    Tables

  [Table 1]

This article has been cited by
1 Experimental hut and bioassay evaluation of the residual activity of a polymer-enhanced suspension concentrate (SC-PE) formulation of deltamethrin for IRS use in the control of Anopheles arabiensis
Richard M Oxborough,Jovin Kitau,Rebecca Jones,Franklin W Mosha,Mark W Rowland
Parasites & Vectors. 2014; 7(1)
[Pubmed] | [DOI]
2 Identification of Proteasome Subunit Beta Type 6 (PSMB6) Associated with Deltamethrin Resistance in Mosquitoes by Proteomic and Bioassay Analyses
Sun, L. and Ye, Y. and Sun, H. and Yu, J. and Zhang, L. and Sun, Y. and Zhang, D. and Ma, L. and Shen, B. and Zhu, C.
PLoS ONE. 2013; 8(6)
[Pubmed]
3 High level of resistance in the mosquito Anopheles gambiae to pyrethroid insecticides and reduced susceptibility to bendiocarb in north-western Tanzania
Natacha Protopopoff,Johnson Matowo,Robert Malima,Reginald Kavishe,Robert Kaaya,Alexandra Wright,Philippa A West,Immo Kleinschmidt,William Kisinza,Franklin W Mosha,Mark Rowland
Malaria Journal. 2013; 12(1): 149
[Pubmed] | [DOI]
4 Social economic factors and malaria transmission in Lower Moshi, Northern Tanzania
Asanterabi Lowassa,Humphrey D Mazigo,Aneth M Mahande,Beda J Mwang’onde,Shandala Msangi,Michael J Mahande,Epiphania E Kimaro,Eliapenda Elisante,Eliningaya J Kweka
Parasites & Vectors. 2012; 5(1): 129
[Pubmed] | [DOI]
5 Protective efficacy of menthol propylene glycol carbonate compared to N, N-diethyl-methylbenzamide against mosquito bites in Northern Tanzania
Eliningaya J Kweka,Stephen Munga,Aneth M Mahande,Shandala Msangi,Humphrey D Mazigo,Araceli Q Adrias,Jonathan R Matias
Parasites & Vectors. 2012; 5(1): 189
[Pubmed] | [DOI]



 

Top
  
 
  Search
 
  
    Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
    Email Alert *
    Add to My List *
* Registration required (free)  


    Abstract
   Introduction
    Materials and Me...
   Results
   Discussion
   Conclusion
   Acknowledgements
    References
    Article Figures
    Article Tables

 Article Access Statistics
    Viewed2657    
    Printed139    
    Emailed0    
    PDF Downloaded20    
    Comments [Add]    
    Cited by others 5    

Recommend this journal

Sitemap | What's New | Feedback | Copyright and Disclaimer | Contact Us
© 2008 Journal of Global Infectious Diseases | Published by Wolters Kluwer - Medknow
Online since 10th December, 2008