Bionomics of the malaria vector Anopheles farauti in Temotu Province, Solomon Islands: issues for malaria elimination

Malaria Journal, May 2011

In the Solomon Islands, the Malaria Eradication Programmes of the 1970s virtually eliminated the malaria vectors: Anopheles punctulatus and Anopheles koliensis, both late night biting, endophagic species. However, the vector, Anopheles farauti, changed its behaviour to bite early in the evening outdoors. Thus, An. farauti mosquitoes were able to avoid insecticide exposure and still maintain transmission. Thirty years on and the Solomon Islands are planning for intensified malaria control and localized elimination; but little is currently known about the behaviour of the vectors and how they will respond to intensified control. In the elimination area, Temotu Province, standard entomological collection methods were conducted in typical coastal villages to determine the vector, its ecology, biting density, behaviour, longevity, and vector efficacy. These vector surveys were conducted pre-intervention and post-intervention following indoor residual spraying and distribution of long-lasting insecticidal nets. Anopheles farauti was the only anopheline in Temotu Province. In 2008 (pre-intervention), this species occurred in moderate to high densities (19.5-78.5 bites/person/night) and expressed a tendency to bite outdoors, early in the night (peak biting time 6-8 pm). Surveys post intervention showed that there was little, if any, reduction in biting densities and no reduction in the longevity of the vector population. After adjusting for human behaviour, indoor biting was reduced from 57% pre-intervention to 40% post-intervention. In an effort to learn from historical mistakes and develop successful elimination programmes, there is a need for implementing complimentary vector control tools that can target exophagic and early biting vectors. Intensified indoor residual spraying and long-lasting insecticide net use has further promoted the early, outdoor feeding behaviour of An. farauti in the Solomon Islands. Consequently, the effectiveness of IRS and the personal protection provided by bed nets is compromised. To achieve elimination, any residual transmission should be targeted using integrated vector control incorporating complementary tools such as larviciding and/or zooprophylaxis.

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Bionomics of the malaria vector Anopheles farauti in Temotu Province, Solomon Islands: issues for malaria elimination

Malaria Journal Bionomics of the malaria vector Anopheles farauti in Temotu Province, Solomon Islands: issues for malaria elimination Hugo Bugoro 0 2 Robert D Cooper 1 Charles Butafa 0 Charles Iro'ofa 0 Donna O Mackenzie 1 Cheng-Chen Chen 2 Tanya L Russell 3 0 National Vector Borne Disease Control Programme, Ministry of Health , Honiara , Solomon Islands 1 Australian Army Malaria Institute , Gallipoli Barracks, Enoggera, 4052 , Australia 2 Institute of Tropical Medicine, National Yang-Ming University , No. 155, Sec.2, Li-Nong Street, Taipei 112 , Taiwan 3 The University of Queensland, School of Population Health, Australian Centre for Tropical and International Health, Pacific Malaria Initiative Support Centre , Herston, 4006 , Australia Background: In the Solomon Islands, the Malaria Eradication Programmes of the 1970s virtually eliminated the malaria vectors: Anopheles punctulatus and Anopheles koliensis, both late night biting, endophagic species. However, the vector, Anopheles farauti, changed its behaviour to bite early in the evening outdoors. Thus, An. farauti mosquitoes were able to avoid insecticide exposure and still maintain transmission. Thirty years on and the Solomon Islands are planning for intensified malaria control and localized elimination; but little is currently known about the behaviour of the vectors and how they will respond to intensified control. Methods: In the elimination area, Temotu Province, standard entomological collection methods were conducted in typical coastal villages to determine the vector, its ecology, biting density, behaviour, longevity, and vector efficacy. These vector surveys were conducted pre-intervention and post-intervention following indoor residual spraying and distribution of long-lasting insecticidal nets. Results: Anopheles farauti was the only anopheline in Temotu Province. In 2008 (pre-intervention), this species occurred in moderate to high densities (19.5-78.5 bites/person/night) and expressed a tendency to bite outdoors, early in the night (peak biting time 6-8 pm). Surveys post intervention showed that there was little, if any, reduction in biting densities and no reduction in the longevity of the vector population. After adjusting for human behaviour, indoor biting was reduced from 57% pre-intervention to 40% post-intervention. Conclusion: In an effort to learn from historical mistakes and develop successful elimination programmes, there is a need for implementing complimentary vector control tools that can target exophagic and early biting vectors. Intensified indoor residual spraying and long-lasting insecticide net use has further promoted the early, outdoor feeding behaviour of An. farauti in the Solomon Islands. Consequently, the effectiveness of IRS and the personal protection provided by bed nets is compromised. To achieve elimination, any residual transmission should be targeted using integrated vector control incorporating complementary tools such as larviciding and/or zooprophylaxis. - Background The leading vector control tools, long-lasting insecticidal nets (LLINs) and indoor residual spraying (IRS) can be very effective at reducing malaria transmission [1-4]. The efficacies of these vector control tools depends heavily of the behaviour of the malaria vectors, and are more effective against vectors which bite indoors (endophagic), late in the night (nocturnal) and which rest indoors after feeding (endophilic). These characteristics are classically observed for the primary malaria vectors in sub-Saharan Africa and are contributing to the success of the malaria programmes in this region [1,2,5,6]. However in the southwest Pacific, the feeding and resting behaviour of vectors are much more variable, with some species expressing a tendency to bite early in the night, outdoors (exophagic), on animals (zoophagic) and to rest outdoor (exophilic) [7-9]. Such behaviours could reduce the efficacy of vector control tools which rely on vectors feeding indoors. The malaria eradication programmes of the 1960-1970s were not successful due to a number of factors including logistical and financial limitations as well as technical and operational issues [10]. With regards to the vector, insecticide resistance was a major world-wide problem [11,12]. However, in the southwest Pacific, there has been no evidence of physiological insecticide resistance despite decades of DDT-IRS followed by pyrethroid-IRS and treated nets. What has been observed, particularly in one of the major vectors, Anopheles farauti, is a change of biting behaviour. In Papua New Guinea, the Solomon Islands and Vanuatu it was found that there was a shift in the behaviour of this vector from feeding indoors late in the night to outdoors early in the night [8,13-16]. This change in behaviour was most likely due to vector irritability caused by the DDT leading to the vector avoiding insecticide exposure [5,14]. In the Solomon Islands, it was found that the proportion of An. farauti biting from 6-8 pm increased from 30% before IRS to 66% after IRS; also the proportion biting indoors changed from 53% before IRS to 33% after IRS [8]. Another factor, relevant to the efficacy of IRS, was that the excito-repellent effect of the DDT reduced or precluded the time An. farauti spent indoors resting so that at least 45% of An. farauti exited houses without picking up a lethal dose of insecticide [16]. This change in resting and biting behaviour reduced the level of personal and communal protection afforded by IRS and ultimately led to the failure of the eradication programme despite the addition of mass drug administration to the programme [17,18]. The international community recently prioritized national and regional elimination with a long term goal of malaria eradication, based on a key strategy of shrinking the malaria map from the margins inwards [19]. Worldwide, a number of geographically defined regions have adopted the goal of regional malaria elimination, including Temotu Province in the Solomon Islands. Temotu Province was selected for elimination because, in addition to its geographic isolation, the incidence of malaria has remained low since the initial eradication efforts in the 1970s. When the current elimination program commenced in 2008, the overall parasite rate determined by mass blood survey was estimated to be 3.83% [20]. The only anopheline found in the Province has been An. farauti s.l. [21]; however more recent molecularbased studies have identified three species of the Farauti Complex in the Solomon Islands [22,23]. Allozyme electrophoresis was used to identify An. farauti from Ndendo [22] and while it is most likely that this is the only species on the other islands this is yet to be confirmed. Given the history of An. farauti, its reaction to IRS, and that the primary intervention measures intended for the elimination of malaria in Temotu Province will target the vector by IRS or LLINs, it is essential to understand the en (...truncated)


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Bugoro, Hugo, Cooper, Robert D, Butafa, Charles, Iro'ofa, Charles, Mackenzie, Donna O, Chen, Cheng-Chen, Russell, Tanya L. Bionomics of the malaria vector Anopheles farauti in Temotu Province, Solomon Islands: issues for malaria elimination, Malaria Journal, 2011, pp. 1-11, Volume 10, Issue 1, DOI: 10.1186/1475-2875-10-133