Acta Tropica, 61 (1996) 169-179 169 Elsevier Science B.V.

ACTROP 00486

Community involvement in the control of Aedes aegypti

Duane J. Gubler* , Gary G. Clark Division of Vector-Borne Infectious Diseases, National Center for Infectious Diseases, Centers for Disease

Control and Prevention, PO Box 2087, Fort Collins, CO 80522, USA

(Accepted 25 April 1995)

In the past 15 years, there has been a dramatic resurgence of dengue and dengue hemorrhagic fever worldwide, with increased frequency of epidemics and geographic expansion of both the mosquito vectors and the viruses. The reasons for this resurgence are not well understood, but include uncontrolled and unplanned urbanization, increased movement of people and viruses by airplane and lack of effective control of Aedes aegypti, the principal mosquito vector of dengue viruses. The recommended method for Ae. aegypti control during the past 20 years has been ultra-low volume (ULV) application of insecticides, a method which targets the adult mosquito. Lack of efficacy of the ULV approach led to a reevaluation of recommended strategies for prevention and control of epidemic dengue and ultimately, resulted in develop- ment and widespread use of community-based, integrated approaches to Ae. aegypti control. This chapter reviews the use of community participation for controlling Ae. aegypti via larval source reduction and critically discusses programs in four countries from the standpoint of effectiveness and sustainability. It is concluded that a combination of vertically structured centralized and community-based approaches should provide short-term success as well as long-term sustainability.

Key words: Dengue; Mosquito control; Community participation

1. Introduction and background

Dengue fever (DF) and dengue hemorrhagic fever (DHF) are caused by four antigenically related viruses (DEN-I, DEN-2, DEN-3 and DEN-4) that belong to the genus Flavivirus, family Flaviviridae (Gubler, 1988). Although remote forest cycles involving lower primates and canopy dwelling Aedes mosquitoes may occur in Asia and Africa, the most important maintenance cycle from a public health standpoint involves humans and mosquitoes in urban and suburban centers of the tropics. The principal mosquito vector is Aedes aegypti, a highly domesticated species that has adapted to the urban environment by using artificial containers that collect rainwater or those used for domestic water storage as a larval habitat. Other mosquito species such as Aedes albopictus, Aedes polynesiensis and Aedes mediovitta- tus may be involved in suburban or rural maintenance cycles, but are less frequently responsible for transmitting epidemics of DF and DHF (Gubler, 1988).

There has been a dramatic increase in incidence of DF and DHF worldwide in

*Corresponding author.

SSDI 0 0 0 1 - 7 0 6 X ( 9 5 ) 0 0 1 0 3 - 4

170

the past 25 years (Halstead, 1984, Gubler, 1991). This has been associated with increasing frequency of epidemic activity and expanding geographic distribution of both the mosquito vector (Ae. aegypti) and the dengue viruses. In 1995, DF/DHF is the most important arboviral disease of humans; more than 2.5 billion people are at risk of infection in urban centers of the tropics (Fig. 1). Each year an estimated 40-50 million cases of DF occur, and depending on the year, tens to hundreds of thousands of cases of DHF.

The reasons for this worldwide increase in dengue activity and the emergence of DHF outside of Asia are not fully understood, but several important factors have influenced the epidemiology of dengue during this period (Gubler and Trent, 1994). First, the world has experienced unprecedented population growth during the past 50 years, most of it in developing tropical countries. This has resulted in unplanned and uncontrolled urbanization in those same countries, which in turn has resulted in deteriorating housing and inadequate water, sewer and waste management sys- tems, and finally to increased populations of rodents, mosquitoes, and other animals living in intimate association with crowded human populations. Second, the dispersal and packaging of consumer goods in nonbiodegradable plastic have contributed to expanding geographic distribution and increased population densities of Ae. aegypti by providing man-made breeding sites for the mosquito. Third, increased commercial air travel has provided the ideal mechanism for the rapid movement of infected travelers, and therefore, dengue viruses between population centers of the tropics. Finally, mosquito control measures used since 1970 have been ineffective in reducing mosquito populations to levels that interrupt dengue transmission. The result has been repeated introductions and movement of new virus serotypes and strains into, and between, tropical urban centers that are highly permissive for dengue transmis- sion. Collectively, these factors have been responsible for the expanding distribution, increased frequency of epidemic activity, and the emergence of DHF in new geo- graphic areas.

W O R L D D I S T R I B U T I O N OF DENGUE - 1995

r • Areas at risk for epidemic dengue ~ 0)2 • Countries with recent dengue activity

Fig. 1.

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Prevention and control of DF and DHF have relied on the control of the urban mosquito vector, Ae. aegypti. While Ae. aegypti control in Asia has been ineffective, in the Americas, this species was eradicated from much of Central and South America in the 1950s and 1960s (Schliessman and Calheiros, 1974). Unfortunately, with the termination of the Ae. aegypti eradication programs in 1970, this species began to reinfest most of those countries, and in 1995, it has a distribution similar to that before eradication (Gubler and Trent, 1994).

Since the early 1970s, prevention and control of epidemic dengue have relied on insecticides used as space sprays to kill adult Ae. aegypti. The most popular and highly recommended method was ultralow volume (ULV) application of malathion (Lofgren, 1970). Recent, carefully controlled and evaluated field studies in Puerto Rico, Trinidad, Suriname, Jamaica, and Venezuela, however, have demonstrated that ULV application by ground or aerial equipment has little or no lasting impact on the female Ae. aegypti population (Chadee, 1985; Hudson, 1986; Gubler, 1989; P. Reiter, Centers for Disease Control and Prevention, unpublished data).

2. New strategies for dengue prevention and control

The dramatic geographic spread and emergence of DHF in the Americas in the 1980s, focused attention on new approaches to prevention and control of epidemic dengue. It became clear that effective and sustainable Ae. aegypti control could not be achieved by reliance on space spraying with insecticides targeted at the adult mosquito. The only effective approach for providing Ae. aegypti control has been the elimination of larval habitats from the domestic environment or source reduction (Soper, et al., 1943; Schliessman and Calheiros, 1974). Resources, however, were not available in the 1980s to develop the large, vertically structured government programs (top-down) that were so successful in eradicating Ae. aegypti from many countries in the Americas. It should be noted that even if resources were available, vertically structured programs were not sustainable when government funds were withdrawn because community members had no defined role or responsibility in program implementation and maintenance.

In an effort to achieve sustainable Ae. aegypti control, emphasis in the 1980s was shifted to community-based, integrated programs (bottom-up). The rationale was that cost-effective Ae. aegypti control could best be achieved by larval source reduc- tion conducted by the occupants of the communities where transmission occurred. The idea became very popular and with support from the World Health Organization (WHO), trials were conducted in Thailand (Phanthumachinda, et al., 1985). However, these programs did not involve true community participation in that members of the community were not involved in planning, implementation and direction of the activities. Instead, these were programs designed and directed by government officials; the citizens who participated simply did what they were told and when support was withdrawn, the programs were not maintained.

These early trials taught us important lessons; 1) that government-directed com- munity-based programs, like the earlier eradication programs in the Americas, did not have sustainability without continued economic and programmatic incentives from the government; and 2) that successful programs would not compete success- fully for limited government health dollars once they had eliminated or reduced

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disease incidence. Sustainability of disease control programs thus requires a sense of community ownership, including the use of community resources, ideas, and leadership in providing program design and direction. This approach was widely accepted in the mid-1980s and currently Ae. aegypti control programs based on active community participation have been, or are in the process of being developed in numerous countries worldwide. Gubler and Clark (1994) recently published a brief review of these programs, which will not be discussed here. Table 1 lists those countries with community-based programs and gives a brief comment on their status.

It will be noted that none of the community-based programs listed in Table 1, have been very effective in preventing epidemic dengue transmission. This underscores a major problem with relying solely on members of the community to assume responsibility for disease prevention and control (Gubler, 1989; Service, 1993). Before this approach can be effective, it must become unacceptable to allow mosquito larval habitats to exist in the community; homeowners must be convinced that it is in their best health interests to control Ae. aegypti on their premises and in their community. Only then will they, in partnership with government agencies, develop effective, sustainable Ae. aegypti control programs (Gubler, 1989). This requires education and continued reinforcement; it is by nature, a very slow process that will probably take many years before members of the community accept responsibility for a task they now perceive to belong to the government. The success of community-based health programs is dependent on redefining the unacceptable as has been done with smoking in the United States (Halstead, 1993). With the exceptions of Singapore, Malaysia, Cuba and Puerto Rico, none of the programs listed in Table 1 have been in operation long enough for that to happen.

3. Case studies

Rather than review all the programs listed in Table 1, four countries have been selected for further discussion. Two (Cuba and Taiwan) have been successful in preventing epidemic dengue transmission, while two other apparently successful programs (Singapore and Puerto Rico) have failed to prevent the occurrence of recent epidemics.

4. Cuba

The Cuban program has been hailed as one of the few success stories in Ae. aegypti control. It was initiated in 1981 during the first and largest DHF epidemic in the Americas. During the epidemic, the Cuban government trained and mobilized over 15 000 civil defense workers to go from house to house implementing mosquito control and educating the citizens about dengue and how to control Ae. aegypti (Armanda-Gessa and Figueredo-Gonzales, 1986). Massive amounts of insecticide were used for both larval and adult control. Water containers were treated with temphos (Abate R), houses were sprayed with residual insecticides, and weekly ULV spraying with malathion was conducted both indoors and from the street. The mosquito control efforts during the epidemic cost an estimated $43 million U.S.

TA

BL

E 1

Cou

ntri

es w

ith

Com

mun

ity-

Bas

ed A

edes

aeg

ypti

Con

trol

Pro

gram

s

Cou

ntry

Y

ear

Scop

e E

valu

ated

C

omm

ents

In

itia

ted

Sing

apor

e*

19

68

C

ount

ryw

ide

Yes

Mal

aysi

a*

19

72

C

ount

ryw

ide

No

Cub

a 19

81

Isla

ndw

ide

Yes

Pu

erto

Ric

o 19

84

Isla

ndw

ide

In P

rogr

ess

Col

ombi

a 19

85

Foca

l, B

ucar

aman

ga

No

Indo

nesi

a*

19

85

C

ount

ryw

ide

No

St.

Luc

ia

1985

Is

land

wid

e N

o T

aiw

an*

1988

So

uth

No

Hon

dura

s 19

90

Foca

l, Y

oro

No

Mex

ico

1990

Fo

cal,

Yuc

atan

sta

te

No

Pan

ama

19

90

C

ount

ryw

ide

No

Sout

h Pa

cifi

c 19

90

Sele

cted

isla

nds

No

Dom

inic

an R

epub

lic

1991

Fo

cal

No

Peop

le's

Rep

. of

Chi

na

1991

H

aina

n Is

land

N

o T

hail

and

1991

Fo

cal

No

Bra

zil

1992

Fo

cal

No

Sri

Lan

ka

1992

Fo

cal

No

Car

ibbe

an S

ubre

gion

19

93

Foca

l N

o A

ustr

alia

19

94

Nor

th Q

ueen

slan

d N

o

Ver

y ef

fect

ive

for

20 y

ears

; re

cent

ly m

ajor

epi

dem

ics

of D

F/D

HF

in

dica

te p

robl

ems

Epi

dem

ic d

engu

e in

dica

tes

prob

lem

s V

ery

effe

ctiv

e fo

r 14

yea

rs;

no r

epor

ted

tran

smis

sion

C

urre

nt d

engu

e ep

idem

ic in

dica

tes

prob

lem

s R

ecen

t de

ngue

out

brea

k in

dica

tes

prob

lem

s E

pide

mic

den

gue

indi

cate

s pr

oble

ms

Ver

y ef

fect

ive

init

iall

y, b

ut s

urve

illa

nce

is p

oor

Ver

y ef

feci

tve,

sm

all

outb

reak

in

1994

D

engu

e tr

ansm

issi

on,

but

surv

eill

ance

is p

oor

Cur

rent

epi

dem

ic,

indi

cate

s pr

oble

ms

Rec

ent

deng

ue o

utbr

eak

indi

cate

s pr

oble

ms

Cur

rent

tra

nsm

issi

on,

but

surv

eill

ance

is p

oor

Den

gue

tran

smis

sion

, bu

t su

rvei

llan

ce is

poo

r C

urre

nt t

rans

mis

sion

, bu

t su

rvei

llan

ce is

poo

r C

urre

nt t

rans

mis

sion

, bu

t su

rvei

llan

ce is

poo

r E

pide

mic

den

gue

indi

cate

s pr

oble

ms

Den

gue

tran

smis

sion

, bu

t su

rvei

llan

ce is

poo

r C

urre

nt t

rans

mis

sion

, bu

t su

rvei

llan

ce is

poo

r T

oo e

arly

to

dete

rmin

e ef

fica

cy

* W

hile

mem

bers

of

com

mun

ity

wer

e us

ed,

thes

e pr

ogra

ms

are

dire

cted

by

the

gove

rnm

ent.

174

dollars, mostly for the purchase of insecticides and spray equipment (Guzman et al., 1992).

With the Ae. aegypti population reduced to an unprecedented low level after the initial control efforts, the Cuban government then set a goal of eradication. Although this has not been achieved, the program was successful in reducing and maintaining the Ae. aegypti house index to less than 0.1%, and in preventing any further dengue transmission. The mechanism for achieving such success was a top-down approach; people were instructed on how to prevent mosquitoes from breeding in and around their home and thousands of inspectors were sent to check individual households, and enforce the anti-mosquito breeding laws. People were fined if Ae. aegypti larval habitats were found on the premises. The motivation to participate was, therefore, the threat of punishment. The program also encouraged the use of artificial flowers in cemeteries, use of mosquito-proof containers for water storage, and controlling unused containers that retain water and provide larval habitat for Ae. aegypti.

Although current data are not available, it is assumed that the control program is still effectively maintaining low Ae. aegypti population densities. It should be noted, however, that recent political and economic events in Cuba may be detrimental to the maintenance phase of this vertically-structured program. As economic condi- tions continue to deteriorate, the laws may not be effectively enforced, thus testing the efficacy of community involvement and the sustainability of a legislative type of control that has been imposed on the population. If there was no real community ownership of the program, Ae. aegypti will likely make a comeback and reinfest many areas.

5. Taiwan

In 1981, after an absence of more than 35 years, epidemic dengue reappeared in Taiwan (Hwang et al., 1992). Over several years, all four dengue virus serotypes were introduced to the island and another major epidemic occurred in 1987-88. In all instances, transmission was limited to the southern part of the island where Ae. aegypti occurs.

In the wake of the resurgence of epidemic dengue in Taiwan, the government initiated a dengue control program in 1988 with active disease surveillance and community-based Ae. aegypti control (Hwang et al., 1992). The program in Taiwan, however, is more top-down than bottom-up in that both national and local govern- ment agencies are involved, but there is very little community ownership. Educational materials are designed, produced and distributed by the government. Moreover, source reduction campaigns and insecticide spraying are also conducted by govern- ment agencies. The insecticide space sprays are applied inside the houses rather than from the street as is the procedure in most countries. In Taiwan, members of the community had very little involvement in planning or implementing the program.

The Taiwan program has been successful in preventing epidemic dengue to date. Ae. aegypti house indices were reduced from approximately 44% in Kaohsiung City in 1988 to 9% in 1991 (Hwang et al., 1992). Since then, Ae. aegypti populations have fluctuated, but despite repeated introductions of dengue viruses from other Asian countries, epidemic activity has not recurred. As soon as dengue cases are detected by the surveillance system, government teams are dispatched to the area to

175

conduct intensified surveillance, indoor space spraying, initiate larval source reduc- tion and to intensify community education efforts. Although dengue activity occurred in 1994, transmission was limited and only 216 cases were reported through November 27 (Anonymous, 1994). It remains to be seen whether the success of this relatively new program will be sustainable.

6. Singapore

The program in Singapore has been the most successful and sustainable Ae. aegypti control program on record. Developed in the late 1960s in the wake of emergent epidemic DHF, it was implemented in 1968 as the Destruction of Disease-Bearing Insects Act (Chan et al., 1990). The program placed emphasis on source reduction and community education, with strictly enforced legislation that made it unlawful for citizens to allow larval habitats for Ae. aegypti mosquitoes on private property. Like Taiwan, the program was more of a top-down structure with over 1500 government inspectors who acted as health educators and law enforcement officers. Between 1973 and 1981, 54 297 orders and 7,047 summonses were served resulting in fines totaling approximately $800000 U.S. dollars (Chan et al., 1990). Receipts from these fines were used for health education and source reduction operations. While the majority of the people participated in this program, the motivation for participation was most likely the threat of punishment for breaking the law.

The program was highly successful. By 1972, the Ae. aegypti house index was below 5% in most of Singapore (Chan et al., 1990). In 1973, however, Singapore experienced its largest dengue epidemic in history, stimulating intensified mosquito control; Ae. aegypti house indices were reduced to about 2% where they have remained until the present. While other countries in the area experienced repeated major epidemics of DHF, Singapore was free of epidemic DF/DHF from 1973 to 1990. Recently, however, Singapore has experienced a resurgence of epidemic DF/DHF with large epidemics, even though the mosquito densities have apparently remained low. Government officials attribute the increased transmission to several factors, including focal increases in the Ae. aegypti population and a waning of herd immunity in the human population. Both of these factors are probably important, but another, unmentioned factor is also a likely contributor. The Singapore program was built on strong, effective leadership and on good management. In 1986, that leadership changed and since then the dengue control program has had several directors that may not have been as effective.

7. Puerto Rico

The emergence of epidemic DF and DHF in the Americas resulted in the develop- ment of new control strategies for this disease by the Centers for Disease Control and Prevention (CDC), and a plan of action was drafted in 1983-84 as part of the U.S. Public Health Service 1990 program objectives (Gubler, 1989). A program that emphasized disease prevention rather than emergency response to epidemic transmis- sion, was initiated in 1985 (Gubler, 1989; Gubler and Casta-Velez, 1991), and had five basic components: 1) proactive, laboratory-based disease surveillance, 2)

176

education of the medical community, 3) emergency hospital contingency plans, 4) emergency vector control, and 5) community-based, integrated Ae. aegypti control.

Implementation of the first and second components has been highly successful; the surveillance system has predicted the last two major epidemics and the level of knowledge among medical personnel about diagnosis and treatment of DF and DHF is considered to be high. An emergency hospitalization plan was developed and partially implemented in 1987, but has not been completed or maintained. The fourth component was never implemented because available emergency mosquito control measures were not effective in reducing adult female Ae. aegypti densities. The last component, perhaps the most difficult to develop and implement, was initiated in 1985 with the establishment of a series of individual programs and is currently being formally evaluated by the Johns Hopkins University.

The community-based Ae. Aegypti control component of the Puerto Rico program has been described and reviewed in some detail (Gubler, 1989; Clark, 1992, Gubler and Clark, 1994). Briefly, the initial objectives were to educate the residents of Puerto Rico about DF/DHF, the impact of the disease on their community and family, and about how to prevent the disease from occurring in their community. The goal was to motivate and encourage them to assume responsibility for controlling mosquitoes in the immediate area around their homes. A major effort was made to create community ownership of the program and transfer principal responsibility for controlling domestic mosquitoes from government agencies to members of the community. Non-government resources, mainly local businesses organized through the Rotary Club of San Juan provided financial support for the program. Medical anthropologists and social scientists were recruited to study ethnocultural differences in the diverse Puerto Rico community and to use this knowledge to develop new educational materials and programs on dengue for specific target audiences. Through Rotary International, public relations and marketing expertise were used to design, produce and distribute professional quality educational materials and programs, which were well-received. The Puerto Rico community-based control program is a model partnership between the private sector represented by The San Juan Rotary Club (Rotary International), the Commonwealth of Puerto Rico Health Department, and the federal government represented by CDC, working together on disease prevention.

Utilization of mass media in this program has been very successful in producing a high level of community awareness about DF/DHF in Puerto Rico and in convinc- ing the public that dengue is a controllable disease. Several of the program compo- nents focused on youth education and participation (e.g., activity booklets for preschool [Head Start] and elementary school children and teachers, a children's museum exhibit, and Boy Scouts) have become institutionalized and should contrib- ute to a future generation of adults who will take responsibility for dengue prevention and control. Educational programs directed at the medical community have been successful in increasing the physician's knowledge about diagnosis and treatment of DHF and has lead to improved management of severe hemorrhagic disease, thus decreasing the case fatality rate. The successful implementation of these programs is being followed by a careful evaluation of the impact they have had on specific target audiences. Once, this evaluation has been completed, adjustments will be made in materials and presentation of the program to improve their effectiveness, and to integrate their activities at the local level.

177

The occurrence in 1994 of the worst epidemic of dengue in Puerto Rico in 25 years provided an opportunity to review the results of these efforts. Initial indications are that despite an early warning of epidemic activity by the surveillance system, and major efforts by the CDC, there was a failure to convince government officials of the importance of taking measures to prevent epidemic transmission rather than waiting to implement an emergency response after the epidemic has been ordered, and that such prevention programs must be carefully developed, implemented, and evaluated prior to epidemic transmission. This has occurred in an environment where DHF has been endemic for 10 years. The response, or lack of response in 1994, suggests that the level of acceptability for significant dengue transmission in Puerto Rico is high. The lack of success is exemplified by the absence of an organized prevention program with specific objectives and priorities for which adequate human resources have been assigned.

The response to increased dengue transmission in 1994 was one of political expediency rather than one based on scientific recommendations. For example, vector control personnel received instructions to use ultralow volume (ULV) insecti- cide applications for mosquito control, a method that has been demonstrated in Puerto Rico and elsewhere in the Americas, to be ineffective in adequately reducing vector mosquito densities. This pressure originated from within the health agency or externally from elected officials. In some cases, it came from the public at large, even though there is an increasing concern about the safety aspects of insecticide usage and environmental concerns. While some residents recognize its ineffectiveness, others close their windows when the insecticides are applied. Often, after health officials have stated that the ULV sprays are ineffective, they are used anyway, thus sending a "mixed message" to the public; this also creates a false sense of security that the government is taking care of the situation and thus reduces the impact of prevention messages (Gubler, 1989).

It is clear that the program in Puerto Rico is not working as well as expected. Why and how the 1994 dengue epidemic in Puerto Rico happened, and whether the epidemic could have been prevented if an emergency, community-based, source reduction approach had been used in the early stages of the outbreak is unknown. However, it is clear that the use of ULV application of insecticides again failed to interrupt transmission. Despite early detection and prompt notification of increasing dengue incidence in 1994, the documented high level of awareness and understanding about dengue prevention by the public, were not used as the basis from which to mobilize the public to action.

8. Summary and conclusions

Community-based, integrated Ae. aegypti control is currently viewed by many public health officials as the only approach that is cost-effective and that will provide sustainable and effective disease control over the long term. The rationale used for this conclusion is that only by involving the persons who are responsible for creating or tolerating Ae. aegypti larval habitats in the domestic environment in control or elimination of those habitats, will they learn that it is in their best interest to participate with other members of their community and create community ownership of the program. To be effective and sustainable, community organizations at the

178

local level must provide the guidance, leadership, and enforcement of the community standards that govern what is acceptable and what is not acceptable in small geo- political areas. As indicated above, modification of attitude and behavior may take many years to accomplish, much as the changes in acceptability (or nonacceptability) of cigarette smoking has taken 30 years to achieve in the U.S. Therefore, we should not be too discouraged by the apparent lack of effective control demonstrated by those community-based programs outlined in Table 1.

Recognizing that in the short term, community participation will not provide effective prevention and control of epidemic DF/DHF, but that it is essential for developing effective programs that are sustainable, we must develop interim approaches that will achieve immediate results while preparing the community to assume more responsibility in the long term. Clearly, what is needed are integrated control strategies that utilize the best of both the vertically structured (top-down) and the community-based (bottom-up) approaches in initial phases of the program, with progressively more emphasis on community participation as the program evolves and matures (Gubler, 1989).

Initial success will require considerable guidance and direction by the government, but care should be taken to prevent establishing another government-funded and directed program that will fail as soon as financial and administrative support wavers. Efforts must be made in the initial phases of the project to develop strong, effective leadership for vector control programs. Staff must include social scientists who can conduct the proper ethno-geographic studies needed to better understand the values and diversity of the community, use this information to develop and target education messages, and to design intervention strategies. Marketing experts should be involved as community members to help develop educational materials/ programs and to help market the program to the community. Entomologists and physicians are needed to direct the control efforts and to evaluate intervention strategies to determine program efficacy.

The ultimate goal should be to create an effective government-community partner- ship, with the transfer of program ownership from the government to the community as early as possible. The timing for this transfer of "power" and responsibility will vary considerably from program to program, depending on the culture, economics, and type of government. It must be emphasized, however, that community ownership and sustainability can only be achieved if government officials are committed to this type of partnership and implement policies to facilitate community involvement in Ae. aegypti control.

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