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. aegypti’s distribution is more closely correlated with the 10°C 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 man’s 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

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 Health’s 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: ‘LD₅₀ 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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