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The Lancet 2005; 365:613-617
DOI:10.1016/S0140-6736(05)17913-6
New strategy against Aedes aegypti in Vietnam
Prof Brian KayPhD
a 
and Vu Sinh NamPhD b
See Comment
Summary
The strategy
Elimination of A aegypti
References
Summary
The container-breeding mosquito, Aedes aegypti, is the major global vector of dengue viruses, causing around 50 million infections annually. We have developed a mosquito control strategy, incorporating four elements: (1) a combined vertical and horizontal approach that depends on community understanding; (2) prioritised control according to the larval productivity of major habitat types; (3) use of predacious copepods of the genus Mesocyclops as a biological control agent; delivered by (4) community activities of health volunteers, schools, and the public. We have previously reported that, from 1998 to 2003, community-based vector control had resulted in A aegypti elimination in six of nine communes, with only small numbers of larvae detected in the others. Here, we report eradication in two further communes and, as a result of local expansion after the project in three northern provinces, elimination from 32 of 37 communes (309
730 people). As a result, no dengue cases have been detected in any commune since 2002. These findings suggest that this strategy is sustainable in Vietnam and applicable where the major sources of A aegypti are large water storage containers.
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Dengue, which is caused by four antigenically similar viruses, is the most common arthropod-borne virus infection globally, causing 50 million infections, 500000 cases of dengue haemorrhagic fever, and at least 12000 deaths per year.1 Before 1970, only nine countries had had the sometimes fatal dengue haemorrhagic fever, but by 1999, 60 countries had. This alarming situation has been caused by increased population movements by air travel, unprecedented population growth and overcrowding, uncontrolled and underserviced urbanisation (which severely affects on the poor), and deterioration of public-health infrastructure and mosquito control efforts.2 The container-breeding mosquito, Aedes aegypti, which is the major global vector of dengue, has been favoured by poor urban infrastructure such as an unreliable or absent water supply, which forces residents to store water, or no refuse collection, which results in accumulation of water-bearing discards suitable as larval habitats.3
Gubler4 reviewed the successful paramilitary-style house-to-house inspection approach of Gorgas and Soper (the vertical or top-down approach) in the Americas, but noted that most countries lacked the resources to be able to employ the thousands of inspectors and other support staff to maintain an effective campaign. Moreover, these programmes were not sustainable because they failed to transfer the responsibility for mosquito control to its rightful place: the community. Thus, a culture developed of governments promising what they could never deliver, and of a community taking no responsibility for their own health. Gubler4 advocated integration of both vertical and horizontal (or bottom-up) approaches (full responsibility by communities), which we report herein. Halstead5 has further analysed the factors leading the global failure of A aegypti control and concluded ?programs are broken beyond the power of mere money to fix them?.
An additional reason for failure has been the doctrine of container homogeneity, which is implicit in adoption of the standard larval indices?eg, Breteau index, house index, and container index?that were promoted by WHO from the 1970s.6 Although Breteau7 referred to his index (the number of positive containers per 100 houses) as an index of prevalence, it was promoted as an index of abundance, which compounded the error. Containers of different capacities, for example a 0?5 L bottle compared with a 5000 L concrete tank, can produce vastly different numbers of adult mosquitoes,8 so that to score them equally is absurd. This standard larval indices system, however, resulted in non-prioritised mosquito control, and a basic lack of understanding of what was causing the problem.
Thus, the objective of this report is to promote the key elements of our successful strategy on the basis of published studies on container productivity8 quantitative sampling methodologies,9?13 and use of copepods of the genus Mesocyclops in successful community-based programmes in Vietnam,14?18 and to add new data that show that such programmes are sustainable.
The strategy
Community programme and structure (element 1)
From 1998 to 2003, funding for phase 1 (northern provinces) and phase 2 (central provinces) was raised and managed by a non-governmental organisation, the Australian Foundation of Peoples of Asia and the Pacific. We have now started phase 3 operations in Long An, Vinh Long, and Ben Tre (figure). Technical expertise was provided by the Queensland Institute of Medical Research and the Queensland University of Technology in collaboration with local counterparts, led by the National Institute of Hygiene and Epidemiology (NIHE).
Click to enlarge image
Figure. Provinces in Vietnam where new dengue strategy is being used Numbers indicate incidence rates per 100000 people for 1998.
The vertical element of the strategy was directed through the Ministry of Health, which convenes the National Dengue Control Committee for oversight, with technical advice and training provided by four national institutes: NIHE in Hanoi with responsibility for 29 provinces (north); the Institut Pasteur Ho Chi Minh responsible for 20 provinces (south); Institut Pasteur, Nha Trang with another 11 (central); and Tay Nguyen Institute of Hygiene and Epidemiology with four provinces (highlands). Nominated institutional staff, Vietnamese project team staff, and advisers supervised implementation through provincial, district, and commune-level health staff.
For each commune, the Vietnamese project team and relevant provincial and district level representatives met with the People's Committee leader and commune health centre staff to fully discuss the strategy and to gain initial consent. After approval had been given, the horizontal component was guided by community project officers who provided monthly support in liaising at commune level, by attending project management committee meetings (the management group comprising key local figures) and undertaking knowledge, attitude, and practice surveys in the communities being evaluated for interventions. These officers attended communal functions, ran commune training for health collaborators and school teachers, helped development of schools programmes, and guided the commune level programme.
Prioritised control based on key container productivity (element 2)
From 1992, new quantitative methods were developed for sampling A aegypti larvae with purpose-designed nets10?12 or funnel traps9,12,13 to help understand container productivity and prioritisation of control based on key containers.8 Such quantitation based on numbers of third and fourth instar A aegypti and A albopictus facilitated the ranking of specific container type frequencies (in terms of total containers) as the estimated numbers of larvae within each container type. This ranking formed the basis for prioritising control according to the most productive container types and for monitoring control effectiveness, based on successive surveys every 3 months.
Mesocyclops as a local biological control agent (element 3)
Details of the effectiveness and number of Mesocyclops spp collected in Vietnam have been published,14?18 as have methods of mass culture. Local Mesocyclops spp were found during entomological surveys of containers in all communes while assessing the suitability of such communes for the establishment of dengue vector control programmes.
Samples of cyclopoid copepods were identified to species level at NIHE, mass cultured,16 and inocula of about 50 Mesocyclops each returned to the commune to be introduced into 20?50 public wells or large water stores with water characteristics amenable to copepod establishment. Roughly 4?6 weeks later, these large container habitats could be sampled and the Mesocyclops used for distribution throughout the commune. The inoculation process was usually driven by commune personnel and was done in stages, depending on availability of Mesocyclops. Health collaborators monitored progress monthly and were taught to record presence or absence of Aedes and to differentiate large cyclopoids from other copepods. Monthly collaborator survey records were checked every 3 months against survey data from the technical project team.
Community activities (element 4)
Dengue control was driven by the chairman of each commune, and by other leaders from the women's union and youth union, and implemented by communal health personnel, health collaborators, schoolteachers, and their pupils.
Health collaborators each were responsible for monthly inspection of about 100 houses, delivery of health education messages, and reporting of any suspected dengue cases to the communal health centre. Rating systems were developed for both collaborator and householder performance. Collaborators also assisted with periodic clean-up campaigns and with the distribution of Mesocyclops. For these duties, they were provided with an official uniform and paid US$2 per month. Such duties were part-time, usually occupying less than 4 days per month.
The extent of activities of schoolchildren varied by commune, but included clean-up campaigns of discarded containers, providing household support to the aged and infirm, and participation in dengue or project-oriented plays, songs, quiz nights, and in one district a Meso football cup.
The Australian Foundation of Peoples of Asia and the Pacific also managed a small projects scheme to foster new business activities or to improve returns on them that complemented the dengue control programme. For example, in **** Yen province, a recyclable waste compactor was bought to expedite removal of metal parts. As with discards, such parts were suitable as breeding habitats, but unsuitable for Mesocyclops inoculation. Some of the increased economic return was paid to the commune to cover collaborator costs after the project. The funding agencies usually attended annual programme meetings to confirm that milestones had been met and commented on written reports that were submitted to them.
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Elimination of A aegypti
We were pleased when our project team was able to report elimination of A aegypti from six northern communes in Nam Dinh, **** Yen (both rural), and Hai Phong (urban) from 1998 to 2000.16 Elimination in Lac Vien and Xuan Kien communes followed soon after project cessation. The original eradication from Phan Boi village14 in August, 1994, was extended to seven other villages that make up Di Su commune, with the last detection of A aegypti in September, 1999 (table 1). From 2000 to 2003, we worked under different social conditions in three central province communes (5913 households and 27167 people) in Quang Nam, Quang Ngai, and Khanh Hoa. A aegypti was eliminated at Cam Thanh and Binh Chanh, whereas the effectiveness of control in Ninh Xuan was 99?6% (11 third and fourth instars remaining).18 Dengue incidence data have been provided,16,18 but in the absence of, or with remnant numbers of A aegypti, this disease has been absent since 2001 (north) or 2002 (central), despite rates as high as 112?8 per 100000 in the surrounding untreated communes.
Table 1. Summary of control efficacy against A aegypti in nine northern and central communes by June 2003*
Sustainability of the strategy
From 2000 in the northern provinces, a control programme was started at Xuan Tien commune, Nam Dinh (1896 households, 9865 people), because it was one of the untreated controls from the 1998?2000 phase 1 project. However, control in Xuan Tien and for 36 other communes was overseen by provincial and district health personnel and implemented at commune level. A aegypti has been eliminated in 32 of these 37 communes, with low numbers remaining in five (table 2).
Table 2. Summary of effectiveness of control against A aegypti in 37 northern communes in Nam Dinh, **** Yen, and Hai Phong provinces, with locally directed programmes
Including project infrastructure, administration costs, and virological surveillance, as well as delivery of the entomological strategy, the average cost per person year was US$2, but our estimates of costs in the post-project expansion suggest approximately 0?20 cents. The returns from the small projects scheme initiated during the phase 1 project activities are VND70 million (US$ 4666), which ensures a monthly allowance of VND20000 (US$1?33) for each collaborator. In **** Yen, the control programme receives an extra VND10 million from the local authority in recognition of the benefits that dengue control brings to the community. During 2005, we will commence a study to examine the elements of this sustainability, including the driving force behind provincial, district, and community motivation, cost-effectiveness, and how the existing health system interacted with this programme.
Prognosis and risks
Except for the vertical strategies of Singapore and Cuba after the 1981 epidemic,4 broad-scale vector control has been a global disaster. This failure has resulted in an exponential increase in dengue and dengue haemorrhagic fever cases every decade since the 1960s.1?4 However, since viral surveillance and diagnosis is poor, and since only severe clinical cases may be recorded in notifiable diseases systems, the actual number of dengue cases is imprecise, but underestimated. Halstead described dengue as ?one of the great neglected diseases of mankind?,19 and Gubler has decried the 20 years of inaction and lack of funding to address this global crisis.3 Consideration of the economic cost of dengue has been based on individual epidemics and has ignored the total burden of disease through periods between epidemics, until the disability-adjusted life years approach was applied to Puerto Rico20 and via the World Health Report.21 The findings for Puerto Rico suggested a total effect similar to several other infectious diseases such as malaria, the childhood cluster (pertussis, polio, measles, tetanus), meningitis, and hepatitis for the Latin American and Caribbean region.
Because a paediatric dengue vaccine is probably 10 years away,22 our broad-scale success in dengue vector control is extremely important, but more importantly it has been embraced by local health personnel and by communities. In total, 386544 people have been protected from dengue since none of these communes has had cases since 2001.16,18 In the south, a Netherlands-Vietnam Medical Committee project in Kien Giang has returned similar results.
All four elements of the strategy are important to success. The development of quantitative methods for estimating numbers of third and fourth instar A aegypti is an essential precursor to identification of key container types,8 which directs prioritisation of control. Preliminary assessment of community knowledge, attitudes, and practice is crucial to establish whether dengue is viewed as a serious problem, its causes, possible intervention measures, and appropriate methods for delivering knowledge. If people, for example, believe dengue is ?ka dinga pepo? (a Swahili term for cramp-like seizure caused by evil spirits), then support is unlikely for a mosquito control strategy.
The third element?Mesocyclops copepods?represents a local low-cost option and a natural resource that already exists in most communes.15?18 Cyclopoids and Mesocyclops, but also Macrocyclops, Acanthocyclops, and Megacyclops23?25 are predacious on Aedes and Anopheles larvae, and some have been used mainly in field evaluations to control Aedes in large water storages (wells, tanks, large jars, drums) but also in tyre piles,25 land crab burrows,26 temporary pools,23 and small containers.24 However, in field trials in hundreds of tyres, use of Acanthocyclops vernalis was less successful at eliminating larvae than Macrocyclops and large Mesocyclops spp,23,27 and the same was true for rice fields, temporary pools, and marshes in Louisiana.23,28 In Vietnam, the main use for Mesocyclops has been in large water stores since these habitats represent the most productive habitats for A aegypti. Local health personnel, health collaborators, and schoolchildren can become adept at recognising Mesocyclops (or more correctly large cyclopoids) and Aedes larvae, and thus have no problem in servicing community needs.
Since 1953?54, dengue haemorrhagic fever emerged in Asia and has reached crisis point, with a later but similar expansion in the western hemisphere. Its effects have been exacerbated by high population growth and the fact that most people without a water supply live in Asia.21 Many communities, especially rural ones, have pre-existing populations of Mesocyclops awaiting integration as one element in our strategic model. As agreed with WHO, we advocate our model only in countries that are free of Guinea worm because Mesocyclops are intermediate hosts. In Vietnam, the potential for exacerbation of relatively rare parasitic conditions caused by Gnathostoma and Diphyllobothrium is virtually nil, as evidenced by dissection of over 15000 Mesocyclops and by comparison of ophthalmological case data from five provinces in which Mesocyclops has been adopted for control of A aegypti.29 There is no association between the suggested vertebrate hosts of these parasites and the types of large water storage containers that are the major target of our control programmes.
Although this model has been applied successfully in some communes in urban Hai Phong, use of Mesocyclops alone is unlikely to provide the major solution in cities with reticulated water, and with household waste, discards, and bases under potted plants, which contribute to the production of A aegypti. Rather, this copepod may be used as a tool for control in specified environments?large volume habitats, eg, tyre piles25 and subterranean service manhole systems.30 Thus, other solutions are urgently needed.
Although the government of Vietnam has adopted this strategy into their national programme, the challenge is to transfer this framework to the rest of southeast Asia and beyond. Whereas the hierarchical structure of society in Vietnam undoubtedly affected successful adoption of our model, we judge the key factor in motivating communities to be perception of the seriousness of the dengue problem, and willingness to take responsibility. As the global prognosis is poor, we predict that this model, or modifications of it, will become increasingly important.
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Contributors
Both authors contributed equally to the study. B Kay wrote the original manuscript.
Conflict of interest statement
We declare that we have no conflict of interest.
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Acknowledgments
We thank our team members involved in implementation; the Australian Foundation of Peoples of Asia and the Pacific, National Institute of Hygiene and Epidemiology, Institut Pasteur Nha Trang, the provincial, district, and commune health staff, and the communities in which we worked. Peter Ryan (Queensland Institute of Medical Research) and John Aaskov (Queensland University of Technology) reviewed the original manuscript and Gerald Marten (Kwansei Gakuin University) provided additional comment. The study was funded by the Australian and UK governments under their respective foreign aid programmes: AusAID (1998?2003) and the Department for International Development (1998?2000). The sponsors of the study had no role in study design, data collection, data analysis, data interpretation, or writing of the report. The corresponding author had full access to all the data in the study and had final responsibility for the decision to submit for publication.
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<!--start tail=-->References
1. Secretariat of Fifty-fifth World Health Assembly. Dengue prevention and control. Dengue Bull 2002; 26: 218-220.
2. Lifson AR Mosquitoes, models, and dengue. Lancet 1996; 347: 1201-1202. MEDLINE | CrossRef
3. Gubler DJ. Epidemic dengue/dengue hemorrhagic fever as a public health, social and economic problem in the 21st century. Trends Microbiol 2002; 10: 100-103. CrossRef
4. Gubler DJ. Aedes aegypti and Aedes aegypti-borne disease control in the 1990s: top down or bottom up. Am Trop Med Hyg 1989; 40: 571-578.
5. Halstead SB. Dengue haemorrhagic fever: why can't we control it?. Arbovirus Res Australia 1987; 4: 30-35.
6. World Health Organization. . Weekly Epidemiological Record 1972; 47: 73-84.
7. Breteau H. La fievre jaune en Afrique occidentale fran?aise. Un aspect de la medicine preventive massive. Bull World Health Organ 1954; 11: 453-481. MEDLINE
8. Tun-Lin W, Kay BH, Barnes A. Understanding productivity, a key to Aedes aegypti surveillance. Am J Trop Med Hyg 1995; 53: 595-601. MEDLINE
9. Kay BH, Cabral CP, Araujo DB, Ribeiro ZM, Braga PH, Sleigh AC. Evaluation of a funnel trap for the collection of copepods and immature mosquitoes from wells. J Am Mosq Control Assoc 1992; 8: 372-375. MEDLINE
10. Zhen TM, Kay BH. Comparison of sampling efficacy of sweeping and dipping for Aedes aegypti larvae in tires. J Am Mosq Control Assoc 1993; 9: 316-320. MEDLINE
11. Tun-Lin W, Kay BH, Burkot TR. Quantitative sampling of immature Aedes aegypti in metal drums using sweep net and dipping methods. J Am Mosq Control Assoc 1994; 10: 390-396. MEDLINE
12. Russell BM, Kay BH. Calibrated funnel trap for quantifying mosquito (Diptera: Culicidae) abundance in wells. J Med Entomol 1999; 36: 851-855.
13. Nam VS, Ryan PA, Yen NT, Phong TV, Marchand RP, Kay BH. Quantitative evaluation of funnel traps for sampling Aedes aegypti immatures from water storage jars. J Am Mosq Control Assoc 2003; 19: 220-227.
14. Nam VS, Yen NT, Kay BH, Marten GG, Reid JW. Eradication of Aedes aegypti from a village in Vietnam using copepods and community participation. Am J Trop Med Hyg 1998; 59: 657-660.
15. Nam VS, Yen NT, Holynska M, Reid JW, Kay BH. National progress in dengue vector control in Vietnam; survey for Mesocyclops (Copepoda), Micronecta (Corixidae) and fish as biological control agents. Am J Trop Med Hyg 2000; 62: 5-10.
16. Kay BH, Nam VS, Tien TV, et al. Control of Aedes vectors of dengue in three provinces of Vietnam, using Mesocyclops (Copepoda) and community based methods, validated by entomologic, clinical and serologic surveillance. Am J Trop Med Hyg 2002; 66: 40-48.
17. Kay BH, Nam VS, Yen NT, Tien TV, Holynska M. Successful dengue vector control in Vietnam: A model for regional consideration. Arbovirus Res Australia 2001; 8: 187-193.
18. Nam VS, Yen NT, Phong TU, et al. Elimination of dengue by community programs using Mesocyclops (Copepoda) against Aedes aegypti in central Vietnam. Am J Trop Med Hyg 2005; 72: 79-85.
19. Halstead S. The xxth century dengue pandemic: need for surveillance and research. World Health Stat Q 1992; 45: 292-298. MEDLINE
20. Meltzer MI, Rigau-Perez JG, Clark GC, Reiter P, Gubler DJ. Using disability-adjusted life years to assess the economic impact of dengue in Puerto Rico: 1984?1994. Am J Trop Med Hyg 1998; 59: 265-271.
21. United Nations. Water for People. Water for LifeThe United Nations World Water Development Report 2003. Barcelona: UNESCO and Berghahn Books, 2003:.
22. Almond J, Clemens J, Engers H, et al. Accelerating the development and introduction of a dengue vaccine for poor children, 5?8 December 2001, Ho Chi Minh City, Vietnam. Vaccine 2002; 20: 3043-3046. CrossRef
23. Marten GG, Bordes ES, Nguyen M. Use of cyclopoid copepods for mosquito control. Hydrobiologia 1994; 292/293: 491-496.
24. Dieng H, Boots M, Tuno N, Tsuda Y, Takagi M. A laboratory and field evaluation of Macrocyclops distinctus, Megacyclops viridis and Mesocyclops pehpeiensis as control agents of the dengue vector Aedes albopictus in a peridomestic area in Nagasaki, Japan. Med Vet Entomol 2002; 16: 285-291. CrossRef
25. Marten GG. Elimination of Aedes albopictus from tire piles by introducing Macrocyclops albidus (Copepoda, Cyclopidae). J Am Mosq Control Assoc 1990; 6: 689-693. MEDLINE
26. Lardeux F, Riviere F, Sechan Y, Kay BH. Release of Mesocyclops aspericornis (Copepoda) for control of larval Aedes polynesiensis in land crab burrows, on an atoll in French Polynesia. J Med Entomol 1992; 29: 571-576. MEDLINE
27. Marten GG. Evaluation of cyclopoid copepods for Aedes albopictus control in tires. J Am Mosq Control Assoc 1990; 6: 681-688. MEDLINE
28. Marten GG, Nyuyen M, Ngo M. Copepod predation on Anopheles quadrimaculatus larvae in rice fields. J Vector Ecol 2000; 25: 1-6.
29. Than PV, Phuong TTK. Observation on the eye and dermal parasite diseases related to Mesocyclops. J Practice Med, MoH, Vietnam 2004; 477: 89-93.
30. Kay BH, Lyons SA, Holt JS, Holynska M, Russell BM. Point source inoculation of Mesocyclops (Copepoda: Cyclopidae) gives broad-acre control of Ochlerotatus and Aedes immatures in service manholes and pits in north Queensland, Australia. J Med Entomol 2002; 39: 469-474.
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DOI:10.1016/S0140-6736(05)17913-6
New strategy against Aedes aegypti in Vietnam
Prof Brian KayPhD
a and Vu Sinh NamPhD bSee Comment
Summary
The strategy
Elimination of A aegypti
References
Summary
The container-breeding mosquito, Aedes aegypti, is the major global vector of dengue viruses, causing around 50 million infections annually. We have developed a mosquito control strategy, incorporating four elements: (1) a combined vertical and horizontal approach that depends on community understanding; (2) prioritised control according to the larval productivity of major habitat types; (3) use of predacious copepods of the genus Mesocyclops as a biological control agent; delivered by (4) community activities of health volunteers, schools, and the public. We have previously reported that, from 1998 to 2003, community-based vector control had resulted in A aegypti elimination in six of nine communes, with only small numbers of larvae detected in the others. Here, we report eradication in two further communes and, as a result of local expansion after the project in three northern provinces, elimination from 32 of 37 communes (309
730 people). As a result, no dengue cases have been detected in any commune since 2002. These findings suggest that this strategy is sustainable in Vietnam and applicable where the major sources of A aegypti are large water storage containers.Back to top
Dengue, which is caused by four antigenically similar viruses, is the most common arthropod-borne virus infection globally, causing 50 million infections, 500
000 cases of dengue haemorrhagic fever, and at least 12000 deaths per year.1 Before 1970, only nine countries had had the sometimes fatal dengue haemorrhagic fever, but by 1999, 60 countries had. This alarming situation has been caused by increased population movements by air travel, unprecedented population growth and overcrowding, uncontrolled and underserviced urbanisation (which severely affects on the poor), and deterioration of public-health infrastructure and mosquito control efforts.2 The container-breeding mosquito, Aedes aegypti, which is the major global vector of dengue, has been favoured by poor urban infrastructure such as an unreliable or absent water supply, which forces residents to store water, or no refuse collection, which results in accumulation of water-bearing discards suitable as larval habitats.3Gubler4 reviewed the successful paramilitary-style house-to-house inspection approach of Gorgas and Soper (the vertical or top-down approach) in the Americas, but noted that most countries lacked the resources to be able to employ the thousands of inspectors and other support staff to maintain an effective campaign. Moreover, these programmes were not sustainable because they failed to transfer the responsibility for mosquito control to its rightful place: the community. Thus, a culture developed of governments promising what they could never deliver, and of a community taking no responsibility for their own health. Gubler4 advocated integration of both vertical and horizontal (or bottom-up) approaches (full responsibility by communities), which we report herein. Halstead5 has further analysed the factors leading the global failure of A aegypti control and concluded ?programs are broken beyond the power of mere money to fix them?.
An additional reason for failure has been the doctrine of container homogeneity, which is implicit in adoption of the standard larval indices?eg, Breteau index, house index, and container index?that were promoted by WHO from the 1970s.6 Although Breteau7 referred to his index (the number of positive containers per 100 houses) as an index of prevalence, it was promoted as an index of abundance, which compounded the error. Containers of different capacities, for example a 0?5 L bottle compared with a 5000 L concrete tank, can produce vastly different numbers of adult mosquitoes,8 so that to score them equally is absurd. This standard larval indices system, however, resulted in non-prioritised mosquito control, and a basic lack of understanding of what was causing the problem.
Thus, the objective of this report is to promote the key elements of our successful strategy on the basis of published studies on container productivity8 quantitative sampling methodologies,9?13 and use of copepods of the genus Mesocyclops in successful community-based programmes in Vietnam,14?18 and to add new data that show that such programmes are sustainable.
The strategy
Community programme and structure (element 1)
From 1998 to 2003, funding for phase 1 (northern provinces) and phase 2 (central provinces) was raised and managed by a non-governmental organisation, the Australian Foundation of Peoples of Asia and the Pacific. We have now started phase 3 operations in Long An, Vinh Long, and Ben Tre (figure). Technical expertise was provided by the Queensland Institute of Medical Research and the Queensland University of Technology in collaboration with local counterparts, led by the National Institute of Hygiene and Epidemiology (NIHE).
Click to enlarge image
Figure. Provinces in Vietnam where new dengue strategy is being used Numbers indicate incidence rates per 100
000 people for 1998.The vertical element of the strategy was directed through the Ministry of Health, which convenes the National Dengue Control Committee for oversight, with technical advice and training provided by four national institutes: NIHE in Hanoi with responsibility for 29 provinces (north); the Institut Pasteur Ho Chi Minh responsible for 20 provinces (south); Institut Pasteur, Nha Trang with another 11 (central); and Tay Nguyen Institute of Hygiene and Epidemiology with four provinces (highlands). Nominated institutional staff, Vietnamese project team staff, and advisers supervised implementation through provincial, district, and commune-level health staff.
For each commune, the Vietnamese project team and relevant provincial and district level representatives met with the People's Committee leader and commune health centre staff to fully discuss the strategy and to gain initial consent. After approval had been given, the horizontal component was guided by community project officers who provided monthly support in liaising at commune level, by attending project management committee meetings (the management group comprising key local figures) and undertaking knowledge, attitude, and practice surveys in the communities being evaluated for interventions. These officers attended communal functions, ran commune training for health collaborators and school teachers, helped development of schools programmes, and guided the commune level programme.
Prioritised control based on key container productivity (element 2)
From 1992, new quantitative methods were developed for sampling A aegypti larvae with purpose-designed nets10?12 or funnel traps9,12,13 to help understand container productivity and prioritisation of control based on key containers.8 Such quantitation based on numbers of third and fourth instar A aegypti and A albopictus facilitated the ranking of specific container type frequencies (in terms of total containers) as the estimated numbers of larvae within each container type. This ranking formed the basis for prioritising control according to the most productive container types and for monitoring control effectiveness, based on successive surveys every 3 months.
Mesocyclops as a local biological control agent (element 3)
Details of the effectiveness and number of Mesocyclops spp collected in Vietnam have been published,14?18 as have methods of mass culture. Local Mesocyclops spp were found during entomological surveys of containers in all communes while assessing the suitability of such communes for the establishment of dengue vector control programmes.
Samples of cyclopoid copepods were identified to species level at NIHE, mass cultured,16 and inocula of about 50 Mesocyclops each returned to the commune to be introduced into 20?50 public wells or large water stores with water characteristics amenable to copepod establishment. Roughly 4?6 weeks later, these large container habitats could be sampled and the Mesocyclops used for distribution throughout the commune. The inoculation process was usually driven by commune personnel and was done in stages, depending on availability of Mesocyclops. Health collaborators monitored progress monthly and were taught to record presence or absence of Aedes and to differentiate large cyclopoids from other copepods. Monthly collaborator survey records were checked every 3 months against survey data from the technical project team.
Community activities (element 4)
Dengue control was driven by the chairman of each commune, and by other leaders from the women's union and youth union, and implemented by communal health personnel, health collaborators, schoolteachers, and their pupils.
Health collaborators each were responsible for monthly inspection of about 100 houses, delivery of health education messages, and reporting of any suspected dengue cases to the communal health centre. Rating systems were developed for both collaborator and householder performance. Collaborators also assisted with periodic clean-up campaigns and with the distribution of Mesocyclops. For these duties, they were provided with an official uniform and paid US$2 per month. Such duties were part-time, usually occupying less than 4 days per month.
The extent of activities of schoolchildren varied by commune, but included clean-up campaigns of discarded containers, providing household support to the aged and infirm, and participation in dengue or project-oriented plays, songs, quiz nights, and in one district a Meso football cup.
The Australian Foundation of Peoples of Asia and the Pacific also managed a small projects scheme to foster new business activities or to improve returns on them that complemented the dengue control programme. For example, in **** Yen province, a recyclable waste compactor was bought to expedite removal of metal parts. As with discards, such parts were suitable as breeding habitats, but unsuitable for Mesocyclops inoculation. Some of the increased economic return was paid to the commune to cover collaborator costs after the project. The funding agencies usually attended annual programme meetings to confirm that milestones had been met and commented on written reports that were submitted to them.
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Elimination of A aegypti
We were pleased when our project team was able to report elimination of A aegypti from six northern communes in Nam Dinh, **** Yen (both rural), and Hai Phong (urban) from 1998 to 2000.16 Elimination in Lac Vien and Xuan Kien communes followed soon after project cessation. The original eradication from Phan Boi village14 in August, 1994, was extended to seven other villages that make up Di Su commune, with the last detection of A aegypti in September, 1999 (table 1). From 2000 to 2003, we worked under different social conditions in three central province communes (5913 households and 27
167 people) in Quang Nam, Quang Ngai, and Khanh Hoa. A aegypti was eliminated at Cam Thanh and Binh Chanh, whereas the effectiveness of control in Ninh Xuan was 99?6% (11 third and fourth instars remaining).18 Dengue incidence data have been provided,16,18 but in the absence of, or with remnant numbers of A aegypti, this disease has been absent since 2001 (north) or 2002 (central), despite rates as high as 112?8 per 100000 in the surrounding untreated communes.Click to view table
Table 1. Summary of control efficacy against A aegypti in nine northern and central communes by June 2003*
Sustainability of the strategy
From 2000 in the northern provinces, a control programme was started at Xuan Tien commune, Nam Dinh (1896 households, 9865 people), because it was one of the untreated controls from the 1998?2000 phase 1 project. However, control in Xuan Tien and for 36 other communes was overseen by provincial and district health personnel and implemented at commune level. A aegypti has been eliminated in 32 of these 37 communes, with low numbers remaining in five (table 2).
Click to view table
Table 2. Summary of effectiveness of control against A aegypti in 37 northern communes in Nam Dinh, **** Yen, and Hai Phong provinces, with locally directed programmes
Including project infrastructure, administration costs, and virological surveillance, as well as delivery of the entomological strategy, the average cost per person year was US$2, but our estimates of costs in the post-project expansion suggest approximately 0?20 cents. The returns from the small projects scheme initiated during the phase 1 project activities are VND70 million (US$ 4666), which ensures a monthly allowance of VND20
000 (US$1?33) for each collaborator. In **** Yen, the control programme receives an extra VND10 million from the local authority in recognition of the benefits that dengue control brings to the community. During 2005, we will commence a study to examine the elements of this sustainability, including the driving force behind provincial, district, and community motivation, cost-effectiveness, and how the existing health system interacted with this programme.Prognosis and risks
Except for the vertical strategies of Singapore and Cuba after the 1981 epidemic,4 broad-scale vector control has been a global disaster. This failure has resulted in an exponential increase in dengue and dengue haemorrhagic fever cases every decade since the 1960s.1?4 However, since viral surveillance and diagnosis is poor, and since only severe clinical cases may be recorded in notifiable diseases systems, the actual number of dengue cases is imprecise, but underestimated. Halstead described dengue as ?one of the great neglected diseases of mankind?,19 and Gubler has decried the 20 years of inaction and lack of funding to address this global crisis.3 Consideration of the economic cost of dengue has been based on individual epidemics and has ignored the total burden of disease through periods between epidemics, until the disability-adjusted life years approach was applied to Puerto Rico20 and via the World Health Report.21 The findings for Puerto Rico suggested a total effect similar to several other infectious diseases such as malaria, the childhood cluster (pertussis, polio, measles, tetanus), meningitis, and hepatitis for the Latin American and Caribbean region.
Because a paediatric dengue vaccine is probably 10 years away,22 our broad-scale success in dengue vector control is extremely important, but more importantly it has been embraced by local health personnel and by communities. In total, 386
544 people have been protected from dengue since none of these communes has had cases since 2001.16,18 In the south, a Netherlands-Vietnam Medical Committee project in Kien Giang has returned similar results.All four elements of the strategy are important to success. The development of quantitative methods for estimating numbers of third and fourth instar A aegypti is an essential precursor to identification of key container types,8 which directs prioritisation of control. Preliminary assessment of community knowledge, attitudes, and practice is crucial to establish whether dengue is viewed as a serious problem, its causes, possible intervention measures, and appropriate methods for delivering knowledge. If people, for example, believe dengue is ?ka dinga pepo? (a Swahili term for cramp-like seizure caused by evil spirits), then support is unlikely for a mosquito control strategy.
The third element?Mesocyclops copepods?represents a local low-cost option and a natural resource that already exists in most communes.15?18 Cyclopoids and Mesocyclops, but also Macrocyclops, Acanthocyclops, and Megacyclops23?25 are predacious on Aedes and Anopheles larvae, and some have been used mainly in field evaluations to control Aedes in large water storages (wells, tanks, large jars, drums) but also in tyre piles,25 land crab burrows,26 temporary pools,23 and small containers.24 However, in field trials in hundreds of tyres, use of Acanthocyclops vernalis was less successful at eliminating larvae than Macrocyclops and large Mesocyclops spp,23,27 and the same was true for rice fields, temporary pools, and marshes in Louisiana.23,28 In Vietnam, the main use for Mesocyclops has been in large water stores since these habitats represent the most productive habitats for A aegypti. Local health personnel, health collaborators, and schoolchildren can become adept at recognising Mesocyclops (or more correctly large cyclopoids) and Aedes larvae, and thus have no problem in servicing community needs.
Since 1953?54, dengue haemorrhagic fever emerged in Asia and has reached crisis point, with a later but similar expansion in the western hemisphere. Its effects have been exacerbated by high population growth and the fact that most people without a water supply live in Asia.21 Many communities, especially rural ones, have pre-existing populations of Mesocyclops awaiting integration as one element in our strategic model. As agreed with WHO, we advocate our model only in countries that are free of Guinea worm because Mesocyclops are intermediate hosts. In Vietnam, the potential for exacerbation of relatively rare parasitic conditions caused by Gnathostoma and Diphyllobothrium is virtually nil, as evidenced by dissection of over 15
000 Mesocyclops and by comparison of ophthalmological case data from five provinces in which Mesocyclops has been adopted for control of A aegypti.29 There is no association between the suggested vertebrate hosts of these parasites and the types of large water storage containers that are the major target of our control programmes.Although this model has been applied successfully in some communes in urban Hai Phong, use of Mesocyclops alone is unlikely to provide the major solution in cities with reticulated water, and with household waste, discards, and bases under potted plants, which contribute to the production of A aegypti. Rather, this copepod may be used as a tool for control in specified environments?large volume habitats, eg, tyre piles25 and subterranean service manhole systems.30 Thus, other solutions are urgently needed.
Although the government of Vietnam has adopted this strategy into their national programme, the challenge is to transfer this framework to the rest of southeast Asia and beyond. Whereas the hierarchical structure of society in Vietnam undoubtedly affected successful adoption of our model, we judge the key factor in motivating communities to be perception of the seriousness of the dengue problem, and willingness to take responsibility. As the global prognosis is poor, we predict that this model, or modifications of it, will become increasingly important.
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Contributors
Both authors contributed equally to the study. B Kay wrote the original manuscript.
Conflict of interest statement
We declare that we have no conflict of interest.
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Acknowledgments
We thank our team members involved in implementation; the Australian Foundation of Peoples of Asia and the Pacific, National Institute of Hygiene and Epidemiology, Institut Pasteur Nha Trang, the provincial, district, and commune health staff, and the communities in which we worked. Peter Ryan (Queensland Institute of Medical Research) and John Aaskov (Queensland University of Technology) reviewed the original manuscript and Gerald Marten (Kwansei Gakuin University) provided additional comment. The study was funded by the Australian and UK governments under their respective foreign aid programmes: AusAID (1998?2003) and the Department for International Development (1998?2000). The sponsors of the study had no role in study design, data collection, data analysis, data interpretation, or writing of the report. The corresponding author had full access to all the data in the study and had final responsibility for the decision to submit for publication.
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