Barriers and Bridges to Prevention and Control of Dengue: The Need for a Social–Ecological...

Barriers and Bridges to Prevention and Control of Dengue:The Need for a Social–Ecological Approach

Jerry Spiegel,1 Shannon Bennett,2 Libby Hattersley,3 Mary H. Hayden,4 Pattamaporn Kittayapong,5

Sustriayu Nalim,6 Daniel Nan Chee Wang,7 Emily Zielinski-Gutierrez,8 and Duane Gubler2

1Liu Institute for Global Issues, University of British Columbia, 203-6476 N.W. Marine Drive, Vancouver, British Columbia, Canada V6T 1Z22Asia-Pacific Institute of Tropical Medicine and Infectious Diseases, University of Hawaii, Honolulu, HI3Global Health Research Program, University of British Columbia, Vancouver, British Columbia, Canada4CU Trauma Center, NISSC, University of Colorado, Colorado Springs, CO5Center for Vectors and Vector-Borne Diseases and Department of Biology, Faculty of Science, Mahidol University, Bangkok, Thailand6Vector and Reservoir Control Research Unit, National Institute of Health Research and Development, Central Java, Indonesia7National Environment Agency, Singapore, Singapore8Division of Vector-Borne Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, GA

Abstract: This article critically examines how programs for the prevention and control of dengue fever have

been conducted in the absence of an integrated approach, and considers the social and ecological factors

influencing their effectiveness. Despite recognition of dengue fever as the most important arboviral disease

affecting humans, and in spite of a greater emphasis on community-based control approaches, the burden

placed on the communities, countries, and regions affected by this disease continues to rise. In considering

historical experience in the Americas and the Asia-Pacific region, as well as the global forces that are exerting

new pressures, the important elements of successful control programs are identified as community ownership,

partnership with government, leadership, scalability, and control of immature mosquitoes. The key barriers to

the exchange of knowledge and the transdisciplinary cooperation necessary for sustainable dengue control are

rooted in differences in values among policy-makers, citizens, and scientists and are repeatedly expressed in

technical, economic, cultural, geographic, and political dimensions. Through consideration of case studies in

Cuba, Guatemala, Singapore, Thailand, Indonesia, and Vietnam, the limitations of control approaches that fail

to take into account the complexities of ecological and social systems are presented. Bridges to effective control

are identified as the basis for adaptability, both of control programs to the mosquito vector’s changing behavior

and of education programs to public, regional and local particularities, as well as transdisciplinarity, com-

munity empowerment, the ability to scale local experiences up to the macro-level, and the capacity to learn

from experience to achieve sustainability.

Key words: dengue fever, Aedes aegypti mosquitoes, social and ecological systems, driving forces, community-

based, partnership

Published online: November 4, 2005

Correspondence to: Jerry Spiegel, e-mail: [email protected]

EcoHealth 2, 273–290, 2005DOI: 10.1007/s10393-005-8388-x

� 2005 EcoHealth Journal Consortium

INTRODUCTION AND BACKGROUND

Dengue fever (DF), the most important arboviral disease

affecting humans, is an increasingly significant cause of

morbidity and mortality in tropical and subtropical re-

gions around the world. Over half of the global human

population lives in areas of risk, and more than 100

countries are experiencing DF and/or dengue hemorrhagic

fever (DHF) epidemics in the early 21st century (Guha-

Sapir and Schimmer, 2005). Each year, there are an esti-

mated 50 to 100 million new dengue infections globally

(Gubler, 1998a, 2004), of which 500,000 are DHF, and

25,000 are fatal (Gubler, 1998a; Guzman and Kouri, 2002;

Guha-Sapir and Schimmer, 2005), although marked

underreporting results in the notification of far fewer

cases (Gubler, 1998b) (Fig. 1). The disease is endemic in

the Americas, southeast Asia region (SEAR), western Pa-

cific region (WPR), Africa, and the eastern Mediterranean,

with the major disease burden falling into the first three

regions (Guzman and Kouri, 2002; Renganathan et al.,

2003) (Fig. 2).

The clinical presentation and epidemiology of DF, an

acute viral disease caused by infection with any one of four

dengue virus serotypes (DENV-1, DENV-2, DENV-3,

DENV-4), is well understood and has been recently re-

viewed (Rigau-Perez et al., 1998; Guzman and Kouri,

2002). The dengue viruses are single-stranded RNA viruses

belonging to the family Flaviviridae, and are transmitted

principally in an urban cycle involving humans and Aedes

aegypti mosquitoes (Guzman and Kouri, 2002). In the ab-

sence of a vaccine, the emphasis has been on mosquito

control to prevent and control dengue epidemics (Rigau-

Perez et al., 1998). Although there have been some tem-

porary successes achieved in controlling dengue, these have

not persisted, partly because the single approach so often

taken, spraying against mosquitoes, is too costly to be

sustainable. While new and more effective approaches to

prevention and control are urgently required (Gubler,

1989), our scientific understanding of the factors that

influence success in this domain remains minimal.

Today’s climate of emerging infectious diseases amid

extensive global socio-economic change increasingly calls

Figure 1. Average annual number of dengue fever/

dengue hemorrhagic fever cases reported to the World

Health Organization, 1955–2003.

Figure 2. World distribution of Aedes

aegypti, 2005.

274 Jerry Spiegel et al.

for integrative, adaptive approaches that recognize the

complexities inherent in intertwined and constantly

evolving social-ecological systems (SES) (Wilcox and Gu-

bler, 2005; Gunderson et al., 1995). This requires building

bridges between disciplines and decision-makers not tra-

ditionally in the ‘‘disease control’’ network, so that the

driving forces that produce vulnerability to disease can be

altered ‘‘upstream’’ from where effects are manifest, rec-

ognizing the fundamental institutional and knowledge-re-

lated barriers that must be overcome to achieve the needed

intersectoral collaboration. The failure of previous linear

modes of understanding and their policy prescriptions

(such as a reliance on mosquito spraying), for example,

challenges us to broaden our understanding of the behav-

iors of complex natural systems, including their resilience

in the face of changing pressures (Levin, 1999; Holling,

2001), and how social institutions must comparably re-

spond (Gunderson, 2002; Gunderson et al., 1995). The SES

approach to dengue control accordingly applies multiple

methodologies to target the mosquito vector at all life-

stages, as well as continuous community engagement at all

levels to ensure adaptive intervention.

This article is the result of a workshop, Social–Ecolog-

ical Systems and Emerging Infectious Diseases, hosted by the

East-West Center and the University of Hawaii’s Asia-

Pacific Institute of Tropical Medicine and Infectious Dis-

eases in Honolulu, March 2005. Its purpose was to facilitate

interdisciplinary integration as part of National Institutes

of Health (NIH) Roadmap initiative Research Teams of the

Future (Lewis, 2005), applying a coupled, human–natural

systems approach to emerging infectious diseases (Wilcox

and Colwell, 2005); in this case, to the dengue virus. The

specific purpose of this article is thus to critically examine

approaches for preventing and controlling DF/DHF,

drawing lessons from a variety of community case studies

from the Americas and Asia, to identify barriers and

bridges to effective intervention, and to recommend new

strategies and approaches for effectively controlling this

disease. Knowledge and organizational requirements for

sustaining success will be emphasized, with regard to both

ecological and social systems.

Historical Overview of Dengue Control

DF/DHF has never been effectively contained in the Asia-

Pacific region, with the notable exception of Singapore. In

the Americas, on the other hand, epidemic dengue was

successfully controlled from 1945 until the late 1970s,

with the exception of sporadic DF epidemics in the

Caribbean islands (Gubler and Trent, 1993; Gubler, 1997).

The highly successful program, spearheaded by the Pan

American Health Organization (PAHO) amid yellow fever

epidemic concerns (Guzman and Kouri, 2003), was based

on A. aegypti larval control in domestic water storage and

collection containers and emphasized insecticide use

(particularly DDT). It was a vertically structured, para-

military approach, without community involvement

(Soper, 1943; Schliessman and Calheiros, 1974). As a re-

sult of this program, epidemic dengue transmission was

prevented in most of the tropical American region for 30

years (Guzman and Kouri, 2003). It was, however, a

classic example of success breeding failure, eventually

being disbanded in the early 1970s (Gubler, 1998b) when,

in the absence of DF/DHF epidemics, there was no longer

a perceived need for such an expensive program (Gubler,

1989).

Amid competing priorities for resources, major policy

changes at this time included the merging of dengue and

yellow fever control with malaria control, and the use of

ultra-low-volume adulticides as the recommended method

to control A. aegypti, and thus DF. Both these decisions

were major policy failures and ultimately ineffective in

preventing the reemergence of epidemic DF and the

emergence of DHF in the region (Gubler, 2005).

During the 1970s and 1980s, A. aegypti reinfested most

of the countries from which it had been eliminated (WHO,

1997). Generally, within a few years of reinfestation, these

countries experienced epidemic DF, followed by hyperen-

demicity and the emergence of DHF (Gubler, 1997; Pin-

heiro and Corber, 1997). Alarm-bells were sounded,

however little has been accomplished to reverse the trend of

increasing epidemic activity, and, in a short period of 20

years, this disease went from virtual nonexistence to one of

the region’s most important public health problems at the

dawn of the 21st century (Gubler, 2002; Guzman and

Kouri, 2002).

During the 1980s, in an effort to achieve sustainable

A. aegypti control, the emphasis was shifted from a top-down

to a bottom-up approach (Gubler, 1989). The goal was to

convince people living in the homes in which most trans-

mission was occurring to take ownership of household and

neighborhood mosquito control. The term ‘‘bottom-up’’

refers to an integrated community-based approach to mos-

quito control by environmental management, with increased

emphasis placed on health education, and community-

ownership (Gubler, 1989; WHO, 2001; Renganathan, 2003).

Prevention and Control of Dengue 275

This public health approach, combining active surveillance,

emergency response, case management, and community-

based A. aegypti control (Gubler and Casta-Velez, 1991)

received wide acceptance in the 1990s, became the basis for

the World Health Organization (WHO) global strategy for

prevention and control of DF/DHF (WHO, 2001) and was

echoed regionally in declarations and programs in the

Americas (PAHO, 1994) and Asia Pacific region (WHO,

1999). Today, A. aegypti control programs based on active

community participation have been developed in numerous

countries worldwide (Parks et al., 2004). Nevertheless, suc-

cessful program implementation has remained a significant

challenge, and the spread of epidemic DF/DHF persists

(Fig. 3).

Global Driving Forces

Dengue’s progressive expansion and increasing impact on

vulnerable communities has accompanied a number of

trends in global human influences: rapid and unplanned

urbanization; population growth; increasingly inadequate

municipal services; increased use of nonbiodegradable

products (bottles, plastic, cans, tires, etc.); and an unprec-

edented growth in the movement of people and com-

modities via travel and commerce, all amid largely

ineffective mosquito control efforts (Gubler, 1989; Gubler,

1997; Gubler, 1998a; WHO, 2001). Above all, as A. aegypti

is a highly domesticated urban mosquito, the public health

problem posed by DF is particularly important in cities in

the tropical developing world, where aides to human–

mosquito interaction, such as unscreened housing, dense

residential areas with large numbers of household breeding

sites (such as containers and tires), and absence of waste

management, sewer, and water systems produce ideal

conditions for mosquito breeding in the domestic envi-

ronment. Thus, large populations of mosquitoes are living

in intimate contact with crowded human populations. In

addition, dengue endemic areas are spatially well-con-

nected, undermining the feasibility of eradication in iso-

lated locales. Furthermore, the public health capacity of

states was fundamentally weakened by fiscal restraints in

the 1970s, 1980s, and 1990s (Gubler, 1989; Rigau-Perez,

1998), creating even greater challenges to effective pre-

vention and control. Therefore, local circumstances have

been subject to driving forces that extend across both

spatial and temporal scales, well beyond the capacity of

local control efforts, and thus strategies are required that

reflect this.

ELEMENTS OF A SUCCESSFUL AND

SUSTAINABLE CONTROL PROGRAM

Through the experience of failed control efforts, we have

learned that the coupled human–natural interaction of

humans and dengue behaves as a complex adaptive system

that has undergone repeated phases of management ef-

forts from local to regional scales, much as described by

the ‘‘adaptive cycle’’ metaphor (i.e., Gunderson and

Holling, 2002), from ephemerally stable periods of mos-

quito control through to destabilized periods of release

and reorganization due to economic constraints, mosquito

recolonization, and rapid human expansion. Such man-

agement experiences have stimulated policy-makers and

researchers to review successes and failures, and consider

barriers to success and sustainability in dengue control.

Figure 3. Aedes aegypti distribution in

the Americas.


Given the need for broad synthesis and collaboration,

critical ‘‘barriers’’ can best be regarded as those that

fundamentally arise from differences in values among

policy-makers, citizens, and scientists and interfere with

the exchange of knowledge and the transdisciplinary

cooperation necessary for sustainable dengue control

(Gunderson et al., 1995). As a result, piecemeal policies

have developed, favoring the targeting of single elements

in an inefficient and unsustainable fashion (Holling,

1995), historically giving rise to vertically structured

intervention programs and approaches that have relied

almost exclusively on using insecticide application to

break the transmission cycle, proven to be incapable of

achieving sustainable control. Our review identifies the

following program elements as being critical to success

because they require bridging disciplines and the divergent

short-term objectives of the various interested parties in-

volved: (i) focus on immature mosquito control; (ii)

community ownership; (iii) partnership with government;

(iv) leadership; (v) scale; and (vi) adaptability.

Immature Mosquito Control

Programs that solely or primarily rely on eliminating adult

mosquitoes in crisis situations are doomed to failure

(Gubler, 1989; Newton and Reiter, 1992). While such

intervention plays an important contingency role in a

comprehensive program, and certainly generates the

greatest public satisfaction, it nonetheless entails consid-

erable and avoidable economic cost and ecological impact,

and should be strategically minimized. Therefore, the

emphasis should be on interrupting the transmission cycle

at an early phase through immature mosquito control. This

can only be achieved through an integrated approach that

addresses the complex, nonlinear behavior of the SES in

which the dengue virus exists (Gunderson et al., 1995;

Wilcox and Gubler, 2005).

Community Ownership

Community-based programs are increasingly being touted

as the key to successful control programs (Gubler and

Clark, 1996; Rifkin, 1996; Parks and Lloyd, 2004; Parks

et al., 2004), recognizing the fundamental importance of

mobilizing and channeling household-level behaviors and

capacities in eliminating mosquito breeding sites, reducing

exposure, and targeting efforts. What is actually meant by

‘‘community’’ must, of course, take into account social,

geographical, and political factors specific to a local con-

text, fully recognizing multi-cultural complexity (e.g., rur-

al–urban migration; diversity in norms and practices).

Above all, community engagement is best achieved through

creating and reinforcing local ownership of efforts, not

merely passively conveying information developed outside

of the community itself.

Partnership with Government

Community-based programs have often been viewed as an

economical alternative to government intervention.

However, the role of government in coordinating efforts

cannot be underestimated. Without a coordinated ‘‘top-

down’’ and ‘‘bottom-up’’ approach, successful imple-

mentation of control programs is unlikely to be achieved

and sustained (Gubler, 1989). Because dengue is only one

among many health problems faced by residents, gov-

ernment support is essential if coordination of control

efforts and stimulus to participate is to be maintained. For

example, visible concern on the part of government af-

firms the serious nature of the threat and validates the

need to continue source-reduction efforts at the local

level. The likelihood of success is further enhanced if a

wide range of local and regional partners are engaged in

the effort (Halstead, 2000), and government is in an

excellent position to facilitate and broadly extend this

process, especially to ensure coordination with clinical-

epidemiological recognition and management of dengue

cases in the context of timely feedback of information on

DF and vector incidence.

Leadership

Leadership at a local level guides the successful establish-

ment and follow-through of intervention programs. Those

executing the control project must take the time to identify

and enlist local leaders who have the credibility to ensure

buy-in by members of the community. Formal and infor-

mal local leaders have necessary insider knowledge of

neighborhood practices, and, as such, may be better able to

control mosquito breeding sites using environmental

management by enlisting community participation.

Investment of time and effort must go into the identifica-

tion of mosquito breeding sites, which may vary among

neighborhoods. Educational campaigns need to be targeted

locally and adapted seasonally to potentially changing

ecologies, both human and vector.


Scale

An important caveat to the above discussion is the stability

of the social structure at all scales. In this sense, what may

work in ideal circumstances may not necessarily lend itself

to wider application. Communities beset by insecurity,

influx of recent immigrants and/or extreme poverty may

lack the cohesion to work on source-reduction as a

concerted effort, and individuals may be hard-pressed to

focus daily efforts on reducing breeding sites. Under such

conditions, government agencies must still be held

responsible for mounting control efforts, although they

may be realistically able to respond only when necessary to

avoid an outbreak. The question remains as to the feasi-

bility of extending the local-level scale of successful com-

munity participation in immature mosquito control to a

‘‘macro’’ regional, national, or cross-border level.

Adaptability

In recognizing the dengue problem in the context of complex

social and ecological systems, the capacity to adapt becomes

an undeniable emergent property. Mosquitoes rapidly

recolonize sprayed territory. Female mosquitoes adapt to

utilize new breeding habitats, from disposable containers to

manhole covers, as old breeding sites are eliminated and new

ones become available. Any successful control strategy needs

to be similarly adaptable through a built-in monitoring

component that provides feedback to respond and adjust

with rapidly executable control measures. This adaptability

requires such changes be neither costly nor require major

changes in the infrastructure needed to execute them.

BARRIERS AND THEIR EXPRESSION

Fundamental differences in the value systems and short-term

objectives of the different sets of actors involved in man-

agement of dengue transmission form the bedrock for the

‘‘barriers’’ (Gunderson et al., 1995) that impede a transdis-

ciplinary and therefore adaptive and sustainable control

program. As a result, failed management strategies are often

directed towards single targets, policies are piecemeal, the

scale of focus is myopic in both time and space, and there is

an over-reliance or confidence that ignores the plasticity of

the system (Holling, 1995). How such approaches have failed

at effective dengue control can be readily observed by

examining the range of contexts in which they have been

manifest and expressed, while critically assessing each from

the perspective of the complex, integrated cycle that ulti-

mately impacts on the functional and adaptive capacities of

social and ecological systems (Gunderson et al., 1995).

Technical Cure-alls

Despite the unequivocal targeting of A. aegypti as the

principal vector of interest, an over-reliance on technical

management ‘‘solutions’’ is costly, unsustainable, falsely

lulls citizens into a state of complacence, and ultimately

leads to failure of control and resurgence when control

programs are dropped. Application of chemical insecti-

cides, for example, remains only minimally effective in

ultimately restricting human exposure to the vector. A. ae-

gypti is primarily an indoor-resting mosquito, greatly

reducing the potential of typical insecticide spraying to

penetrate resting sites. In addition, the residual effect of

most insecticides used today is limited, making periodic

application necessary, and thus effective vector control too

costly for most countries. Insecticide resistance, which oc-

curs in mosquito vector populations after continued

application of the same chemical compounds, or when

insecticides become freely used by several communities

with a lack of collaboration and technical skill, serves as

another significant impediment to sustainable control.

Persistence of insecticide application as an option is a

result of barriers to the exchange of knowledge required for

integrated mosquito control and cooperation among agen-

cies planning and implementing application regimes. Over-

coming these barriers requires bridging the gaps in inter-

agency communication, between individuals with different

disciplinary training, among other factors. For example,

when an understanding of the evolutionary ecology of

mosquito populations is integrated with that of the physio-

logical mechanisms of chemical controls used, sustainable

control measures become apparent. In the case of dengue,

insecticide application to control adult mosquitoes should be

limited to emergency response during disease epidemics, and

guidelines for monitoring insecticide use and insecticide

resistance should be continually updated. Reduction of

insecticide use could be achieved by integrating it with other

control approaches, such as lethal ovitraps and pyrethroid

impregnated curtains and bednets, although more research is

needed to assess the efficacy and feasibility of these measures.

In addition, research suggests that knowledge of mosquito

preference for certain containers can help to target and in-

crease the effectiveness of control of immatures.


Surveillance for both DF/DHF cases and vectors is also

of critical importance. However, dengue case reporting is

frequently delayed relative to time of transmission, nor

does it achieve anything near full coverage, hampering

control efforts. While an ideal on-line electronic case

reporting system could be a solution to this problem, this is

far from the reality of most developing country health

systems. Surveillance can fail at numerous stages: less severe

cases may never seek care, care providers may elect not to

collect a sample, samples collected may not arrive in suit-

able condition for analysis, and even laboratories with the

means for testing may lack sufficient supplies to fully

analyze all samples. Thus, in many countries, the resulting

surveillance data may reflect only a fraction of actual cases.

Unfortunately, surveillance for dengue mosquito vec-

tors has furthermore not routinely been effective because

vector indices and dengue epidemics have not always been

correlated. For example, the pupal index may be more

closely correlated with dengue transmission than the more

familiar larval indices (Focks, 2003). Research is still

ongoing to search for better vector indices and to achieve

agreement regarding their use.

False Economies

It is ironic that economically expensive approaches to

dengue control are favored when less costly government and

community cooperatively based programs would do, par-

ticularly since dengue afflicts poverty-stricken communities

greatest, where there is a lack of reliable disease-burden

estimates; i.e., who becomes clinically ill with DF/DHF and

what happens to them (clinic visits, hospitalizations, days

off work, etc.). Impoverished communities will only adopt

interventions when they can clearly see the economic ben-

efits, however lack of data currently makes it difficult to

demonstrate such benefits. Burden estimates are available

(Meltzer et al., 1998; Gubler and Meltzer, 1999) but these

are typically based on extrapolations from small datasets.

While resources are often expended during a dengue out-

break, the burden imposed by dengue during nonoutbreak

periods could be considerable, albeit ignored (Meltzer et al.,

1998; Gubler and Meltzer, 1999). Furthermore, there are

very few cost–benefit estimates available for existing inter-

ventions (e.g., larvae control) (Shepard et al., 2004).

Cultural Insensitivity or Gross Oversimplification

Given the necessary reliance on community mobilization

strategies to achieve larval mosquito control, programs that

ignore or gloss over the ‘‘cultural,’’ social structure or

heterogeneity across different scales will not succeed in

dengue transmission prevention. A first consideration must

be which unit of ‘‘community,’’ and therefore which as-

pects of culture, are being examined. The householder/

family, the neighborhood, the broader social units and,

indeed, the culture of the public health workforce and of

policymakers must all be considered.

Household

At the household level, the perceived risk for dengue, and

therefore motivation for taking action, may be low

(Fig. 4). People may not identify fevers as pertaining to

dengue infection, and laboratory diagnosis may be

unavailable. Dengue is frequently ‘‘invisible’’ during inter-

epidemic periods, and the seasonality of the disease can

further affect mobilization efforts. It is difficult to ask

people to prioritize dengue among other acute health and

environmental concerns, and the reduction in fatalities

due to advances in DHF treatment may reduce perceived

severity. Tragic fatalities do, sadly, serve to motivate

community action, though often too late to intervene in

the trajectory of the outbreak (Kouri et al., 1986; Deitz

et al., 1996).

Larval control activities typically focus on household

breeding sites, often taking the form over many years of a

broader focus on ‘‘cleanliness.’’ This approach may ulti-

mately prove inefficient by diverting attention away from

the most productive breeding sites, which may be out-of-

view or ‘‘acceptable’’ by cleanliness standards. Of course,

some items identified as disposable by researchers may in

fact have household function and are being saved for future

use. Though source reduction campaigns increasingly rec-

ognize this issue, control of these useful containers can

remain a problem.

It can also be challenging to engage householders in

prevention (and, arguably, may be epidemiologically

pointless) when vector breeding continues unabated in

neighboring households, commercial sites such as tire

shops, and ‘‘unregulated’’ sources such as informal dumps.

This highlights the need to consider the local human

ecology as a whole, rather than focusing on individual

actions.

Another household factor is the availability of indoor

climate control (air-conditioning), which was protective

during a dengue outbreak on the US–Mexico border

(Reiter et al., 2003). This ‘‘adaptation’’ of more affluent


populations, living in ‘‘sealed’’ environments where vec-

tor issues are reduced, is seldom available to the wider

population. Less income-dependent factors, such as

‘‘open’’ housing styles, adapted for and preferred in the

tropics, may also be a factor contributing to indoor

exposure to mosquitoes and these demand consideration

when developing interventions to reduce human–vector

contact.

Community

Level of community integration is an important factor to

consider when implementing a dengue transmission

control program. Areas with networks of volunteers and

institutions (such as churches and schools) present

greater opportunity for mobilization than newly urban-

izing zones with high levels of poverty and large numbers

of new migrants. In such communities, there may be few

households with intact families, limited relationships be-

tween neighbors, and large numbers of people working at

the subsistence level, with little time to participate in

mobilization efforts. Communities in regions of conflict,

likewise, are not suited to traditional mobilization ap-

proaches. Formative research prior to an intervention is

therefore critical, and has major implications for project

scale-up.

As already noted, rapid urbanization and other changes

in land-use also contribute to vast areas without adequate

services or infrastructure. Household water-storage is

widespread and, in expanding peri-urban areas, is com-

bined with massive numbers of people drawn into close

quarters. These areas often lack infrastructure to deal with

refuse, exacerbating the problem of potential breeding sites.

The influence of global consumer culture further adds to

this risk with disposable but nonbiodegradable water-

holding containers, vector breeding sites, proliferating

widely (Gubler, 1989).

Policy and Intervention Culture

Finally, the ‘‘culture’’ of interventions themselves is highly

relevant. Government-sponsored vector control is still

practiced in many dengue endemic areas, complicating

attempts to create community ownership of dengue control

programs. Educational interventions more directly,

including pre-testing of community-directed messages, can

be rare due to limited time and personnel. A tendency

toward the inertia of previously used messages and cam-

paigns can prevail regardless of proof of their efficacy. For

example, dispersing the broad message to ‘‘keep the patio

clean’’ and ‘‘control all household breeding sites,’’ despite

indications that a more limited number of containers may

house the majority of mosquito breeding sites, represents a

potential misdirection of community efforts.

Geographical

Migrating populations in search of work (and travelers in

general) have the potential to carry the dengue virus with

them, as does global shipping. Exponential growth in such

global interconnectivity highlights the importance of wider,

regional approaches to control. The rapid dissolution of the

dengue virus’ geographic impediments to transmission also

emphasizes the need to establish scalable and sustainable

Figure 4. Knowledge (left) and attitude (right) on dengue and vector control in Thailand.


adaptive approaches to dengue prevention and control, as

opposed to focusing on eradication.

Political

Dengue epidemics give rise to serious public concern and

alarm, as hundreds to thousands of new infections can arise

every week. The public must be kept informed, however,

heightened awareness further exacerbates the level of

concern. It is natural, therefore, that the public will turn to

the government for a solution, and yet, ironically, it will be

the government that must turn to the public to solve the

problem.

Despite the ineffectiveness of chemical control and its

potential collateral effects on nontarget organisms, insec-

ticides remain the leading dengue vector control method in

most developing countries. A significant contributing rea-

son for this is that adulticiding is a highly visible, and

therefore politically popular, method of control which

demonstrates that a government is responsive. While

adulticiding may provide some ‘‘psychological satisfaction’’

for both public health authorities and householders, this

can also create a false sense of security among both gov-

ernment officials and the public (Gubler, 1989).

In fact, the control of dengue can only be effective

when the entire community agrees to accept responsibility

to prevent A. aegypti from breeding. The government needs

to forge an alliance with the community and, in doing so,

provide the leadership and coordination for an integrated

effort. Such leadership, however, does not usually exist in

most affected communities, and a lack of trust in public

authorities rapidly undermines the feasibility of a govern-

ment–community alliance. To overcome this, local gov-

ernment must be a full partner and provide competent

leadership in initiating control activities, and encouraging

and facilitating community participation (and not solely

for dengue control).

Equally important is that governments forge an alli-

ance at the regional level, sharing surveillance information

and pooling resources in order to better cope with DF/

DHF outbreaks. Dengue transmits easily through travelers

moving from country to country. Therefore, no matter

how well equipped a country may be, it will not be able to

prevent epidemic transmission unless all other countries

in the region participate in serious DF/DHF control

efforts.

Ultimately, the greatest political barrier to DF/DHF

prevention and control in most endemic countries is lack of

political skill and the will to develop and maintain effective

programs.

CROSS-COUNTRY COMMUNITY CASES

In the context of the preceding assessment of barriers to

dengue control and elements critical to its success, the

experiences of a range of affected countries have been

examined. Table 1 provides a summary of these cases for

comparative purposes, however a brief description of each

setting is also provided in the text below.

Cuba

A strong vertically structured control program was rein-

forced in Cuba in 1981 following the first and largest DHF

epidemic in the Americas (Kouri et al., 1986), notably

including regular home visits by environmental inspectors.

Amid the outbreak itself, there was heavy reliance on pesti-

cide use. Despite the program’s recognized efficacy (Gubler

and Clark, 1994), and after more than 15 years without re-

ported dengue activity, serious outbreaks reoccurred in 1997

(Guzman et al., 1999) and 2001–2002 (Spiegel et al., 2002).

This prompted a strong interest and commitment to alter-

native strategies that placed greater emphasis on intersectoral

coordination beyond just the health sector, as well as com-

munity participation in vector control (Sanchez et al., 2005).

Cuba’s strong health care infrastructure plays a key role

in dengue control in this country. At the local level, family

medicine centers provide free and accessible health care for

120 families each, enabling effective clinical-epidemiologi-

cal surveillance through rapid detection and isolation of

cases. These centers reinforce the efforts of Health Area

Teams, which serve between 10,000 and 30,000 inhabitants,

and provide a platform for working on health promotion

matters with each district’s Popular Council of elected

officials and community organizations. They further com-

plement national strengths in laboratory analysis and vector

control capacity. Another element critical to the 2001–2002

dengue campaign was a great mobilization of people to

identify and eliminate breeding sites, clean up high-risk

areas, and conduct comprehensive adulticide spraying.

Although this enabled effective containment of what be-

came an uncontrolled epidemic in other countries in the

region, authorities deemed it too costly to be sustainable.

In 2003, pilot projects were initiated in two commu-

nities in the City of Havana to explore how integrated


Tab

le1.

Co

mp

arat

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Sum

mar

yo

fSi

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ross

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Co

mm

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01

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top

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bil

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situ

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d

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surveillance and community participation can form the

basis for sustainable control and prevention of dengue

(Spiegel et al., 2004). This study includes a case-control

examination of factors associated with the presence of

breeding sites in homes in a nonoutbreak period.

Guatemala

In 1997, a dengue prevention project based on community

mobilization was carried out on the Pacific coast of Gua-

temala by the Ministry of Public Health and Social Assis-

tance, the Guatemalan Institute of Social Security, and the

Institute for Nutrition of Central America and Panama

(part of the Pan-American Health Organization), with

funding from the US Agency for International Development

(USAID). The project was in response to DHF cases iden-

tified in 1996, and in recognition of the potential for further

DHF cases. A variety of ‘‘best practices’’ were employed,

such as involving the community through children’s events,

talks given by Public Health employees, collaboration with

local officials, outreach to physicians, mass media and, in

some sectors, the training to conduct neighboring house-

hold visits to look for mosquito breeding sites.

There was no outbreak during the project and many

household prevention practices increased from the baseline

assessment. Local officials and health workers were exten-

sively involved in the implementation of the program, al-

though funding primarily came from outside the national

government, and when funds were no longer available

many staff were reassigned to other activities.

A 3-year post-evaluation was conducted to examine

lasting effects of the project in 2000 (Zielinski-Gutierrez,

2002). Cross-sectional surveys were undertaken with resi-

dents who had lived in the intervention communities since

before the project period. While some knowledge indicators

declined in the intervening 3 years, many household pre-

vention practices for control of breeding sites had, in fact,

continued or even increased. Entomological indices of

larval infestation had, however, increased in almost every

category of container. In this instance, the remaining pre-

vention practices were not sufficient to hold down vector

populations.

Factors such as recent interactions with health or

vector control workers were not significant in their asso-

ciation with positive prevention practices or the presence of

mosquito larvae. Interestingly, however, multivariate anal-

ysis suggested that households in areas that received visits

from neighbors during the 1997 intervention (vs. areas

where only mass media and community-wide events were

carried out) were significantly less likely to become Aedes

larvae-infested over time. While a whole range of caveats

could explain this association, it may suggest that further

evaluation of the effects of direct neighbor-to-neighbor

interaction is warranted, and bolster other case studies

discussed in this article.

Singapore

For many years, Singapore’s strategy for the prevention and

control of DF was based on a strong surveillance capability,

an extensive public education program, and a strict

enforcement regime.

The Aedes House Index (AHI) was reduced to

approximately 2%, which was considered below the

threshold level of epidemic transmission, but there were

many occasions when some neighborhoods registered an

AHI of more than 5, which increased the risk of a localized

outbreak. Evidence from surveillance indicated that female

mosquitoes quickly adapted to control measures by

switching breeding sites, even to such unlikely places as

manhole covers, requiring the need for constant vigilance

and adaptive responses at all levels.

It became clear that while public education served to

raise awareness, it did not spur action. Surveys have shown

that while the knowledge content was extremely high,

attitudes were very poor. Enforcement did not change

people’s attitude. Four years ago, Singapore revised its

strategy, with emphases given to winning the community

over and getting them to take responsibility for the dengue

problem. Working very closely with the private, public, and

people (3-P) sectors, the government was able to raise the

level of ownership of the dengue control program among

residents, who volunteered their time to help carry out

surveillance and conduct public education programs.

The government, on the other hand, openly displayed

full commitment to join in the battle with the community.

It strengthened its surveillance system and started a re-

search facility to study dengue. Internally, the government

also initiated a program to change the mindset of its field

staff and provided training to employees in facilitation

rather than regulation.

In 2005, the Singapore government had succeeded in

establishing a closer rapport with the community and, in

many of the campaigns organized with grassroots support,

the number of breeding sites has declined significantly (Ooi

et al., 2005). The major challenge now is sustainability.


Thailand

Dengue vector control in Thailand has not had much

impact in reducing dengue transmission at the national

level. To find an effective strategy to control this disease, a

pilot intervention project, funded by the WHO, was re-

cently conducted in eastern Thailand using a combination

of top-down and bottom-up approaches [Kittayapong et

al., unpublished data]. Implementation was initiated by

local administrative authorities, including public health

and school officials in collaboration with householders,

public health volunteers, and school children. The local

public health volunteers are mostly women who do not

work outdoors and have more free time at home. As

volunteers for public health activities, they usually bene-

fited from their public health service. Local public health

volunteers and students were the key persons for con-

ducting control activities at homes and schools, respec-

tively. An educational series for students and public health

volunteers was organized in both schools and communi-

ties. General education in dengue, vector biology, and

vector control was followed by specific training in vector

control methodologies and production of local vector

control materials, which were then distributed following a

clean-up campaign prior to the rainy season.

The strategy combined source-reduction campaigns

with appropriate vector-control technologies applied only

in the foci where dengue cases were clustered, within 100

meters around those foci, and within schools attended by

children from the control areas. Vector control measures by

local government authorities included the source-reduction

campaign noted above, followed by a routine weekly gar-

bage pickup during the rainy season. Integrated vector-

control methodologies used in this campaign included lo-

cally made screen covers designed to fit tightly over the

opening of clay water-storage jars, a combination of locally

produced Bti, local predaceous copepods, and locally

constructed lethal ovitraps. The success of this intervention

was evidenced by a significant reduction in both dengue

mosquito vector populations and serologically confirmed

dengue cases in control areas compared to noncontrol areas

(pre-intervention: 265.25 vs. 217.86 per 100,000 popula-

tion; post-intervention: 0 vs. 332.23 per 100,000 popula-

tion).

Even though cost-effective suppression of dengue

transmission was clearly demonstrated, it was a challenge

for this pilot program to be maintained and scaled-up. The

main reason for the reluctance to accept this environ-

mentally friendly approach was related to the psychological

satisfaction of insecticide spraying. It was concluded that

the key factors for program sustainability are the change in

attitude and behaviors of both communities and public

health authorities; they must accept and promote the

community-based approach with minimal use of insecti-

cides and integrate locally appropriate control methodol-

ogies. The Knowledge, Attitude and Practice (KAP) survey

showed that background knowledge on dengue and its

mosquito vectors among householders was moderately

high, but knowledge alone did not translate to control

action; dengue did not rank as a high priority disease to

Thai’s in most communities (Fig. 5).

The key person with leadership standing in each

community is also an important driving force for the

development and maintenance of an effective and sus-

tainable community dengue control program. A remaining

challenge is the adoption of a national policy for dengue

control to include an integrated community-based ap-

proach aimed at controlling larval mosquito vectors, as well

as to promote environmental management and source

reduction.

Indonesia

A dengue control project was initiated in Indonesia in 1997,

with support from the Rotary Foundation of Rotary

International. Rotary Indonesia, ‘‘PKK’’ (Family Welfare

Movement) at the national level and the Department of

Health at the national and local levels, collaborated to de-

sign a community education program on topics such as the

mosquito life cycle, mode of DF/DHF transmission, and

ways in which the community can protect itself. Weekly

household inspections, both indoors and outdoors, were

conducted in every village (kelurahan) as a means of edu-

cating and motivating communities. Many community

organizations have since evolved, including farmers’

groups, neighborhood groups, and women’s groups. One

of these is the ‘‘Dasawisma’’ (ten-house) groups, the

smallest unit of the national ‘‘PKK,’’ initiated through the

Interior Department.

The Department of Health and local government

officials were requested to continue motivating the com-

munity through repeated visits. Rotary has initiated the

‘‘Jumantik’’ (surveyor of mosquito larvae) in the 13 cities

where the weekly inspection program was first initiated.

Continuous supervision by local PKK members (including

the Mayor’s wife in one city) and local health officials


promote the weekly inspection by the villagers. It is

emphasized that households are expected to inspect their

wider Dasawisma neighborhood.

In the city of Purwokerto, where the initial phase of the

project was conducted, reported cases of DF fell from 103

in the 1997 to 8 cases in 2000 (Nalim and Hartono, 2002).

A significant decrease in DHF cases has been noted since

1999, however DF incidence rose steadily following project

termination (14 DF cases reported in 2001, 22 in 2002, and

30 in 2003) (Nalim and Hartono, 2002).

Upon termination of Rotary support, WHO Fort

Collins, through the World Health Organization continued

to support this project. Rotary is still trying to obtain more

funds for highly endemic DHF cities.

Vietnam

A collaborative, community-based A. aegypti control pro-

gram has been active in Vietnam since 1995 (Nam et al.,

2004). Prior to this, DF control in Vietnam had been based

primarily around adulticide spraying as a responsive mea-

sure during epidemic periods, an expensive and quickly

reversible method. Key activities of the continuing pro-

gram, initially developed by a transdisciplinary, multi-

national team of entomologists, health workers, and

nongovernmental organization staff, include community

mobilization and education campaigns, the breeding and

use of local copepod predators against A. aegypti, and the

ongoing surveillance of both vector populations and

household behaviors. Individual projects are tailored to suit

local conditions through a combination of KAP and vector

surveys, and evaluations are conducted annually to ensure

program activities adapt to changing conditions, and thus

ultimately remain effective.

By the year 2000, full A. aegypti control had been

achieved in 5 out of the 6 communes initially involved in

the first project, and subsequent program expansion

achieved control in 32 out of 37 new communes by 2003

(Nam et al., 2004). In light of its broad community

acceptability and cost-effectiveness, the program’s focus

was rapidly extended from the northern provinces of the

country to become a national strategy (Nam et al., 2000,

2005).

Through utilizing a combination of bottom-up com-

munity mobilization, and top-down expertise, monetary

support, and leadership, the Vietnamese experience has

thus far demonstrated a cost-effective and sustainable SES-

compatible approach to dengue control since it was

adopted in 1995.

RESPONDING TO THE CHALLENGE: BRIDGES TO

SUSTAINABLE CONTROL

While some short-term successes in dengue control have

been achieved, such as the apparent elimination of the

disease in the Americas in the post-World War II period,

over time, nature, in this case a highly resilient vector, has

found ways to adapt. The result has been the 20th Century

resurgence of DF/DHF.

Figure 5. KAP household survey results

for indirect dengue control in Thailand.


Past experience has vividly demonstrated the ineffec-

tiveness of approaches to dengue control that have failed to

take into account the complex behaviors of ecological and

social systems, and, in this sense, have failed to build

adequate ‘‘bridges,’’ the term employed by Gunderson

et al.(1995) to refer to the potential linkages between social

actors dispersed across various disciplines and institutions,

who are all called upon to contribute to both an under-

standing of complexity and a construction of effective

interventions capable of achieving impact.

Insights gained have also underscored the importance

of developing and reinforcing community capacity to play a

pivotal role in control efforts. This capacity encompasses

the ability of communities to identify risks and undertake

interventions, as well as their agility to recognize and adapt

to changes in the social–ecological systems. Thus, the above

failure analysis provided using this coupled human–natural

systems perspective provides insight into the key elements

of a sustainable dengue control program. Bridges built by

the social actors in the relevant arenas are thus necessary to

enable the development of each of these elements.

Adapt Control Programs to the Mosquito’s

Changing Behavior

In pursuing vector control in the absence of a vaccine, a

strategy must be developed that is fully cognizant of how

A. aegypti adapts to interventions, including pesticide

resistance and breeding-site selection. An understanding of

this adaptative response to habitat change or other control

measures is necessary to target and modify control strate-

gies accordingly. In this sense, campaigns focusing on the

same breeding sites year-after-year may not be effective.

Adapt Education Programs to the Public

In DF/DHF affected areas, wide-ranging needs must be

balanced among scarce resources. In this sense, knowledge

must be regarded as a two-way street, where ‘‘experts’’

must develop technical approaches and solutions that

correspond to social realities. Social realities themselves

must be acknowledged as dynamic and constantly in flux,

and other stakeholders, from policy-makers to community

representatives, must be engaged to support sustainable

and effective dengue control practices.

Regional and Local Focus

Local social realities vary regionally. Recognizing that the

control of dengue cannot be geographically isolated, and

that there is much interaction of both vectors and infected

humans among countries and regions, strategies must ac-

count for both regional and local factors. This calls for a

more profound understanding of political, economic, so-

cial, and ecological similarities and differences among

countries in a region, and for continued efforts at regional

and international communication of epidemiological,

entomological, and laboratory information.

Transdisciplinarity

The challenge of understanding complex social and eco-

logical systems calls for building transdisciplinary capacity

that recognizes the interplay between social and ecological

systems. The entomologist must collaborate with the epi-

demiologist and the anthropologist. And all must work in

close collaboration with communities, policy-makers, and

other stakeholders who are intimately involved in the

success of control efforts.

Empowerment

Failures of previous top-down efforts have demonstrated

that all segments of the community must play an active

and conscious role. To carry out this role, however,

communities must have access to the information and

resources they need, reinforced by governments who are

better placed to consolidate and disseminate information,

and facilitate this support. Note that empowering com-

munities may mean that dengue control will become one

among many environmental health goals pursued by

communities which choose to focus on wider sanitary

and/or water access issues. Programmatic goals and

mechanisms may need to be adjusted to reflect these less

direct projects.

Scalability

While pilot projects play an essential role in developing

effective methods, progress cannot be made unless the

approaches can be scaled up to the national and regional

level. This calls for a commitment to go beyond the

‘‘learning’’ phase at the local level and engage in a new level

of learning at the macro, indeed the global, level.

Adaptability

Sustainable dengue control, above all, calls for the will-

ingness to adapt to new information and create ‘‘learning


systems.’’ In this sense, surveillance capacities play an

important role in real-time management of evolving situ-

ations, but they must also constantly reevaluate their

effectiveness. The overall success of global DF/DHF control

calls for forging transdisciplinary capacities to share lessons

and adapt to inevitable changes.

Sustainability

Sustainability of dengue control remains a continued

challenge, and realistic expectations for, and indicators of,

sustainability must be defined according the characteristics

of each specific setting. Community participation ap-

proaches have often been seen by governments as

‘‘inexpensive alternatives’’ to vector control. This is unre-

alistic in the short-term, but may succeed in the long-term.

Short-term, project-focused funding from bilateral aid

agencies is unsustainable due to its lack of ongoing support.

Sustainable, effective long-term DF/DHF control must

begin with a combination top-down/bottom-up program

that provides initial success, followed by a gradual transi-

tion to integrated, community-owned programs.

The level of control that can be locally sustained at any

given time may need to be adjusted to reflect local capac-

ities and resources. For example, reduction of A. aegypti

populations below transmission levels may be achievable in

some settings, whereas readiness to detect and respond to a

pending outbreak may be an achievable goal elsewhere.

CONCLUSIONS

To effectively and sustainably protect human populations

from dengue fever, we must be prepared to dynamically

translate our understanding of social-ecological systems

into effective actions. The failure to appreciate how

complex systems interact has ultimately prevented sus-

tainable solutions from being adopted. Dengue provides

an ideal terrain for evaluating how successfully we are

able to take on this challenge, as despite our growing

understanding of the problem, we have witnessed a

pandemic increase of this disease. Here we have consid-

ered dengue transmission in an SES framework, as a

coupled human–natural system of elements separated by

value-based barriers demanding transdisciplinary solu-

tions. Ultimately, what is required is a transformation of

the control effort itself, to extend beyond the barriers that

reinforce compartmentalized visions and, through the

catalyst of implementation for the benefit of vulnerable

communities and the application of an integrated SES

approach, to forge bridges among the myriad of social

actors who heretofore have followed separate agendas.

ACKNOWLEDGMENTS

Ideas for this article were developed during a working

meeting on social–ecological systems and emerging infec-

tious diseases, hosted by the Asia-Pacific Institute of

Tropical Medicine & Infectious Diseases and the East-West

Center in Honolulu, Hawaii (March 9–11, 2005). This

meeting was supported by a grant to promote methodo-

logical innovation in interdisciplinary health research from

the National Institutes of Health (R13 TW007300) and

funded by the Fogarty International Center and Office of

Behavioral and Social Sciences under the NIH Roadmap

initiative ‘‘Research Teams of the Future.’’ We acknowledge

the efforts of the meeting organizers, and especially other

colleagues who played a full role in these discussions that

produced the core ideas for the article, including Martin

Meltzer, Eileen Shea, and Rainer Sauerborn. Special thanks

to Mayee Wong for her valuable contributions to the

working group discussions.

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