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NEW THIS SUNDAY: MALARIA AND LYMPHATIC FILARIASIS: THE CASE FOR INTEGRATED VECTOR MANAGEMENT

Thursday, 22nd of August 2013

• NEW THIS SUNDAY: MALARIA AND LYMPHATIC FILARIASIS: THE CASE FOR INTEGRATED VECTOR MANAGEMENT

The Lancet Infectious Diseases, Volume 13, Issue 1, Pages 89 - 94, January 2013

Published Online: 19 October 2012

Original Text

Henk van den Berg PhD a, Louise A Kelly-Hope PhD b, Prof Steve W Lindsay PhD c

Best viewed at

 http://www.thelancet.com/journals/laninf/article/PIIS1473-3099(12)70148-2/fulltext

Summary

The global programmes to eliminate both malaria and lymphatic filariasis are facing operational and technical challenges. Available data show that the use of treated or untreated bednets and indoor residual spraying for malaria control concomitantly reduced filarial rates. In turn, mass drug administration campaigns against lymphatic filariasis can be combined with the distribution of insecticide-treated bednets. Combining these disease control efforts could lead to more efficient use of resources, more accurate attribution of effects, and more effective control of both diseases. Systematic integration requires coordination at all levels, mapping of coendemic areas, and comprehensive monitoring and evaluation.

Introduction

Several groups have advocated combining control efforts for malaria with those for neglected tropical diseases, lymphatic filariasis in particular.1—5 Malaria, caused by protozoa of the genus Plasmodium, and lymphatic filariasis, caused by the nematodes Wuchereria bancrofti, Brugia malayi, and Brugia timori, overlap in their distribution in most of Africa, south and southeast Asia, and some parts of Latin America.6, 7 Similarities exist between malaria and lymphatic filariasis in relation to their transmission: both diseases may be transmitted by the same or related vector species, both are potentially controlled by the same vector-control interventions, both have no or almost no hosts other than human beings, and both prevail under conditions of poverty and poor environmental sanitation.

Malaria and lymphatic filariasis cause the highest global burdens of all vector-borne diseases, particularly in Africa and southeast Asia (table 1).7—11 Malaria is transmitted by Anopheles species in all regions, whereas regional differences exist in the mosquito genera that transmit filarial parasites. In much of Africa and parts of the western Pacific (eg, Papua New Guinea), the anopheline vectors of malaria are also the principal vectors of lymphatic filariasis.12Culex quinquefasciatus is an important vector in urban areas of east Africa, but in west Africa this species is considered refractory to infection with W bancrofti.13 Elsewhere, members of the Culex pipiens complex (predominantly C quinquefasciatus) and Aedes species are the principal vectors of lymphatic filariasis.7, 11

  

Table 1Table image 

Risk, burden, and vectors of malaria and lymphatic filariasis, by WHO region

Integrated vector management is promoted by WHO as the best approach to improve the efficacy, cost-effectiveness, ecological soundness, and sustainability of vector control.14 To achieve integration, vector control should be based on local evidence, adopt a multidisease approach, and combine interventions wherever appropriate and feasible. In its implementation, integrated vector management depends on collaboration between health-sector programmes, other sectors, and communities.15, 16 Here we aim to substantiate a recent statement by WHO on integrated vector management to control malaria and lymphatic filariasis17 by summarising available evidence and suggesting the way forward.

Two global programmes and their challenges

The history of global programmes for the control of malaria and filariasis shows that the emphasis on vector control or drugs changes over time. Vector control, primarily through indoor residual spraying with DDT (dichlorodiphenyltrichloroethane) and dieldrin, was central in the first malaria eradication campaign (1955—69), but lost its significance as financial and technical constraints put eradication out of reach; eradication of malaria was never attempted in sub-Saharan Africa.18—20 Malaria control programmes have regained a strong emphasis on vector control in the past two decades, following evidence of the cost-effectiveness and general applicability of insecticide-treated bednets21 and indoor residual spraying.22 Both interventions, when used on a large scale, have resulted in major reductions in malaria in many countries.23 Similarly for lymphatic filariasis, vector control once was the primary control strategy, but the emphasis switched to preventive chemotherapy; however, vector control is regaining recognition because of recent problems in mass drug administration programmes.24, 25

The contemporary Global Malaria Programme8 and Global Programme for Elimination of Lymphatic Filariasis25 share the goals of local elimination and global eradication of disease by achieving universal coverage of populations at risk with appropriate interventions. These shared aims suggest that the two programmes are a good match.

Despite major progress in malaria control towards reaching targets for the distribution and use of long-lasting insecticidal nets (LLINs),8 much more is needed to increase penetration within communities and to access hard-to-reach communities. The high coverage with insecticidal vector-control methods, however, will exert strong selective pressure for insecticide resistance in vector populations,26, 27 which emphasises the importance of surveillance, resistance management, and the need to diversify interventions. As such, both global programmes will face operational and technical challenges with regards to vector control in the future.

Regarding filariasis, the primary form of control remains preventive chemotherapy. A barrier to initiation of programmes to eliminate lymphatic filariasis is the coendemicity of Loa loa in large parts of central Africa.28, 29 Patients with loiasis can develop serious neurological reactions to the drugs used in mass drug administration,30 especially at high L loa microfilariae burdens.31 Elsewhere, the challenge in lymphatic filariasis elimination is to reach minimum effective coverage of mass drug administration25 in annual rounds through scale-up and promotion of compliance; however, there is uncertainty about the coverage level and the number of annual rounds needed to achieve elimination in the local context.29 Field studies and mathematical models have shown that vector control can have an important complementary role in the elimination effort.24, 32, 33 As such, where mass drug administration is supplemented by vector control, lower coverage levels and fewer annual rounds would be needed to achieve elimination.

Programme interactions

Vector control to prevent transmission of malaria parasites and mass drug administration to prevent transmission of microfilariae are two strategies that can affect several diseases. Vector control can reduce vector—human contact for more than one disease, particularly where malaria and lymphatic filariasis have the same principal vectors. Mass drug administration campaigns can facilitate the improvement of vector control if linked with the distribution of LLINs.1 In central Nigeria, this linkage resulted in substantial improvement in both ownership and use of LLINs for malaria control, without an adverse effect on drug administration operations.34

Mass drug administration can have several effects: treatment substantially reduces the microfilariae load of Wuchereria sp and Brugia sp parasites in human hosts.35 Additionally, the drugs albendazole and ivermectin have broad anthelmintic activity with benefits for the prevention and control of other widespread diseases, such as intestinal helminth infection and onchocerciasis.36, 37 An auxiliary result of mass drug administration is the known temporary effect of the drugs on the survival of mosquito vectors feeding on treated hosts in operational settings, thus contributing to control of malaria and lymphatic filariasis.38—41 Interactions between malaria parasites and filariae in people with both are complex and largely unknown. Helminth infections might adversely affect the acquisition of immunity to malaria,42, 43 and so the treatment of lymphatic filariasis would indirectly relieve the burden of malaria. Direct effects of anthelmintic drugs on Plasmodium species have not been reported. More generally, as mass drug administration causes worm expulsion, it affects various morbidity outcomes, including those associated with malaria control: anaemia, growth retardation, and cognitive impairment.44

Evidence of combined effects

Several studies have documented the outcome of integrated control of malaria and lymphatic filariasis (table 2).45—55 In some studies, the integration was deliberate; in others, vector control interventions intended for malaria control inadvertently affected lymphatic filariasis. In most reported instances, both diseases had the same anopheline vectors.

Table 2Table image

Studies that show the effect of integrated control of malaria and lymphatic filariasis

In the Solomon Islands, where both diseases had anopheline vectors, indoor residual spraying with DDT targeted at malaria inadvertently eliminated lymphatic filariasis, but did not eliminate malaria.45, 46

In Papua New Guinea, two studies in the absence of mass drug administration showed that untreated bednets had a stronger effect on microfilariae burden than on malaria sporozoite antigen rates.49, 53 In the same country, insecticide-treated bednets in combination with weekly mass drug administration caused a decline in microfilariae but had no significant effect on malaria prevalence.50 In Cambodia, treated bednets offered better protection against the morbidity of lymphatic filariasis than did untreated bednets.54

In Pondicherry, India, lymphatic filariasis is concentrated in urban and malaria in rural areas, and the diseases have separate vectors. Environmental management was implemented at large scale with the participation of communities and collaboration between sectors.47, 48 The microfilariae burden dropped substantially for young children, and malaria was locally eliminated. Other studies have confirmed the value of environmental management of lymphatic filariasis transmitted by Culex sp mosquitoes where breeding is confined to wells and pits,32, 56, 57 but without the integration of malaria vector control.

On the Kenyan coast, insecticide-treated bednets aimed at control of malaria had a large effect on the vector potential of lymphatic filariasis, based on the human blood index and mosquito density.51 In a follow-up study, although insecticide-treated bednets reduced the vector biting rate by just 22%, this resulted in the annual infected biting rate plummeting by 95% and the annual transmission potential (ie, the number of infective larvae inoculated per person per year) by 92%.52 Hence, despite a modest reduction in biting rate, the transmission of W bancrofti was strongly suppressed. A recent study from Uganda showed a substantial reduction in W bancrofti infection and infectivity in people where both mass drug administration and LLINs were used, but the contribution of LLINs remains unclear.55

The effect of insecticide-treated bednets on culex-transmitted lymphatic filariasis has not been systematically assessed. Bednets are used against nuisance biting from culex mosquitoes. Insecticide-treated bednets do not seem to kill culex mosquitoes, possibly because of tolerance or contact irritability to the insecticides,58 although an irritant effect could cause mosquitoes to exit the homes of bednet users, reducing the number of bites received. Insecticide-treated bednets might also divert C quinquefasciatus from human to non-human hosts.51

In summary, in places where anophelines have been implicated as principal vectors for both lymphatic filariasis and malaria parasites, the use of untreated and treated bednets and indoor residual spraying have convincingly reduced filarial rates. In several instances, the effect was greater for W bancrofti than for malaria, which could be because of the density-dependent processes involved in anopheline transmission of filariae,59, 60 or because transmission of lymphatic filariasis is less efficient than that of malaria.24, 61 Integration of environmental management for malaria and lymphatic filariasis, including the construction of soakage pits, cleaning of drains, and improvement of sanitation, also merits attention in the context of integrated vector management, as suggested from the results from India, especially where vector breeding is focal and within human habitations. Consequently, integration requires inputs from various sectors, many of which lie outside the health sector.

Towards integration

Malaria and lymphatic filariasis have much in common in terms of their geographical distribution, transmission biology, and mutual interactions. Moreover, the global programmes to contain them have matching goals, strategies, and challenges.8, 25 Integration would be required at the level of communities, districts, ministries, and donors.16 The prospects for integration are contingent on the local context of disease epidemiology, vector ecology, and a countrys operational capacity. Therefore, the initial focus for integration should be where the potential benefits are greatest, which seems to be in sub-Saharan Africa and parts of the Pacific where both diseases are transmitted by anopheline vectors.7, 62

We propose four reasons for integration: more efficient use of resources; segregated programmes could have unintended consequences; more accurate attribution of effects; and increased effect on both diseases.

First, efficiency is improved when activities of geographical reconnaissance, planning, implementation, monitoring and evaluation, data management, and reporting for the two diseases are combined, and when expertise, training, logistics, and infrastructure are shared. Particularly, the distribution of LLINs or indoor residual spraying could be planned, implemented, and assessed in tandem with mass drug administration.1, 34 Entomological expertise generally available for malaria could be used to improve vector control of lymphatic filariasis3—eg, by establishing a core group on vector control with a cross-disease mandate.16 Also, lymphatic filariasis programme staff could contribute to annual checks of the quality and use of bednets during mass drug administration campaigns, with benefits for control of both malaria and lymphatic filariasis. Broadening the remit of staff that have managed a single disease programme to one that covers several diseases can initially be challenging, since personnel can feel uncomfortable about moving into new areas. Careful training and mixing of staff can make this process more straightforward. Importantly, as the prevalence of either disease drops to extremely low, pre-elimination, levels, continued surveillance is essential to prevent disease resurgence. This detailed surveillance is long-term and expensive, but becomes less so if the surveillance system can be used for monitoring and evaluation of several diseases simultaneously. In many ways this is similar to how the smallpox eradication programme evolved into the expanded programme on immunisation.63

Second, in the absence of integration, a disease-specific programme could inadvertently increase risk for the other disease. Even though the available evidence suggests mostly complementary and synergistic effects between control of the two diseases, the interactions between filariae and malaria in co-infected vectors or hosts are dynamic and still largely unknown. Hence, uncertainty about the overall effect on malaria transmission could be circumvented by supplementary vector control.64 Moreover, as countries approach elimination of either disease, whether removing one disease will lead to a change in prevalence of the other remains unclear.65 This uncertainty emphasises the importance of national coordination between the two programmes throughout their elimination phases.

Third, integration of programmes would enable improvement of evaluation, with more accurate attribution of the observed effects to the resources used, with the recognition that interventions can affect both diseases. Hence, in an area covered by LLINs and mass drug administration, the malaria programme should consider the role of anthelmintic drugs in the reduction of plasmodia transmission,40 and the lymphatic filariasis programme should account for the effect of malaria-control interventions on filarial transmission.

Fourth, the ultimate benefit of integration will be improved control of both diseases. Past studies have shown inadvertent benefits of malaria vector control on lymphatic filariasis.45,46,49,52—54 The synergistic effects between the control of malaria and lymphatic filariasis are evident and should no longer be left to chance, but should be optimised through improvements in three areas: coordination, logistics, and use of existing infrastructure; microstratified mapping of coendemic areas and interventions; and monitoring and evaluation of the efficacy of approaches, including drug and insecticide resistance surveillance. Donors must support the unique requirements for programme integration—requirements that could be in addition to those of disease-specific programmes, but that will make those programmes more effective.

Between 2008 and 2010, an estimated 294 million insecticide-treated bednets were delivered to sub-Saharan Africa, aimed at malaria control.8 If in the coming years the distribution of LLINs were coordinated between the national disease-control programmes and optimally targeted, while using the infrastructure of mass drug administration wherever feasible, this could benefit control of both diseases. Likewise, the mass administration of ivermectin could be optimised by scheduling at times of peak vector biting to reduce transmission,66 or at low transmission levels with the aim of malaria elimination. Such strategies would be especially relevant in situations where insecticide resistance or outdoor biting reduce the effectiveness of LLINs and indoor residual spraying.67, 68 Perhaps the biggest advantage of the coordination of drug administration and LLINs will be their combined effect on anaemia, a major killer of young children, through the reduction of malaria and hookworm infections.1

The use of microstratified mapping of malaria and lymphatic filariasis endemic areas, overlaid with the distribution of LLINs and coverage of mass drug administration, is an important requirement.37 These maps would help prioritise geographical areas for integrated control of malaria and lymphatic filariasis, along with operational research, and assist in prediction of the anticipated benefits from integration. Moreover, the recently developed maps for the rapid assessment procedure for loiasis provide valuable information that demarcates L loa endemic areas in Africa.28 Where the endemicity of L loa and lymphatic filariasis overlap ivermectin is contraindicated, so interventions targeted at the vectors of lymphatic filariasis should be emphasised.37

In the face of spreading resistance in anophelines against the pyrethroids used in LLINs,27 a window of opportunity seems to exist in endemic countries to use LLINs in a so-called attack phase, to substantially reduce prevalence of malaria and lymphatic filariasis and so to reach more manageable or pre-elimination levels of both diseases.27, 69 From pre-elimination to postelimination, vector control will have a continuing role to reduce transmission risk and prevent a rebound of infection, with progressive use of additional methods within the context of integrated vector management.70—73

Search strategy and selection criteria

We searched PubMed and Scopus for articles published from 1960 to May, 2012. Studies were identified using search terms “malaria” and “Wuchereria” or “Brugia”. References from the retrieved articles were used to identify other relevant publications that were not identified from the database searches. Each article written in English was assessed for its methodological quality and the relevance of its results.

Contributors

HvdB did the reference review and drafted the report. LAK-H and SWL contributed to the further development of the report.

Conflicts of interests

HvdB has received consultancy fees from WHOs Department of Control of Neglected Tropical Diseases, though not for preparation of this report. LAK-H and SWL declare that that they have no conflicts of interest.

Acknowledgments

LAK-H was supported by a grant from the UK Department for International Development for research on the elimination of lymphatic filariasis. SWL was supported by the US National Institutes of Health (grant 1R01AI082537), the Research and Policy for Infectious Disease Dynamics programme of the Science and Technology Directorate (US Department of Homeland Security), and Fogarty International Center (National Institutes of Health). The sponsors had no role in the preparation of the report.

References

1 Molyneux DH, Nantulya VM. Linking disease control programmes in rural Africa: a pro-poor strategy to reach Abuja targets and millennium development goals. BMJ 2004; 328: 1129-1132. CrossRef | PubMed

2 Molyneux DH, Hotez PJ, Fenwick A, Newman RD, Greenwood B, Sachs J. Neglected tropical diseases and the Global Fund. Lancet 2009; 373: 296-297. Full Text | PDF(106KB) | CrossRef | PubMed

3 Manga L. Vector-control synergies, between Roll Back Malaria and the Global Programme to Eliminate Lymphatic Filariasis, in the African Region. Ann Trop Med Parasitol 2002; 96 (suppl 2): S129-S132. PubMed

4 Prasittisuk C. Vector-control synergies, between Roll Back Malaria and the Global Programme to Eliminate Lymphatic Filariasis, in South-east Asia. Ann Trop Med Parasitol 2002; 96 (suppl 2): S133-S137. PubMed

5 Muturi EJ, Jacob BG, Kim CH, Mbogo CM, Novak RJ. Are coinfections of malaria and filariasis of any epidemiological significance?. Parasitol Res 2008; 102: 175-181. CrossRef | PubMed

6 Manguin S, Bangs MJ, Pothikasikorn J, Chareonviriyaphap T. Review on global co-transmission of human Plasmodium species and Wuchereria bancrofti by Anopheles mosquitoes. Infect Genet Evol 2010; 10: 159-177. CrossRef | PubMed

7 WHO. Geographical distribution of arthropod-borne diseases and their principal vectors. Geneva: World Health Organization, 1989.

8 WHO. World malaria report 2011. Geneva: World Health Organization, 2011.

9 WHO. The global burden of disease: 2004 update. Geneva: World Health Organization, 2008.

10 WHO. Global Programme to Eliminate Lymphatic Filariasis: progress report on mass drug administration, 2010. Wkly Epidemiol Rec 2011; 35: 377-388. PubMed

11 WHO. Defining the roles of vector control and xenomonitoring in the global programme to eliminate lymphatic filariasis. Geneva: World Health Organization, 2002.

12 Sasa M. Human filariasis: a global survey of epidemiology and control. Tokyo: University of Tokyo, 1976.

13 Curtis CF, Graves PM. Genetic variation in the ability of insects to transmit filariae, trypanosomes, and malarial parasites. In: Harris KF, ed. . New York: Praeger, 1983: 31-62.

14 WHO. WHO position statement on integrated vector management. Geneva: World Health Organization, 2008.

15 Mnzava A, Williams J, Bos R, Zaim M. Implementation of integrated vector management for disease vector control in the Eastern Mediterranean: where are we and where are we going?. East Mediterr Health J 2011; 17: 453-459. PubMed

16 WHO. Handbook for integrated vector management. Geneva: World Health Organization, 2012.

17 WHO. WHO position statement on integrated vector management to control malaria and lymphatic filariasis. Wkly Epidemiol Rec 2011; 86: 121-127. PubMed

18 Bruce-Chwatt LJ. Man against malaria: conquest or defeat. Trans R Soc Trop Med Hyg 1978; 73: 605-617. CrossRef | PubMed

19 Nájera JA, Gonzalez-Silva M, Alonso PL. Some lessons for the future from the global malaria eradication programme (1955—1969). PLoS Med 2011; 8: e1000412. CrossRef | PubMed

20 Nájera JA. Malaria control: achievements, problems and strategies. Parassitologia 2001; 43: 1-89. PubMed

21 Lengeler C. Insecticide-treated bednets and curtains for preventing malaria. Cochrane Database Syst Rev 2004; 2. CD000363.

22 Pluess B, Tanser FC, Lengeler C, Sharp BL. Indoor residual spraying for preventing malaria. Cochrane Database Syst Rev 2010; 4. CD006657.

23 OMeara WP, Mangeni JN, Steketee R, Greenwood B. Changes in the burden of malaria in sub-Saharan Africa. Lancet Infect Dis 2010; 10: 545-555. Summary | Full Text | PDF(371KB) | CrossRef | PubMed

24 Bockarie MJ, Pedersen EM, White GB, Michael E. Role of vector control in the global program to eliminate lymphatic filariasis. Annu Rev Entomol 2009; 54: 469-487. CrossRef | PubMed

25 WHO. Progress report 2000—2009 and strategic plan 2010—2020 of the global programme to eliminate lymphatic filariasis: halfway towards eliminating lymphatic filariasis. Geneva: World Health Organization, 2010.

26 Kelly-Hope L, Ranson H, Hemingway J. Lessons from the past: managing insecticide resistance in malaria control and eradication programmes. Lancet Infect Dis 2008; 8: 387-389. Summary | Full Text | PDF(88KB) | CrossRef | PubMed

27 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: 91-98. CrossRef | PubMed

28 Zouré HGM, Samuel Wanji S, Noma M, et al. The geographic distribution of Loa loa in Africa: results of large-scale implementation of the rapid assessment procedure for loiasis (RAPLOA). PLoS Med 2011; 5: e1210. PubMed

29 Addiss D. The 6th meeting of the Global Alliance to Eliminate Lymphatic Filariasis: a half-time review of lymphatic filariasis elimination and its integration with the control of other neglected tropical diseases. Parasit Vectors 2010; 3: 100. PubMed

30 Padgett JJ, Jacobsen KH. Loiasis: African eye worm. Trans R Soc Trop Med Hyg 2008; 102: 983-989. CrossRef | PubMed

31 Gardon J, Gardon-Wendel N, Ngangue D, Kamgno J, Chippaux JP, Boussinesq M. Serious reactions after mass treatment of onchocerciasis with ivermectin in an area endemic for Loa loa infection. Lancet 1997; 350: 18-22. Summary | Full Text | PDF(170KB) | CrossRef | PubMed

32 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 Organ 2007; 85: 138-145. CrossRef | PubMed

33 Michael E, Malecela-Lazaro MN, Simonsen PE, et al. Mathematical modelling and the control of lymphatic filariasis. Lancet Infect Dis 2007; 4: 223-234. Summary | Full Text | PDF(238KB) | CrossRef | PubMed

34 Blackburn BG, Eigege A, Gotau H, et al. Successful integration of insecticide-treated bed net distribution with mass drug administration in Central Nigeria. Am J Trop Med Hyg 2006; 75: 650-655. PubMed

35 Tisch D, Michael E, Kazura JW. Mass chemotherapy options to control lymphatic filariasis: a systematic review. Lancet Infect Dis 2005; 5: 514-523. Summary | Full Text | PDF(191KB) | CrossRef | PubMed

36 Ottesen EA, Hooper PJ, Bradley M, Biswas G. The global programme to eliminate lymphatic filariasis: health impact after 8 years. PLoS Negl Trop Dis 2008; 2: e317. PubMed

37 Kelly-Hope LA, Thomas BC, Bockarie MJ, Molyneux DH. Lymphatic filariasis in the Democratic Republic of Congo; micro-stratification overlap mapping (MOM) as a prerequisite for control and surveillance. Parasit Vectors 2011; 4: 178. PubMed

38 Kobylinski KC, Sylla M, Chapman PL, Sarr MD, Foy BD. Short report: Ivermectin mass drug administration to humans disrupts malaria parasite transmission in Senegalese villages. Am J Trop Med Hyg 2011; 85: 3-5. CrossRef | PubMed

39 Chaccour C, Lines J, Whitty CJ. Effect of ivermectin on Anopheles gambiae mosquitoes fed on humans: the potential of oral insecticides in malaria control. J Infect Dis 2010; 202: 113-116. CrossRef | PubMed

40 Sylla M, Kobylinski KC, Gray M, et al. Mass drug administration of ivermectin in south-eastern Senegal reduces the survivorship of wild-caught, blood fed malaria vectors. Malar J 2010; 9: 365. CrossRef | PubMed

41 Bockarie MJ, Hii JLK, Alexander NDE, et al. Mass treatment with ivermectin for filariasis control in Papua New Guinea: impact on mosquito survival. Med Vet Entomol 1999; 13: 120-123. CrossRef | PubMed

42 Druilhe P, Tall A, Sokhna C. Worms can worsen malaria: towards a new means to roll back malaria?. Trends Parasitol 2005; 21: 359-362. CrossRef | PubMed

43 Metenou S, Dembele B, Konate S, et al. Filarial infection suppresses malaria-specific multifunctional Th1 and Th17 responses in malaria and filarial coinfections. J Immunol 2011; 186: 4725-4733. CrossRef | PubMed

44 Molyneux DH. 10 years of success in addressing lymphatic filariasis. Lancet 2009; 373: 529-530. Full Text | PDF(365KB) | CrossRef | PubMed

45 Webber RH. The natural decline of Wuchereria bancrofti infection in a vector control situation in the Solomon Islands. Trans R Soc Trop Med Hyg 1977; 71: 396-400. CrossRef | PubMed

46 Webber RH. Eradication of Wuchereria bancrofti infection through vector control. Trans R Soc Trop Med Hyg 1979; 73: 722-724. CrossRef | PubMed

47 Rajagopalan PK, Panicker KN, Das PK. Control of malaria and filariasis vectors in South India. Parasitol Today 1987; 3: 233-241. CrossRef | PubMed

48 Rajagopalan PK, Das PK, Pani SP, et al. Evaluation of integrated vector control measures on filariasis transmission in Pondicherry. Indian J Med Res 1988; 87: 434-439. PubMed

49 Burkot TR, Garner P, Paru R, et al. Effects of untreated bed nets on the transmission of Plasmodium falciparum, P. vivax and Wuchereria bancrofti in Papua New Guinea. Trans R Soc Trop Med Hyg 1990; 84: 773-779. CrossRef | PubMed

50 Prybylski D, Alto WA, Mengeap S, Odaibaiyue S. Introduction of an integrated community-based bancroftian filariasis control program into the Mt Bosavi region of the Southern Highlands of Papua New Guinea. PNG Med J 1994; 37: 82-89. PubMed

51 Bøgh C, Pedersen EM, Mukoko DA, Ouma JH. Permethrin-impregnated bednet effects on resting and feeding behaviour of lymphatic filariasis vector mosquitoes in Kenya. Med Vet Entomol 1998; 12: 52-59. CrossRef | PubMed

52 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-S95. PubMed

53 Bockarie MJ, Tavul L, Kastens W, Michael E, Kazura JW. Impact of untreated bednets on prevalence of Wuchereria bancrofti transmitted by Anopheles farauti in Papua New Guinea. Med Vet Entomol 2002; 16: 116-119. CrossRef | PubMed

54 Odermatt P, Leang R, Bin B, Bunkea T, Socheat D. Prevention of lymphatic filariasis with insecticide-treated bednets in Cambodia. Ann Trop Med Parasitol 2008; 102: 135-142. CrossRef | PubMed

55 Ashton RA, Kyabayinze DJ, Opio T, et al. The impact of mass drug administration and long-lasting insecticidal net distribution on Wuchereria bancrofti infection in humans and mosquitoes: an observational study in northern Uganda. Parasit Vectors 2011; 4: 134. PubMed

56 Maxwell CA, Curtis CF, Haji H, Kisumku S, Thalib AI, Yahya SA. Control of bancroftian filariasis by integrating therapy with vector control using polystyrene beads in wet pit latrines. Trans R Soc Trop Med Hyg 1990; 84: 709-714. CrossRef | PubMed

57 Maxwell CA, Mohammed K, Kisumku U, Curtis CF. Can vector control play a useful supplementary role against Bancroftian filariasis?. Bull World Health Organ 1999; 77: 138-143. PubMed

58 Curtis CF, Myamba J, Wilkes TJ. Comparison of different insecticides and fabrics for anti-mosquito bednets and curtains. Med Vet Entomol 1996; 10: 1-11. CrossRef | PubMed

59 Duerr HP, Dietz K, Eichner M. Determinants of the eradicability of filarial infections: a conceptual approach. Trends Parasitol 2005; 21: 88-96. CrossRef | PubMed

60 Michael E, Malecela-Lazaro MN, Kabali C, Snow LC, Kazura JW. Mathematical models and lymphatic filariasis control: endpoints and optimal interventions. Trends Parasitol 2007; 22: 226-233. CrossRef | PubMed

61 Southgate BA. Recent advances in the epidemiology and control of filarial infections including entomological aspects of transmission. Trans R Soc Trop Med Hyg 1984; 78: 19-28. CrossRef | PubMed

62 Okorie PN, McKenzie FE, Ademowo OG, Bockarie M, Kelly-Hope L. Nigeria Anopheles vector database: an overview of 100 years research. PLoS One 2011; 6: e28347. PubMed

63 Okwo-Bele JM, Cherian T. The expanded programme on immunization: a lasting legacy of smallpox eradication. Vaccine 2011; 29S: D74-D79. PubMed

64 Pichon G. Limitation and facilitation in the vectors and other aspects of the dynamics of filarial transmission: the need for vector control against Anopheles-transmitted filariasis. Ann Trop Med Parasitol 2002; 96 (suppl 2): S143-S152. PubMed

65 Kelly-Hope LA, Diggle PJ, Rowlingson BS, et al. Negative spatial association between lymphatic filariasis and malaria in West Africa. Trop Med Int Health 2006; 11: 129-135. PubMed

66 Foy BD, Kobylinski KC, Marques da Silva I, Rasgon JL, Sylla M. Endectocides for malaria control. Trends Parasitol 2011; 27: 423-428. CrossRef | PubMed

67 Russell TL, Govella NJ, Salumi Aziz S, Drakeley CJ, Kachur SP, Killeen GF. Increased proportions of outdoor feeding among residual malaria vector populations following increased use of insecticide-treated nets in rural Tanzania. Malar J 2011; 10: 80. CrossRef | PubMed

68 Trape JF, Tall A, Diagne N, et al. Malaria morbidity and pyrethroid resistance after the introduction of insecticide-treated bednets and artemisinin-based combination therapies: a longitudinal study. Lancet 2011; 11: 925-932. PubMed

69 Enayati A, Lines J, Maharaj R, Hemingway J. Suppressing the vector. In: Feachem RGA, Phillips AA, Targett GA, eds. Shrinking the malaria map: a prospectus on malaria elimination. San Francisco: The Global Health Group, Global Health Sciences, University of California, 2009: 143-154.

70 van den Berg H, Takken W. A framework for decision-making in integrated vector management to prevent disease. Trop Med Int Health 2007; 12: 1230-1238. CrossRef | PubMed

71 Burkot TR, Durrheim DN, Melrose WD, Speare R, Ichimori K. The argument for integrating vector control with multiple drug administration campaigns to ensure elimination of lymphatic filariasis. Filiaria J 2006; 5: 10. PubMed

72 WHO. Global malaria control and elimination: report of a technical review. Geneva: World Health Organization, 2008.

73 Beier JC, Keating J, Githure JI, Macdonald MB, Impoinvil DE, Novak RJ. Integrated vector management for malaria control. Malar J 2008; 7 (suppl 1): S4. CrossRef | PubMed

a Laboratory of Entomology, Wageningen University, Wageningen, Netherlands

b Centre for Neglected Tropical Diseases, Liverpool School of Tropical Medicine, Liverpool, UK

c School of Biological and Biomedical Sciences, Durham University, Durham, UK

Correspondence to: Henk van den Berg, Laboratory of Entomology, Wageningen University, PO Box 8031, 6700 EH Wageningen, Netherlands