Tropical Medicine and International Health

doi:10.1111/j.1365-3156.2009.02396.x

volume 14 no 12 pp 15421551 december 2009

Systematic Review

Multi-modal Aedes aegypti mosquito reduction interventions

and dengue fever prevention
Kara K. Ballenger-Browning and John P. Elder
Graduate School of Public Health, San Diego State University, San Diego, CA, USA

Summary

objective To systematically review the effectiveness of biological, chemical and educational dengue
fever prevention programs on the reduction of entomologic indicators.
methods Searches of PubMed, GoogleScholar, CabDirect databases and reference lists yielded over
1000 articles containing mosquito abatement interventions. Inclusion criteria were: Vector control
programs targeting Aedes aegypti and Aedes albopictus mosquitoes; Studies providing pre- and post-test
data. Intervention effectiveness was assessed using Mullas formula to determine percent reductions for
all studies with control groups. Twenty-one studies were reviewed.
results Twelve dependent variables were presented, however, the Breteau, House and Container
indices were the primary measurement tools for monitoring larval populations. Behavioural methods
consisting of educational campaigns and maintaining water containers to reduce the mosquito population were applied in eight studies. Eight studies involved the use of biological methods such as
predatory organisms or bacteria. Finally, eight studies used chemical control techniques including
insecticide sprays, larvicides, insecticide-treated materials, and cleaning water of containers with
household chemicals with three studies using a combination of intervention techniques. Post-intervention reduction in entomologic indices ranged from 100% to an increase of 13.9% from baseline.
conclsuion Little evidence exists to support the efficacy of mosquito abatement programs owing to
poor study designs and lack of congruent entomologic indices. Creation of a standard entomological
index, use of clustered and randomized-controlled trials, and testing the generalizability of proven
methods are recommended for future research.
keywords dengue, Aedes aegypti, vector control, review

Introduction
Dengue fever is the most rapidly advancing vector-borne
disease in the world (WHO 2004; Kroeger et al. 2006;
Farrar et al. 2007). In 2002, the WHO estimated that
2.5 billion people worldwide were at risk of contracting
the disease (WHO 2002). Today, there are an estimated
50 million new infections annually (World Health Organization 2002; Farrar et al. 2007). Although dengue fever
is not often fatal in healthy adults, the attack rate can be
as high as 8090% during epidemics (World Health
Organization 2002). In the past, the cyclical nature of the
disease allowed roughly 1040 years to pass between
epidemics; however, the interval has dramatically
decreased due to a variety of social, economic and
political factors (Gubler & Clark 1995). Despite efforts
to control dengue, the incidence rate continues to climb
1542

and the disease is spreading to new locations (World

Health Organization 2002; Rogers et al. 2006; Farrar
et al. 2007).
Dengue infections are caused by one of four virus
serotypes of the genus Flavivirus and are transmitted via
Aedes aegypti and Aedes albopictus mosquitoes (Gubler
1989; Sulaiman et al. 2002; World Health Organization
2004). A secondary infection with a differing serotype can
lead to dengue hemorrhagic fever (DHF) or dengue shock
syndrome. The case fatality rate for dengue fever is usually
less than 1%; however, in extreme circumstances the rate
for DHF can exceed 20% (World Health Organization
2002). Aedes aegypti prefer sheltered domestic environments and commonly breed in artificial containers with
fresh water such as flower vases, jars, concrete tanks (Kay
et al. 2002; Khun & Manderson 2007), tires, pet water
dishes and discarded items that have filled with rain water

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K. K. Ballenger-Browning & J. P. Elder Ae. aegypti reduction and dengue prevention

(Koenraadt et al. 2006). Aedes albopictus, on the other

hand, breeds primarily outdoors in natural containers such
as coconut shells and tree holes (Gould et al. 1971; Dieng
et al. 2002). As both mosquito species are diurnal and
anthropophilic, vector control activities often require
substantial human intervention.
Erlanger et al. (2008) conducted a recent review of
studies that had as little as a 1 month post-intervention
evaluation. Together, the 57 studies they reviewed indicated that integrated, community-based interventions were
the most effective methods of dengue control for large
populations while environmental management had the least
impact. Although their liberal inclusion criteria allowed
for a larger number of programs to be reviewed and thus
was sufficient for a meta-analysis to be conducted, studies
with only a 1 month post-intervention may not accurately
reflect the sustainability of these methods over a longer
period of time. Similarly, a review by Heintze et al. (2007)
and Elder and Ballenger-Browning (2009) found only weak
evidence that community-based vector control methods
combined with biological or chemical interventions reduced
mosquito populations; however, only 11 community-based
studies were included for their review, which focused
primarily on study design. To the best of our knowledge, no
studies have investigated the role of human behaviour in the
effectiveness and sustainability of an intervention.
The purpose of this paper is to review published literature
on A. aegypti and A. albopictus mosquito reduction

interventions. Like Erlanger et al. (2008) and Heintze et al.

(2007), studies were catalogued by intervention method
and compared the effectiveness of various techniques by
dependent variable. However, to build upon previous
reviews, complicated interventions were divided into distinct treatment groups and longer follow-up times were
assessed using percent reductions to standardize results.

Methods
Inclusion criteria
Searches in PubMed, Science Direct, Google Scholar, and
Cab Direct databases were conducted from July 2007 to
January 2008 using keywords such as dengue control,
Aedes aegypti, Aedes albopictus, mosquito control,
dengue interventions, Breteau index (BI), dengue fever
and dengue vector control to identify potential articles
and reference lists were used to locate other resources.
Figure 1 illustrates article inclusion process. Articles were
included if an intervention was implemented and quantitative pre post-data on larval or adult indices was
reported. Studies measuring mosquitoes other than
A. aegypti or A. albopictus were excluded. Study designs
were organised into cluster randomized controlled trials
(CRT) in which units were grouped into neighbourhoods
or villages and were randomly assigned to receive the
condition; randomized control trials (RCT), individuals or

Assessed for Eligibility

(n = 1238) PubMed,
Google Scholar, Science
Direct, Cab Direct, and
reference lists

Excluded (n = 1007)
Studies describing
vector behaviour,
beliefs, treatment, etc.

Included: (n = 231)
Aedes
aegypti and albopictus
control studies

Excluded (n = 177)
Cross-sectional studies

Figure 1 Selection process for dengue fever

articles.

2009 Blackwell Publishing Ltd

Included: (n = 54)
Intervention with
pre and post data

Excluded (n = 33)
Statistics not included

Included: (n = 21)
Larval or adult mosquito
indices

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K. K. Ballenger-Browning & J. P. Elder Ae. aegypti reduction and dengue prevention

units were randomly assigned to the condition; nonrandomized control trials (CT) in which intervention and
control groups were not assigned through a random
process; and, interrupted time series designs (ITS) in which
there was no control group but multiple data points were
collected before and after the intervention. Unlike the
selection criteria set forth by Erlanger and colleagues,
cross-sectional studies were not included, nor were there
geographic restrictions (Erlanger et al. 2008). Over 1000
articles were reviewed and 21 met the inclusion criteria.
Entomological indices
Among the most commonly used entomologic indices used
were the Breteau index (BI), House index (HI) and
Container index (CI). The BI was defined as the number of
positive containers per 100 houses (Lloyd et al. 1992;
Kroeger et al. 2006). The HI was defined as the number of
positive houses per 100 houses [Pan American Health
Organization (PAHO) 1994; WHO 1997]. The CI was
defined as the number of containers with immature stages
per 100 containers with water (PAHO 1994; Kroeger et al.
2006). Additional variables used to measure larval populations were the Larva Density index (mean number of
larva per container), the Ovitrap index (number of mosquito traps with eggs divided by the total number of traps
multiplied by 100; Pai et al. 2006), the Adult Density index
(number of adult mosquitoes per number of houses
surveyed; Nam et al. 2005), the Indoor Landing Density
(number of female mosquitoes caught per man-hour; Mani
et al. 2005), and the Pupae per Person index (number of
pupae collected per human population in a sector; Kroeger
et al. 2006). Serological data was not reported as the
primary dependent variable, it was given as an ancillary
measurement. Percent reductions of A. aegypti mosquitoes
were calculated using Mullas formula (Mulla et al. 1971):
100(C1 T1 T2 C2) 100.
This formula corrects for natural increases or decreases
occurring in the control group that may have similarly
affected the treatment group over time. The inclusion of
studies and statistics were independently assessed by two
authors and differences were resolved through discussion.
Results
Campaigns to increase knowledge or change human
behaviour were applied in eight studies with three
involving the screening, cleaning or disposal of water
containers. Biological interventions involving copepods or
other predatory organisms comprised another eight of the
21 studies. Although not a true biological control,
bacteria (Bacillus thuringiensis) was also included in this
1544

category due to its organic nature. Chemical interventions were also commonly implemented. Of the eight
studies within this category, five measured the effectiveness of insecticide sprays and or chemical larvicides.
Two studies measured the effectiveness of insecticidetreated materials and one used an insecticide-treated strip
in an ovitrap. Finally, three studies contained behavioural
and biological or chemical components, and therefore are
listed in both categories. Table 1 provides further information on each publications geographical location,
intervention type, study design, sample size and outcome
measures.
Study design
Three studies were CRTs, two studies were RCTs, 14
studies were CTs and two studies were ITSs. Most studies
used either clustered or non-clustered designs that compared the intervention and control groups. Three studies
employed CRTs which are considered the gold standard
design for dengue fever (Lloyd et al. 1992; Perich et al.
2003; Kroeger et al. 2006). Two studies were of questionable quality and did not contain control groups (Gould
et al. 1971; Pai et al. 2006) and one study contained only
one baseline measurement (Pai et al. 2006). The presentation of results varied greatly with only two studies
presenting confidence intervals (Espinoza-Gomez et al.
2002; Kroeger et al. 2006) and eight studies presenting
P-values (Lloyd et al. 1992; Phan-Ural et al. 1995;
Fernandez et al. 1998; Umniyati & Umayah 2000; EspinozaGomez et al. 2002; Perich et al. 2003; Mahilum et al. 2005;
Kroeger et al. 2006).
The BI was reported in eight studies, the HI was reported
in five studies and the CI was reported in seven studies.
Pupae per person was only reported in one study (Kroeger
et al. 2006).
Intervention techniques
Approximately one-third of the studies reviewed contained
educational or behaviour-altering elements. Percent
reductions using Mullas formula were calculated for five
studies (Table 2). The known monitoring durations ranged
from 18 weeks to 15 months with an average reduction of
41.6% (range 4.087.6%). Although the rates of infestation were relatively low to start, the most significant
decrease in A. aegypti populations occurred in Cuba where
a 12-month social mobilization campaign to eliminate
water containers was implemented (Sanchez et al. 2005).
Alternatively, at 15 months post-intervention, only a 4%
reduction was found for an intervention designed to teach
individuals a specific water container cleaning method

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K. K. Ballenger-Browning & J. P. Elder Ae. aegypti reduction and dengue prevention

Table 1 Summary of dengue fever interventions

Reference

Setting

Intervention type

Design and sample size

Borjas et al.
(1993)

El Progreso, Honduras

Biological: juvenile Trachemys

scripta turtles in laundry
containers

Dieng et al.
(2002)

Nagasaki, Japan

Biological: copepods in the

natural environment

Espinoza-Gomez
et al. (2002)

Colima City, Mexico

Fernandez et al.
(1998)

El Progreso, Honduras

Focks et al.
(1987)

New Orleans, USA

Chemical and Behavioural:

larvicide, insecticide sprays,
individual and mass media
educational campaign
Behavioural: cleaning cement
washbasins using the
Untadita method
Chemical: ground-applied
malathion insecticide

CT; T1:n = 6 laundry tanks

T2:n = 30 laundry tanks
(in progress at time of
publication)
CT; n = 6 units of five
water containers
(one control)
RCT; n = 187 houses
(45 controls)

GorrochoteguiEscalante
et al. (1998)

Monterrey, Mexico

Biological: Mesocyclops
longisetus copepods

Gould et al.
(1971)

Koh Samui, Thailand

Chemical: ground-applied
malathion insecticide and
Abate larvicide

Kay et al.
(2002)

Hai Phong, Hung Yen

and Nam Dinh
provinces, Vietnam

Kroeger et al.
(2006)

Vera Cruz, Mexico and

Trujillo, Venezuela

Biological and Behavioural:

copepods and face-to-face
educational campaign
during dengue fever outbreak
Chemical: insecticide-treated
window curtains and water
container covers

Lardeux et al.
(2002)

French Polynesia

Biological: copepods in water

containers

Lloyd et al.
(1992)
Madarieta et al.
(1999)

Merida, Mexico

Behavioural: door-to-door
educational campaign
Chemical: permethrin
treated curtains

Cebu City, Philippines

Mahilum et al.
(2005)

Cebu City, Philippines

Biological: larvicide
Bacillus thuringiensis

Mani et al.
(2005)

Chennai, Tamil Nadu,

India

Chemical: indoor and

peridomestic deltacide
insecticide fog

2009 Blackwell Publishing Ltd

CT; n = 13
neighbourhoods
(five controls)
CT; n = 42 ovitraps
(20 control) N = 7 adult
traps (two controls)
RCT; T1:n = 64 peri-domestic
drums 36 with routine water
use, 18 with no water use
(10 controls) T2:n = 28 tires
(10 controls) T3:n = 68
flower vases at cemetery
(23 controls)
ITS; n = 1108 indoor
containers n = 1318
outdoor containers
(no control)
CT; n = 2 urban communes
(one control) n = 8 rural
communes (three controls)
100 houses per commune
CRT; T1:n = 18 clusters of
houses, 1095 houses (nine
clusters controls) T2:n = 18
clusters of houses, 1122
houses (nine clusters controls)
ITS, no data on sample size
given; no control
information given
CRT; n = 12 four-block
communities (six controls)
CT; n = 130 households in
two barangays (65
households in one
barangay control)
CT; n = 11 breeding sites
(containers selected for
control)
CT; n = 3 residential
communities, 216260
homes in multistory
buildings per community
(one control community)

Outcome
Measurement
Cumulative Larva
Density Index
for all containers
Larva Density
Index
BI and KAP

CI, Washbasin
Infestation
Index
Adult mosquitoes
per trap per hour
CI

CI

BI and serological
testing

BI, HI, Pupae

per person and
serological
testing
CI

BI and HI
BI, HI and CI

Larva Density
Index and
serological testing
BI and Landing
Density

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K. K. Ballenger-Browning & J. P. Elder Ae. aegypti reduction and dengue prevention

Table 1 (Continued)

Reference

Setting

Intervention type

Design and sample size

Outcome
Measurement

Nam et al.
(2005)

Quang Nam and

Khanh Hoa
provinces, Vietnam

CT; n = 4 communes, 100

houses per commune (one
control)

Adult Density Index,

KAP and serological
testing

Pai et al.
(2006)

Three districts of
Kaohsiung, in
South Taiwan
Areia Branca and
Nilopolis,
Brazil

Biological and Behavioural:

copepods and face-to-face
educational campaign
during dengue fever outbreak
Behavioural: mass media
water container clean-up
campaign
Chemical: insecticide
impregnated strip in
mosquito ovitrap

ITS; n = 90 households in
three districts (no control)

Ovitrap Index and

knowledge and
behaviour survey
CI, Adult Density
Index

Perich et al.
(2003)

Phan-Ural et al.
(1995)
Sanchez et al.
(2005)

Amphoe Khlung,
Thailand
Havana City, Cuba

Sulaiman et al.
(2002)
Umniyati and
Umayah (2000)

Kuala Lumpur,
Malaysia
Yogyakarta,
Indonesia

CRT; n = 30 houses at two

neighbourhoods in two
municipalities (one
neighbourhood per
municipality control)
CT; n = 2 villages, 153 houses
(92 houses in control village)
CT; n = community leaders in
two communities (one control
community)
CT; n = 3 sectors of 10 houses
each (one sector control)
CT; n = 2 neighbourhoods of
187 houses (90 houses in
control neighbourhood)

Biological: larvicide
Bacillus thuringiensis
Behavioural: social
mobilization and
education
Chemical: cypermethrin and
cyfluthrin insecticide spray
Behavioural: emptying,
washing and removing water
containers with mosquito larva

BI, HI, CI and Landing

Density Index
HI, Percent of
Mosquito-Free blocks
Percent Mortality
BI and Ovitrap Index

CT, non-randomized controlled trial; CRT, clustered randomized control trial; ITS, interrupted time series; RCT, randomized controlled
trial; T, treatment group; n, sample size.
Table 2 Summary of results of behavioural interventions

Duration

Mullas
percent
reduction

unknown

73.1

15 months

4.0

6 months

22.9

12 months

87.6

1.7
28.2

18 weeks

33.1

34.4
54.1

29.9
26.7

18 weeks

28.6

35.2

29.3

Reference

Treatment and control groups

Index

Baseline
measure

Espinoza-Gomez
et al. (2002)
Fernandez et al.
(1998)

T3: educational campaign only

C: no treatment
T1: banners, household visits to teach
container cleaning technique, radio spots
C1: neighbourhoods in two towns, exposed
to radio spots
T: door-to-door education campaign
C: no treatment
T: covering and elimination of unused
containers and education of health professionals
C: untreated neighbourhood
T1: emptying, cleaning, covering containers
and removing discarded materials indoors
C1: untreated neighbourhood
T2: emptying, cleaning, covering containers
and removing discarded materials outdoors
C2: untreated neighbourhood

BI
BI
CI

125.5
102.2
26.6

38.2
115.5
19.7

CI

31.4

24.2

BI
BI
HI

126.0
113.9
3.7

129.0
151.3
0.6

HI
OI

1.3
48.5

OI
OI
OI

Lloyd et al.
(1992)
Sanchez et al.
(2005)
Umniyati and
Umayah (2000)

Last
measure

T, treatment group; C, control group; BI, Breteau index; CI, Container index; HI, House index; OI, Ovitrap index.

(Fernandez et al. 1998). Subjects were randomized in only

two studies, with only one using clustered randomization
(Lloyd et al. 1992).
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Nearly all biological interventions such as copepods,

turtles and bacteria concluded in complete eliminations of
mosquito larva (Table 3). Intervention monitoring periods

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K. K. Ballenger-Browning & J. P. Elder Ae. aegypti reduction and dengue prevention

Table 3 Summary of results of biological interventions

Baseline
measure

Last
measure

Duration

Mullas
percent
reduction

2 months

100.0

3
3
3
3

months
months
months
months

100.0
100.0
100.0
100.0

21 months

92.0

21 months

()

Reference

Treatment and control groups

Index

Borjas et al. (1993)

T1: 6 month old turtles in household water

containers
C1: water containers without turtles
T1: Macrocyclops copepods in containers
T2: Megacyclops copepods in water containers
T3: Mesocyclops copepods in water containers
T4: Mixture of three copepod species
C: no copepods
T1: educational campaign and Mesocyclops
copepods in urban neighbourhood
C1: untreated urban neighbourhood
T2: educational campaign and Mesocyclops
copepods in rural neighbourhood
T3: same as T2
T4: same as T2
T5: same as T2
T6: same as T2
C2: untreated rural neighbourhood
T1: educational campaign and Mesocyclops
copepods
T2: same as T1
T3: same as T1
C: untreated village
T: Bacillus thuringiensis in water containers
C: untreated village

LD

20.0

0.0

LD
LD
LD
LD
LD
LD
BI

42.0
0.1
1.6
3.7
0.1
14.7
57.0

51.5
0.0
0.0
0.0
0.0
16.7
3.0

BI
BI

53.0
0.0

35.0
0.0

BI
BI
BI
BI
BI
AD

32.0
10.0
15.0
23.0
25.0
1.2

0.0
1.0
2.0
0.0
30.0
0.0

AD
AD
AD
BI
BI

0.1
0.1
0.7
429.8
344.5

0.0
0.0
0.4
52.0
167.1

Dieng et al. (2002)

Kay et al. (2002)*

Nam et al. (2005)*

Phan-Ural et al.
(1995)

21
21
21
21

months
months
months
months

100.0
91.7
88.9
100.0

3 years

100.0

3 years
3 years

100.0
100.0

4 months

75.1

T, treatment group; C, control group; BI, Breteau index; CI, Container index; LD, Larva density index; AD, Adult density index.
*Contain both biological and behavioural (integrated) interventions.

spanned from 2 months to 3 years with a mean reduction

of 96.3% (range 75.1100%). Two interventions within
this category contained integrated methods in which
educational campaigns were simultaneously employed. All
studies within this category utilized CT study designs with
the exception of Gorrochotegui-Escalante et al. (1998),
who used a RCT design, and Lardeux et al. (2002), who
only used pre- and post-tests within the same sample.
Chemical sprays have been widely used during dengue
fever epidemics for their ability to quickly and effectively
eradicate mosquito populations (WHO 1997). The known
intervention monitoring periods spanned 7 days to
5 months and showed the greatest range in mosquito
populations post-intervention (Table 4). Although the
average reduction was 27.2% (range 73.813.9%), the
most significant decreases were found 5 months postintervention using an ovitrap treated with insecticide
(Perich et al. 2003). Four studies used CTs, one used an
ITS design and one study was a RCT. Two studies used
clustered randomization (Perich et al. 2003; Kroeger et al.
2006). Based on the results of this review, chemical
interventions may not be a long-term solution due to the

2009 Blackwell Publishing Ltd

short-term effectiveness of these products. Mixed or slow

release chemical products may provide longer lasting
results; however, no studies employing these techniques
met our inclusion criteria.
Discussion
Overall, the results of this review have demonstrated that
little concrete evidence exists to support the efficacy of
mosquito abatement programs on reducing the incidence of
dengue fever. Weak study designs, incongruent indices and
poorly reported statistics contribute to the questionable
results. Despite this, valuable information regarding the
practicality of vector control interventions was discussed.
Behavioural interventions
Most behavioural interventions target human behaviour
change, either directly or indirectly through changes in
knowledge and attitude. One advantage is that responsibility for health issues is placed in the hands of individuals
and communities (Lloyd et al. 1992; Sanchez et al. 2005).
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Table 4 Summary of results of chemical interventions

Reference

Treatment and control groups

Index

Espinoza-Gomez
et al. (2002)*

T1: malathion ULV spraying

T2: malathion spraying and educational campaign
C: no treatment
T: ULV malathion sprays
C: untreated neighbourhood
T1: insecticide-treated net curtains and pyriproxyfen
in water containers
C1: untreated neighbourhood
T2: PermaNet insecticide-treated curtains and
covered water containers
C2: untreated neighbourhood
T: 23 permethrin-treated curtains
C: untreated neighbourhood
T1: vehicle mounted peridomestic fogging
C1: untreated neighbourhood
T2: ground-sprayed indoor fogging
C2: same as C1
T1: ovitrap with deltamethrin insecticide
C1: untreated neighbourhood
T2: same as T1
C2: same as C1

BI
BI
BI
MT
MT
BI

110.8
53.0
102.2
12.3
9.3
60.0

102.2
32.6
115.5
11.9
7.9
7.0

Unknown

9.9

BI
BI

113.0
38.0

12.0
11.0

Unknown

42.1

BI
BI
BI
BI
BI
BI
BI
CI
CI
CI
CI

34.0
131.0
98.5
76.7
40.0
50.0
55.0
6.1
4.8
10.3
13.2

17.0
46.0
38.8
55.0
42.5
37.5
47.2
5.1
10.0
3.6
17.6

5 months

10.9

14 days

32.5

14 days

12.7

4 months

59.9

4 months

73.8

Focks et al. (1987)

Kroeger et al. (2006)

Madarieta et al. (1999)

Mani et al. (2005)

Perich et al. (2003)

Last
measure

Mullas
percent
reduction

Baseline
measure

Duration
unknown
unknown
7 days

18.4
45.6
13.9

T, treatment group; C, control group; BI, Breteau index; CI, Container index; MT, adult mosquitoes trap per 24 h.
*Contain both chemical and behavioural (integrated) interventions.
Data is given using the Container index, yet the description matches that of the Breteau index: proportion of containers positive per house.

However, education programs must target behaviours that

are feasible for target population in terms of skills, time and
resources. Additionally, the new behaviours must produce
results that are visible (or at least measurable; see below)
and that can be monitored (Parks & Lloyd 2004; Elder &
Lloyd 2007). Although protecting and emptying water
containers is a relatively simple and inexpensive method of
reducing mosquito populations, there are distinct disadvantages. Firstly, emptying and improper scrubbing of
containers may not kill mosquito eggs (Sherman et al.
1998). Secondly, there are misconceptions regarding the
management of water containers. For example, people
often forgot to cover them, while others believed that an illfitting lid was still effective (Phuanukoonnon et al. 2006).
Thirdly, increased knowledge does not necessarily equate to
behaviour change (Lloyd et al. 1992; Fernandez et al. 1998;
Winch et al. 2002; Pai et al. 2006).
The studies examined in the present review also suggest
that efforts to mobilize community members are essential
for the sustainability of vector control methods. As one
study found, clean-up campaigns that encourage community members to remove trash from the premises require an
infrastructure for the disposal of waste (Lloyd et al. 1992).
Cooperative involvement of individual homeowners, com1548

munity leaders and governmental bodies help to ensure

that this infrastructure exists to continue dengue programs
once an intervention has concluded. This analysis mirrors
several authors conclusions that successful mosquito
control efforts should neither be purely top down nor
bottom up, but instead utilize the strengths of each level
(Gubler 1989; Heintze et al. 2007). Substantial success has
been realized through interventions that use integrated
educational and either chemical or biological methods of
vector control (Heintze et al. 2007; Erlanger et al. 2008).
An optimally integrated approach would concurrently
consider the mosquitos lifecycle and the various control
actions that best address the vector at each of these stages.
We present examples of the interface between actions and
the vectors cycle in Figure 2 (adapted from Elder &
Ballenger-Browning 2009).
Biological interventions
When solely looking at Mullas percent reductions, biological techniques were the most successful and sustainable
class of interventions. In two cases, clinical surveillance of
dengue fever was evidence of disease decline (Kay et al.
2002; Nam et al. 2005). Both studies utilized an integrated

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K. K. Ballenger-Browning & J. P. Elder Ae. aegypti reduction and dengue prevention

Insecticide sprays
Treated materials
Adult
mosquito

Source reduction
Water removal
Ovitraps
Ova

Human
Education
Repellent

Adult
mosquito

Turtles
Larva and
Copepods
pupa
Fish
Larvicide

Figure 2 Mosquito life cycle and related intervention strategies.

approach in which community members were taught

modify their existing practices to maintain copepods in
water containers and to dispose of unsuitable water
containers. Biological methods of vector control such as
copepods and bacteria, were also highly accepted by
homeowners (Borjas et al. 1993; Gorrochotegui-Escalante
et al. 1998; Kay et al. 2002; Nam et al. 2005), were lethal
only to the targeted vector and did not chemically
contaminate the environment (World Health Organization
1997). Nevertheless, six biological studies (75%) were
non-randomized assessments which inherently provide
limited information.
According to field reports, the primary disadvantages of
using predatory organisms included labour intensive
maintenance (World Health Organization 1997; Lardeux
et al. 2002) and high turnover of organisms for containers
with frequent use (Fernandez et al. 1998). Several authors
reported that water was emptied or was subject to seasonal
drying; resulting in the death or escape of the organism
(Borjas et al. 1993; Gorrochotegui-Escalante et al. 1998;
Lardeux et al. 2002; Mahilum et al. 2005) and one
concern issued by the World Health Organization (1997)
was that stronger, healthier adult mosquitoes might result
from lower larval densities.

designs, as no true comparison can be made between

randomized and non-randomized studies.
There are a number of disadvantages to insecticide
spraying. Foremost, the use of insecticides as a primary
control method has led to widespread chemical resistance
(Gould et al. 1971; Lardeux et al. 2002; Chadee et al.
2005). According to Focks et al. (1987), mosquito populations rebounded quickly from insecticide sprays since
one-third of adult mosquitoes survived and larva populations were not affected. Secondly, A. aegypti prefer indoor
environments which often prevents contact with insecticides (Gubler 1989; Mani et al. 2005). Several studies
noted that for insecticides to be effective, a high level of
community involvement was necessary for success, as
people must leave their doors and windows open when
spraying occurred (Focks et al. 1987; Mani et al. 2005).
Health concerns regarding insecticide application were
mentioned in a variety of analyses. Interviewees cited the
chemical as causing coughs and irritation of the respiratory
tract (Kroeger et al. 1995), while others believed that
insecticide sprays would contaminate food and condoned
outdoor spraying only (Phuanukoonnon et al. 2006).
An alternative to insecticide spraying is the use of
insecticide-treated materials. Interventions conducted in
Mexico, Venezuela (Kroeger et al. 2006) and the Philippines
(Madarieta et al. 1999) hung chemically impregnated window curtains. Despite reductions in the intervention groups,
the effectiveness of these studies is questionable owing to
comparable reductions in the control groups (Madarieta
et al. 1999; Kroeger et al. 2006). Given that A. aegypti are
primarily diurnal, the protection offered by curtains was
somewhat limited (World Health Organization 1997), yet
certain groups may benefit, such as bed-ridden or infirm
individuals and babies (Chadee et al. 2005). Curtains also
had the added benefit of providing visual reinforcement since
individuals could see dead mosquitoes. Evidence suggests
that impregnated curtains might also protect against other
vector-borne diseases like malaria, leishmaniasis and chagas
disease (Kroeger et al. 2006).

Chemical interventions
It is widely accepted that insecticides are effective at
reducing mosquito populations; moreover, the results can
be seen and felt immediately (Phuanukoonnon et al. 2006).
The use of chemical larvicides effectively reduces mosquito
populations; however, no articles included in this study
measured the effectiveness of larvicides alone. The results
of Mullas percent reductions were the most diverse for
chemical interventions, compared to all other categories. In
some instances, larval populations decreased dramatically
(73.8%), while some populations increased (13.9%). This
finding illustrates the frustration of having limited study

2009 Blackwell Publishing Ltd

Limitations
The studies were limited by the lack of congruency and
inherent weaknesses in the entomological measurements.
The BI, the HI and CI under-estimate the mosquito population by failing to describe larva densities (Service 1976;
Tun-Lin et al. 1996; Espinoza-Gomez et al. 2002). The
recent trend in dengue research has turned away from the use
of larval indices in favour of pupal indices because of the high
correlation between pupae and adult mosquitoes. Being able
to easily identify pupae of a particular species and to count
the absolute number of individuals makes this index
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K. K. Ballenger-Browning & J. P. Elder Ae. aegypti reduction and dengue prevention

particularly advantageous (Focks et al. 2000). Also, none of

the indices can be directly tied to human behaviours required
to control these containers, creating the potential for
individuals making sincere attempts to become frustrated
and others to remain confident that little or no action is
warranted. Researchers continue to be challenged with
identifying both valid human behavioural links to container
control and affordable measures of these behaviours.
Validity and affordability must be in balance; for example,
numbers of ITNs distributed from a central inventory may be
far easier to track then visual verification of household ITN
use, while such verification is far more valid than householder self-reported use. Another significant limitation of the
collective body of published literature is poor surveillance of
dengue fever. While even minimal reductions in Aedes
mosquito indices were reported in all studies, very few
articles monitored changes in disease rates.
The analysis of dengue interventions poses a number of
challenges. First, studies published in languages other than
English were not included, neither were studies found in
governmental and non-profit publications. This is indeed a
limitation of this review. Furthermore, limited baseline and
post-intervention data resulted in a small sample size of
only 21 studies. Study design was also a significant limiting
factor. Clustered RCT are the gold standard for experimental testing; however, only three studies met this
criterion. Likewise, P-values were present in only eight
studies and therefore advanced statistical comparisons
could not be made.
In summary, dengue fever is a global problem that shows
no signs of slowing (Gubler 1989). As a result, future
research should be conducted using clustered randomizedcontrol trials to eliminate speculation about the casual
relationship of the intervention to the rates of dengue fever
transmission. Finally, serological surveillance should be a
necessary component of all dengue interventions and a
standard entomological index, such as the Pupae per
Person index, should be used to aid in the comparability of
studies. At the same time, more reliable and valid measures
of vector control actions need to be developed in order for
community interventions to be refined and disseminated.
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Corresponding Author K. Ballenger-Browning, C o John Elder, Graduate School of Public Health, San Diego State University, 9245
Sky Park Court #221, San Diego, CA 92123, USA. Tel.: +1 6195328777; Fax: + 6195326030; E-mail: kara.browning@med.navy.mil

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