Impregnating hessian strips with the volatile pyrethroid transfluthrin prevents outdoor exposure to vectors of malaria and lymphatic filariasis in urban Dar es Salaam, Tanzania

Particle and Fibre Toxicology

Gerry Killeen³  Prosper P. Chaki²  John Paliga²  Sheila B. Ogoma¹  Nicodem J. Govella² 

[1] US Army Medical Research Unit Kenya-Walter Reed Project, Kisumu, Kenya;Ifakara Health Institute, Environmental Health and Ecological Sciences Thematic Group, Coordination Office, Kiko Avenue, Mikocheni, Dar es Salaam, United Republic of Tanzania;Department of Vector Biology, Liverpool School of Tropical Medicine, Pembroke Place, Liverpool L3 5QA, United Kingdom

关键词: Diversion;    Vector control;    Hessian strip;    Transfluthrin;    Repellent;    Outdoor transmission;    Mosquitoes;    Malaria;    Filariasis;   

Others  :  1224199
DOI  :  10.1186/s13071-015-0937-8

 received in 2015-01-20, accepted in 2015-06-03,  发布年份 2015

【 摘 要 】

Background

Semi-field trials using laboratory-reared Anopheles arabiensis have shown that, delivering the volatile pyrethroid transfluthrin by absorption into hessian strips, consistently provided > 99 % human protective efficacy against bites for 6 months without retreating. Here the impact of this approach upon human exposure to wild populations of vectors for both malaria and filariasis under full field conditions is assessed for the first time.

Methods

Transfluthrin-treated and untreated strips were placed around human volunteers conducting human landing catch in an outdoor environment in urban Dar es Salaam, where much human exposure to malaria and filariasis transmission occurs outdoors. The experiment was replicated 9 times at 16 outdoor catching stations in 4 distinct locations over 72 working nights between May and August 2012.

Results

Overall, the treated hessian strips conferred 99 % protection against An. gambiae (1 bite versus 159) and 92 % protection against Culex spp. (1478 bites versus 18,602). No decline in efficacy over the course of the study could be detected for the very sparse populations of An. gambiae (P = 0.32) and only a slow efficacy decline was observed for Culex spp. (P < 0.001), with protection remaining satisfactory over 3 months after strip treatment. Diversion of mosquitoes to unprotected humans in nearby houses was neither detected for An. gambiae (P = 0.152) nor for Culex spp. (Relative rate, [95 % CI] = 1.03, [0.95, 1.11], P = 0.499).

Conclusion

While this study raises more questions than it answers, the presented evidence of high protection over long periods suggest this technology may have potential for preventing outdoor transmission of malaria, lymphatic filariasis and other vector-borne pathogens.

【 授权许可】

   
2015 Govella et al.

【 图 表 】

Fig. 1.

Fig. 2.

【 参考文献 】

• [1]De Silva PM, Marshall JM. Factors contributing to urban malaria transmission in sub-Saharan Africa: a systematic review. J Trop Med. 2012; 2012:1-10.
• [2]Roberts V, Macintyre K, Keating J, Trape J-F, Duchemin J-B, Warren M et al.. Malaria transmission in sub-Saharan Africa. Am J Trop Med Hyg. 2003; 68:169-76.
• [3]Pedersen EM, Mukoko DA. Impact of insecticide-treated materials on filaria transmission by the various species of vector mosquito in Africa. Ann Trop Med Parasitol. 2002; 96 Suppl 2:S91-5.
• [4]Bockarie MJ, Pedersen EM, White GB, Michael E. Role of vector control in the global program to eradicate lymphatic filariasis. Ann Rev Entomol. 2009; 54:469-87.
• [5]Simonsen PE, Malecela MN, Michael E, Mackenzie CD. Lymphatic filariasis research and control in Eastern and Southern Africa. DBL-Centre for Health Research and Development. 2008.
• [6]Global Programme to Eliminate Lymphatic Filariasis. Lymphatic Filariasis: Practical Entomology. WHO, Geneva; 2013.
• [7]WHO. World Malaria Report 2014. In.: World Health Organization.
• [8]Simonsen PE, Pedersen EM, Rwegoshora RT, Malecela MN, Derua YA, Magesa SM. Lymphatic filariasis control in Tanzania: effect of repeated mass drug administration with Ivermectin and Albendazole on infection and transmission. PLoS Negl Trop Dis. 2010; 4:e696.
• [9]Sunish IP, Rajendran R, Mani TR, Munirathinam A, Dash AP, Tyagi BK. Vector control complements mass drug administration against bancroftian filariasis in Tirukoilur, India. Bull World Health Org. 2007; 85:138-45.
• [10]Durnez L, Mao S, Denis L, Roelants P, Sochantha T, Coosemans M. Outdoor malaria transmission in forested villages of Cambodia. Malar J. 2013; 12:329. BioMed Central Full Text
• [11]Killeen GF. Characterizing, controlling and eliminating residual malaria transmission. Malar J. 2014; 13:330. BioMed Central Full Text
• [12]Govella NJ, Ferguson H. Why use of interventions targeting outdoor biting mosquitoes will be necessary to achieve malaria elimination. Front Physiol. 2012; 3:1-5.
• [13]Moiroux N, Gomez MB, Pennetier C, Elanga E, Djenontin A, Chandre F et al.. Changes in Anopheles funestus biting behavior following universal coverage of long-lasting insecticidal nets in Benin. J Infect Dis. 2012; 206:1622-9.
• [14]Sougoufara S, Diedhiou SM, Doucoure S, Diagne N, Sembene PM, Harry M et al.. Biting by Anopheles funestus in broad daytime after use of long-lasting insecticidal nets: a new challenge to malaria control. Malar J. 2014; 13:125. BioMed Central Full Text
• [15]Yohannes M, Boelee E. Early biting rhythm in the Afro-tropical vector of malaria, Anopheles arabiensis and challenges for its control in Ethiopia. Med Vet Entomol. 2012; 26:103-5.
• [16]Govella NJ, Okumu FO, Killeen GF. Insecticide-treated nets can reduce malaria transmission by mosquitoes which feed outdoors. Am J Trop Med Hyg. 2010; 82(3):415-9.
• [17]Geissbühler Y, Chaki P, Emidi B, Govella NJ, Shirima R, Mayagaya V et al.. Interdependence of domestic malaria prevention measures and mosquito-human interactions in urban Dar es Salaam, Tanzania. Malar J. 2007; 6:126. BioMed Central Full Text
• [18]Russell TL, Beebe NW, Cooper RD, Lobo NF, Burkot TR. Successful malaria elimination strategies require interventions that target changing vector behaviours. Malar J. 2013; 12:56. BioMed Central Full Text
• [19]Moutinho PR, Gil LHS, Cruz RB, Ribolla EM. Population dynamics, structure and behaviour of Anopheles darlingi in a rural settlement in the Amazon rainforest of Acre, Brazil. Malar J. 2011; 10:174. BioMed Central Full Text
• [20]Moiroux N, Damien GB, Egrot M, Djenontin A, Chandre F, Corbel V. Human exposure to early morning Anopheles funestus biting behavior and personal protection provided by long-lasting insecticidal nets. PLoS One. 2014; 9(8): Article ID e104967
• [21]Gryseels C, Durnez L, Gerrets R, Uk S, Suon S, Set S et al.. Re-imagining malaria: heterogeneity of human and mosquito behaviour in relation to residual malaria transmission in Cambodia. Malar J. 2015; 14:165. BioMed Central Full Text
• [22]Govella NJ, Chaki PP, Killeen GF. Entomological surveillance of behavioural resilience and resistance in residual malaria vector populations. Malar J. 2013; 12:124. BioMed Central Full Text
• [23]Killeen GF, Chitnis N. Potential causes and consequences of behaviural resilience and resistance in malaria vector populations: a mathematical modelling analysis. Malar J. 2014; 13:97. BioMed Central Full Text
• [24]Briet OJT, Chitnis N. Effects of changing mosquito host searching behaviours on the cost effectiveness of a mass distribution of long-lasting, insecticidal nets: a modelling study. Malar J. 2013; 12:215. BioMed Central Full Text
• [25]Achee NL, Bangs MJ, Farlow R, Killeen GF, Lindsay S, Logan JG JMS et al.. Spatial repellents: from discovery and development to evidence-based validation. Malar J. 2012; 11:164. BioMed Central Full Text
• [26]Killeen GF, Chitnis N, Moore SJ, Okumu FO. Target product profile choices for intra-domiciliary malaria vector pesticide products: repel or kill. Malar J. 2011; 10:207. BioMed Central Full Text
• [27]Pates HV, Line JD, Keto AJ, Miller JE. Personal protection against mosquitoes in Dar es Salaam, Tanzania, by using a kerosene oil lamp to vaporize transfluthrin. Med Vet Entomol. 2002; 16:277-84.
• [28]Kawada H, Maekawa Y, Tsuda S, Takagi M. Trial of spatial repellency of metofluthrin-impregnated paper strips in shelters without walls in Lombok island in Indonesia. J Am Mosq Control Assoc. 2004; 20:434-7.
• [29]Kawada H, Maekawa Y, Takagi M. Field trial on the spatial repellency of metofluthrin-impregnated plastic strips for mosquitoes in shelters without walls in Lombok, Indonesia. J Vector Ecol. 2005; 30:181-5.
• [30]Ogoma SB, Ngonyani H, Simfukwe ET, Mseka A, Moore J, Killeen GF. Spatial repellency of transfluthrin-treated hessian strips against laboratory-reared Anopheles arabiensis mosquitoes in a semi-field tunnel cage. Parasit Vectors. 2012; 5:54. BioMed Central Full Text
• [31]Majambere S, Masue D, Mlacha Y, Govella NJ, Magesa SM, Killeen GF. Advantages and limitations of commercially available electrocuting grids for studying mosquito behaviour. Parasit Vectors. 2013; 6:53. BioMed Central Full Text
• [32]Kabula B, Tungu PK, Matowo J, Kitau J, Mweya C, Emidi B et al.. Susceptibility status of malaria vectors to insecticides commonly used for malaria control in Tanzania. Trop Med Int Health. 2012; 17(6):742-50.
• [33]Kabula B, Tungu PK, Malima RC, Rowland MW, Minja J, Wililo R et al.. Distribution and spread of pyrethroid and DDT resistance among the Anopheles gambiae complex in Tanzania. Med Vet Entomol. 2013; 28:1-9.
• [34]Maheu-Giroux M, Castro MC. Impact of community-based larviciding on the prevalence of malaria infection in Dar es Salaam, Tanzania. PLoS One. 2013; 8(8):e71638.
• [35]Ogoma SB, Kannady K, Sikulu M, Chaki PP, Govella NJ, Mukabana WR et al.. Window screening, ceilings and closed eavesas sustainable ways to control malaria in Dar es Salaam, Tanzania. Malar J. 2009; 8:221. BioMed Central Full Text
• [36]Geissbühler Y, Kannady K, Chaki PP, Emidi B, Govella NJ, Mayagaya V et al.. Microbial larvicide application by a large-scale, community-based program reduces malaria infection prevalence in Urban Dar Es Salaam, Tanzania. PLoS One. 2009; 4:e 5107.
• [37]Huho B, Briet OJT, Seyoum A, Sikala C, Bayoh N, Gimnig JE et al.. Consistently high estimates for proportion of human exposure to malaria vector populations occuring indoors in rural Africa. Int J Epidemiol. 2013; 42:235-47.
• [38]Chavasse DC, Lines JD, Ichimori K, Marijani J. Mosquito control in Dar es Salaam. I. Assessment of Culex quinquefasciatus breeding sites prior to intervention. Med Vet Entomol. 1995; 9(2):141-6.
• [39]Govella NJ, Chaki PP, Mpangile J, Killeen GF. Monitoring mosquitoes in urban Dar es Salaam: evaluation of resting boxes, window exit traps, CDC light traps, Ifakara tent traps and human landing catches. Parasit Vectors. 2011; 4:40. BioMed Central Full Text
• [40]Chaki PP, Mlacha Y, Msellem D, Muhili A, Malishee AD, Mtema ZJ et al.. An affordable, quality-assured community-based system for high-resolution entomological surveillance of vector mosquitoes that reflects human malaria infection risk pattern. Malar J. 2012; 11:172. BioMed Central Full Text
• [41]Chavasse DC. The relationship between mosquito density and mosquito coil sales in Dar es Salaam. Trans Roy Soc Trop Med Hyg. 1996; 90:493.
• [42]Castro MC, Tsuruta A, Kanamori S, Kannady K, Mkude S. Community-based environmental management for malaria control: evidence from a small-scale intervention in Dar es Salaam, Tanzania. Malar J. 2009; 8:57. BioMed Central Full Text
• [43]Castro MC, Kanamori S, Kannady K, Mkude S, Killeen GF, Fillinger U. The importance of drains for the larval development of lymphatic filariasis and malaria vectors in Dar es salaam, United Republic of Tanzania. PLoS Negl Trop Dis. 2010; 4:e693.
• [44]Govella NJ, Chaki PP, Geissbühler Y, Kannady K, Okumu FO, Charlwood JD et al.. A new tent trap for sampling exophagic and endophagic members of the Anopheles gambiae complex. Malar J. 2009; 8:157. BioMed Central Full Text
• [45]Gillies MT, De Meillon B. The Anophelinae of Africa South of the Sahara (Ethiopian zoogeographical region). South African Institute for Medical Research, Johannesburg; 1968.
• [46]Lindblade KA. Commentary: Does a mosquito bite when no one is around to hear it. Int J Epidemiol. 2013; 42:247-9.
• [47]Nkya TE, Akhouayri I, Poupardin R, Batengana B, Mosha FW, Magesa SM et al.. Insecticides resistance mechanisms associated with different environments in the malaria vector Anopheles gambiae: a case study in Tanzania. Malar J. 2013; 13:28. BioMed Central Full Text
• [48]Service MW. A critical review of procedures for sampling populations of adult mosquitoes. Bull Entomol Res. 1977; 67:343-82.
• [49]Malaria Entomology and Vector Control. Learner’s Guide. nth ed. World Health Organisation, Geneva; 2002.
• [50]Scott JA, Brogdon WG, Collins FH. Identification of single specimens of Anopheles gambiae complex by polymerase chain reaction. Am J Trop Med Hyg. 1993; 49:520-9.
• [51]Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Steven MHH et al.. Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol. 2009; 24:127-35.
• [52]Gimnig JE, Walker ED, Otieno P, Kosgei J, Olang G, Omboki M et al.. Incidence of malaria among mosquito collectors conducting human landing catches in western Kenya. Am J Trop Med Hyg. 2013; 88:301-8.
• [53]Okumu FO, Mbeyela E, Lingamba G, Moore J, Ntamatungiro AJ, Kavishe DR et al.. Comparative field evaluation of combinations of long-lasting insecticide treated nets and indoor residual spraying, relative to either method alone, for malaria prevention in an area where the main vector is Anopheles arabiensis. Parasites & Vectors. 2013; 6:46. BioMed Central Full Text
• [54]Gimnig JE, Vulule JM, Lo TQ, Kamau L, Kolczak MS, Phillips-Howard PA et al.. Impact of permethrin-treated bed nets on entomologic indices in an area of intense year-round malaria transmission. Am J Trop Med Hyg. 2003; 68 Suppl. 4:16-22.
• [55]Okumu FO, Moore S. Combining indoor residual spraying and insecticides-treated nets for malaria control in Africa: a review of possible outcomes and an outline of suggestions for the future. Malar J. 2011; 10:208. BioMed Central Full Text
• [56]Ranson H, Nguessan R, Lines J, Moiroux N, Nkuni Z, Corbel V. Pyrethroid resistance in African anopheline mosquitoes: what are the implications for malaria control? Trends Parasitol. 2011; 27:91-8.
• [57]Yewhalaw D, Wassie F, Steurbaut W, Spanoghe P, Van Bortel W, Denis L et al.. Multiple insecticide resistance: an impediment to insecticide-based malaria vector control program. PLoS One. 2011; 6(1):e16066.
• [58]Maia MF, Onyango SP, Thele M, Simfukwe E, Turner E, Moore SJ. Do topical repellents divert mosquitoes within a community? Health equity implications of topical repellents as a mosquito bite prevention tool. PLoS One. 2013; 8:e84875.
• [59]Moore SJ, Davis CR, Hill N, Cameron MM. Are mosquitoes diverted from repellent-using individuals to non-users? Results of a field study in Bolvia. Trop Med Int Health. 2007; 12:532-9.
• [60]Tungu P, Magesa SM, Maxwell CA, Malima R, Masue D, Sudi W et al.. Evaluation of Perme Net 3.0 a deltermethrin-PBO combination net against Anopheles gambiae and pyrethroid resistant Culex quinquefasciatus mosquitoes: an experimental hut trial in Tanzania. Malar J. 2010; 9:21. BioMed Central Full Text
• [61]Jones CM, Machin C, Mohammed K, Majambere S, Ali AS, Khatib BO et al.. Insecticides resistance in Culex quinquefasciatus from Zanzibar: implications for vector control programmes. Parasit Vectors. 2012; 5:78. BioMed Central Full Text
• [62]Zyzak M, Loyless T, Cope S, Wooster M, Day JF. Seasonal abundance of Culex nigripalpus Theobald and Culex salinarius Coquillett in north Florida, USA. J Vector Ecol. 2002; 27(1):155-62.
• [63]Worrall E, Fillinger U. Large-scale use of mosquito larval source management for malaria control in Africa: a cost analysis. Malar J. 2011; 10:338. BioMed Central Full Text
• [64]Loll DK, Berthe S, Faye SL, Wone I, Koenker H, Arnold B et al.. User-determined end of net life in Senegal: a qualitative assesment of decision-making related to the retirement of expired nets. Malar J. 2013; 12:337. BioMed Central Full Text
• [65]Ogoma SB, Ngonyani H, Simfukwe E, Mseka A, Moore J, Maia MF et al.. The mode of action of spatial repellents and their impact on vectorial capacity of Anopheles gambiae sensu stricto. PLoS One. 2014; 9: Article ID e110433
• [66]MCLean KA, Byanaku A, Kubikonse A, Tshowe V, Katensi S, Lehman AG. Fishing with bed nets on Lake Tanganyika: a randomized survey. Malar J. 2015; 13:395. BioMed Central Full Text
• [67]Sangoro PO, Kelly A, Mtali S, Moore SJ. Feasibility of repellent use in a context of increasing outdoor transmission: a qualitative study in rural Tanzania. Malar J. 2014; 13:347. BioMed Central Full Text
• [68]Habicht JP, Victora CG, Vaughan JP. Evaluation designs for adequacy, plausibility and probability of public health programme performance and impact. Int J Epidemiol. 1999; 28:10-8.