A Review of the Dengue Mosquito, Aedes

aegypti (Diptera: Culicidae), in Australia

Deon Canyon (PhD)
Tropical Infectious and Parasitic Diseases Unit, School of Public Health and Tropical Medicine, James Cook
University, Townsville Qld 4811, Australia. Deon.Canyon@jcu.edu.au
Dengue
The cosmo-tropical mosquito, Aedes aegypti (Linn. Diptera: Culicidae), serves as the most
important domestic vector of urban yellow fever and dengue (Gubler, 1988; Warren and
Mahmoud, 1990). Ae. aegypti was probably introduced to Australia during the mid 19th
century (Marks, 1974) and dengue epidemics soon followed. Dengue has manifested itself in
epidemic form in Australia since 1879 till the present. A general infection rate of 75% has
been proposed for all areas experiencing dengue up until the 1953-1955 epidemic. Since then,
infection rates have ranged from 2 - 38% depending on geographical area (Kay et al., 1984).
The relationship between death and percentage of population infected varies substantially.
Hayes and Gubler (1992) suggested that from 1 to 7 dengue hemorrhagic fever cases would
typically result from 100 dengue fever cases and that prior to the development of modern and
adequate hospital management, 50% of all DHF cases would die.
The earliest known epidemics occurred from 1897 to 1901 and spread throughout most of
Thursday Island, Townsville, Cairns, Cooktown, Pt. Douglas, Charters Towers, Normanton,
Mackay, Ingham, and Bowen to Brisbane with cases inland at Hughenden, Barcaldine etc.
This widespread epidemic penetrated into New South Wales by 1898. Cases continued to be
reported including at least 3 deaths in Charters Towers (Cleland and Bradley, 1918) and 3
deaths in Brisbane from 1899-1901 (Evaluation Group, 1990). The population of Queensland
was around 500,000 (Cameron, 1997) in 1900 so, based on an infection rate of 75%, it is
possible that 375,000 people were infected with dengue. Cases continued to a lesser degree
until 1904-1906, when the virus traveled north to infect all on Thursday Island and south to
cause an extensive epidemic in Brisbane in which 94 deaths occurred. One death was also
reported in Sydney. Using the previous logic, an estimated 190 DHF cases probably occurred
with a maximum of 19,000 cases of dengue fever. If only 15% actually reported to a health
clinic for examination (Kay et al., 1984), a probable 126,730 people were infected in and
around the Brisbane region. The population of Brisbane at this time was around 126,000
(Cleland and Bradley, 1918). Thus the rate of 1 death to 1,000 possible cases seems likely.
Over the period from 1985 to 1923, 52 deaths were recorded in the Townsville region
(Lumley and Taylor, 1943), which arose from around 52,000 probable infections. From 1916
to 1919 and in 1924, New South Wales and Queensland were broadly struck with a similar
infection rate and the number of infected people is estimated at 600,000 (Cleland and
Bradley, 1918; Walker et al., 1942; Lumley and Taylor, 1943) in each of the two epidemics.
From 1938-1939, dengue made another appearance, which led to the 1941-43 epidemic. At
this time, 486 cases were reported in Townsville equivalent to an estimated 610 infected
individuals. During 1941-1943 a little known epidemic swept Queensland down to Brisbane
with up to 85% infection rates in some towns. In Townsville alone, 5000 cases were reported
with 25,000 probable infections. Judging from past performance and taking other areas into
account, it is guesstimated that this figure could at least be doubled. Dengue struck again in
1953-1955 infecting 75% of the population with an estimated 15,000 cases (Doherty, 1957).
In 1981-1983 dengue returned to Queensland and was confirmed in 458 people. Using the
recent notification rate of 15% found by Kat et al. (1984), a possible 3100 people were
infected in this epidemic. From 1991 to 2000, 2294 confirmed cases have been reported
translating to a probable 15,500 infections.
Cumulatively, this leads to a figure of 1,837,940 dengue infections in Australia in the last
century, which is certain to be conservative due to a lack of information on numerous places
that experienced epidemics.
Distribution
While the latitudinal limits of Ae. aegypti are 45 North and 40 South of the equator, Ae.
aegyptis distribution is more closely correlated with the 10C isotherms (Tabachnick and
Powell, 1979). Estimates of Ae. aegypti distribution and density are affected by the life-
limiting factors of latitude, altitude, temperature, rainfall, humidity, season, habitat and
dispersal (Surtees, 1967; Chinery, 1970; Service, 1974; Russell, 1986; Russell and Whelan,
1986; Scott, 1988; Fontenille and Rodhain, 1989; Koopman et al., 1991; Schultz, 1993). A
model, able to predict Ae. aegypti abundance in Puerto Rico using climatological data
(Moore, 1985), showed that temperature was not a good indicator of larval abundance, but
the amount of rain and number of rainy days over a given period were useful predictors of
abundance. The average temperature during the rainy season was also found to relate strongly
with the estimated risk of dengue infection to the community in Mexico (Koopman et al.,
1991). The same authors found altitude (low-10 m versus high-1200 m) and humidity (moist
versus dry) to be significantly and independently associated with infection.
Seasonal variation and habitat
Seasonal variation in population density and distribution is common for Ae. aegypti since it is
sensitive to changes in temperature and available moisture. Essentially, low mosquito
populations are evident in dry and cool seasons and they increase when temperatures increase
and the wet season commences (Schultz, 1993). In areas like Townsville and Charters
Towers, the climate is semi-arid and Ae. aegypti still occurs year round (Gary Owens,
Townsville City Council, pers. com.; pers. obs.) due to subterranean sites (Russell et al.,
1996) and watering practices. The existence of this species throughout the year is probably
due to the arid climate and subsequent behavior by local residents. Yards have to be watered
more frequently to maintain vegetation such as flowering plants, but this practice may serve
to create and sustain small compact breeding sites. Ae. aegypti habitats vary almost as greatly
as mans habitats, for their primary requirement is the presence of man. Their close
association with man or anthropophilic nature has been shown in many studies (MacDonald,
1956; Surtees, 1969; Harrison et al., 1972; Trpis and Hausermann, 1978; Kay et al., 1985;
Kemp and Jupp, 1991; Schultz, 1993).
Ae. aegypti breeding site preferences have been studied in many areas with varying results.
Discarded automotive tires were found to be an ideal site in the USA (Tinker, 1964;
Chambers et al., 1986) and in Puerto Rico (Moore et al., 1978), whereas large drums were
preferred in Colombia (Nelson et al., 1984). In a brief overview of typical breeding sites
around the world, Ae. aegypti is clearly well able to utilize any available breeding site (Table
1).
The number of positive large water holding sites like drums and water storage jars averaged
39%, mid-sized containers like rock holes, buckets and tires averaged 44%, and all other
small containers averaged 48%. A reduction in large water storage containers due to the
introduction of piped water could be expected to reduce the overall mosquito population and
increase the number of positive mid to small sized containers. Seasonality is unlikely to
influence breeding sites that are maintained by human activities, however, small rain-filled
breeding sites could be severely affected since they require frequent refilling to maintain
larvae.
Figures 1 and 2 below show typical breeding sites with disposables, pot bases and a trailer.
Interestingly, an overlooked water-filled trailer located under a property adjacent to the
Cairns hospital was responsible for producing millions of mosquitoes which were suspected
of playing a major role in the 1997-1999 dengue epidemic in Cairns.
Fig. 1 Fig. 2

Investigations into the nature of Ae. aegypti breeding sites in Northern Australia by Barker-
Hudson et al. (1988) and Tun-lin et al. (1989) found a significant amount of breeding in water
tanks in the four areas: Townsville, Charters Towers, Cairns and Thursday Island. In the
larger, more developed cities (Cairns and Townsville), few water tanks exist and the majority
of breeding sites were garden accoutrements such as pot bases and plant striking containers.
Initially, this adaptation towards smaller breeding sites was thought to be due to the absence
of larger sites, however, the subterranean pits used by telecommunication companies have
been shown recently to be very productive Ae. aegypti breeding sites in Townsville (Russell
and Kay, 1996), but not in Cairns (Scott Ritchie, Cairns Tropical Public Health Unit, pers.
com.). The current situation is that Ae. aegypti has established itself in large and small
breeding sites in distinctly different circumstances. Whether the breeding sites are
subterranean or in small containers in the urban setting, location and treatment is a difficult
problem requiring a multifaceted approach and there is an obvious need for new technologies
and methods to deal with the situation. The proliferation of small breeding sites results in
more costly surveillance and treatment by vector control workers. New control strategies are
needed to effectively address resident behavior in addition to adaptive breeding site selection
and oviposition behavior, which have resulted from alterations in the human environment.
Table 1 - Common Ae. aegypti breeding sites around the world
Country Breeding Site % Positive Wet
Containers
Source
Townsville garden vessels 23-38% Barker-Hudson et al, 1988 and Tun-lin et al,
1989
water storage 33%
discarded
items
26-36%
rubbish 21-27%
other 9-19%
Charters
Towers
garden vessels
water storage
7%
23%
discarded
items
8%
Cairns garden vessels 13%
water storage 29%
discarded
items
11%
rubbish 24%
other 21%
Thursday Island garden vessels
water storage
22%
27%
discarded
items
20%
rubbish 17%
other 31%
Tanzania rock holes 84% (Trpis, 1972)
tires 23%
coconut shells 100%
tins 44%
snail shells 67%
Thailand tires 74% (Kittayapong and Strickman, 1993)
water jar 42%
large jar 16%
ant trap 90%
coconut shells 63%
metal drum 20%
water jar 32% Tonn et al., 1969
ant traps 58%
Pacific
Region
drums 37% Suzuki and Hirshman, 1977
tires 25%
tree holes 4%
Fiji drums 61% Kay et al., 1995
tires 65%
tins/bottles 6%
Indonesia cement cistern 66% Jumali et al., 1979
clay pots 19%
bamboo ends 18%
coconut shells 9%
Dominican
Republic
drums 54% Tidwell et al., 1990
vases 49%
small cont. out 48%
small cont. in 19%
bucket 15%
earthen jars 39%
tires out 41%
tires in 25%
Dispersal
Habitat availability also influences the rate of dispersal within a population. Apostol et al.
(1994) analyzed Ae. aegypti oviposition behavior using DNA amplified by polymerase chain
reaction markers to estimate the number of families at oviposition sites. They found that
most mosquitoes oviposited within 90 m of their origin, several oviposited between 90 and
150 m and very few from 150 to 430 m. Oviposition containers yielding large numbers of
eggs revealed large numbers of families and those containers with a small egg yield also had
few representative families. It was suggested that females ovipositing fewer eggs into
crowded vessels would disperse further to locate less occupied oviposition sites. A rapidly
growing population would thus disperse with increasing speed in enlarging circles.
More recently, mark-release-recapture studies conducted on Ae. aegypti in Pentland, a small
town inland from Townsville, by Muir and Kay (1998) showed the mean distance traveled by
recaptured females and males was 56 m and 35 m respectively, while a maximum dispersal
distance of 160 m was recorded for both sexes. These shorter dispersals were thought to have
been due to hot and dry weather, which typically occurs in this area. Thus, Ae. aegypti in
these conditions may be more focused around their site of origin, which suggests that less
widespread control efforts may suffice to control the mosquito population.
Control
Despite the implementation of various and extensive mosquito control practices and the
formation of a new Dengue Action Response Team (DART) under Queensland Healths
Tropical Public Health Unit in Cairns in response to the 1997 Cairns outbreak, Ae.
aegypti continues to thrive in northeastern Australia.
Although the current dengue management plan used by Queensland Health is based on active
case detection using serological and clinical methods, entomological surveillance with the
aim of detecting changes in adult or immature Ae. aegypti populations, is a crucial component
of active dengue surveillance. Ecological, behavioral and control information on population
size, distribution, survivorship, seasonal abundance and insecticide susceptibility is urgently
required for an understanding of epidemic potential, and for the formulation of control
strategies. Periodic surveys designed to detect changes in key adult indices are important
since they allow the detection of adult population fluctuations, which may prompt changes to
vector control strategy.
Local authorities in Townsville, Cairns and Charters Towers make fairly regular random
inspections to control breeding habitats. In Townsville, oviposition traps are placed, urban
premises are inspected and breeding sites are either emptied or treated with temephos
(Abate

) depending on their size (Gary Owens, Townsville City Council, pers. com.).
Despite these efforts, the mosquito population has probably not been reduced sufficiently to
eliminate the possibility of dengue epidemics. Recent and previous epidemics have generally
been restricted to North Queensland. This indicates a significant contraction of dengue-
receptive areas, which frequently included all of Queensland and northern New South Wales.
All dengue epidemics in Australia have originated from viremic cases imported from
neighboring Asian countries, South America and Papua New Guinea (Scott Ritchie and
Disease Notifications, Queensland Health, pers. com.).
Control operations thus have to use the most appropriate insecticides and must be quickly
mobilized in the event of dengue introduction to maintain non-endemic status and to ensure
that minimum local transmission occurs. The choice of the most appropriate chemicals relies,
in part, on insecticide susceptibility studies that are able to indicate both the most effective
insecticides and the insecticides that are no longer appropriate. When malathion fell into
disuse around ten years ago, natural pyrethrum and synthetic pyrethrum (bioresmethrin)
became the primary adulticides in Townsville and Cairns respectively (Ian Kuhl, Townsville
City Council, pers. com.). Ultra-low-volume (ULV) aerosols are applied only in dengue
epidemics such as the one in 1992-1993, but since Ae. aegypti is somewhat unaffected by
truck-sprayed cold ULV-aerosols (Reiter, 1993), any reduction in the susceptibility of Ae.
aegypti to insecticides used in fogging is at best an artifact of control operations targeting the
local salt marsh nuisance mosquito and Ross River Virus vector, Ae. vigilax (Skuse).
Temephos, an organophosphate larvicide, has also been used in North Queensland for the
past 15 years (Ian Kuhl, pers. com.) to treat large water holding containers, like water tanks
and 200-L drums. Another larvicide, S-methoprene, an isomer of methoprene, has also
recently been introduced to vector control operations in Townsville and Cairns (Ian Kuhl,
pers. com.).
Fig. 3 (WHO) The photo below shows a typical resistance testing setup for adult mosquitoes.

It is a popular view that the use of chemical insecticides is an extreme measure, which is in
essence environmentally unsound. Biological control, on the other hand, is often viewed as
environmentally friendly and many think it will pave the way to a brighter future. Service
(1995), however, views both these control methods as extreme and considers source
reduction, growth regulators and repellents as more moderate measures. He concludes that
pesticide use in vector control will continue well into the future since new, more effective and
less harmful developments are not currently in sight. Whether or not vectors are transmitting
disease also influences the type of control method used. In areas experiencing epidemics,
efficacious and fast-acting chemical pesticides must be employed. Nuisance mosquitoes that
are not a public health risk can be dealt with using slower acting or less effective control
methods. Endemic areas can be dealt with by combining the two methods using unrelated
insecticides since epidemics occur periodically and the rest of the time there are relatively
few cases. The vector target also changes depending on the presence or absence of disease.
When disease does not abound nuisance mosquitoes and potential disease vectors are dealt
with primarily by source reduction and larviciding. When epidemics occur, adulticides
constitute the front line defense against potentially infectious adult vectors.
Biological control with B.t.i.
While numerous biological control agents can kill mosquitoes, only one biological
agent, Bacillus thuringiensis subsp. israelensis (B.t.i.), has seen widespread operational use
for the control of mosquito larvae. B.t.i., a spore forming Bacilli, was discovered in a
stagnant pond located in the Nahal Besor Desert river basin near Kibbutz Zeelim in the north-
western Negev Desert of Israel (Margalit, 1990) in 1976 by Goldberg and Margalit (1977).
de Barjac (in Nugud and White, 1982) identified the new bacterial strain and designated it B.
thuringiensis subsp. israelensis serotype H14. Many studies, such as those by Lacey and
Lacey (1981), Nugud and White (1982), Lacey and Inman (1985), Kramer et al. (1988),
Tietze et al. (1994), and Chui et al. (1995), have evaluated and confirmed the larvicidal
capacity of B.t.i. for many mosquito species in different parts of the world.
Thomas and Ellar (1983) describe the mode of action of B.t.i. endotoxins. B.
thuringiensis produces a proteinaceous parasporal crystalline inclusion during sporulation.
When this is ingested by an insect, it solubilizes in the midgut and releases proteins called d-
endotoxins. These proteins disrupt internal membranes and result in death. In addition to
B.t.i.s effectiveness against arthropods, the World Health Organization (1995) reports an
excellent safety record and a very low mammalian toxicity: LD
50
values for both oral and
dermal toxicity are more than 30,000mg/kg.
Most studies on Bacillus thuringiensis resistance development have been done with
Lepidopteron populations and considerably fewer have been done on mosquitoes
(Tabashnick, 1994). Such studies were undertaken because of the fear that resistance to B.t.i.
would develop quickly as it had to other insecticides. In an effort to examine the possibility
of resistance occurring and the speed at which it would occur in mosquito populations,
Goldman et al. (1986) attempted to artificially select wild and laboratory populations of Ae.
aegypti for resistance to B.t.i.. After 14 generations, one wild strain from Rio de Janeiro,
Brazil had developed a slight, but significant twofold increase in resistance. A study by
Becker and Ludwig (1993) on B.t.i. resistance in Ae. vexans (Meigen) field populations that
had sustained 10 years of B.t.i. control, revealed change in susceptibility. The future for B.t.i.
is promising since the development of resistance to B.t.i. in mosquitoes is by no means
comparable to the speedy and encompassing growth of resistance to organochorine,
organophosphate, carbamate and synthetic pyrethroid insecticides.
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