Surveillance and Control of Aedes aegypti and Aedes albopictus in the United States

Intended Audience

Vector control professionals

Objectives

The primary objective of this document is to provide guidance for Aedes aegypti and Aedes albopictussurveillance and control in response to the risk of introduction of dengue, chikungunya, Zika, and yellow fever viruses in the United States and its territories. This document is intended for state and local public health officials and vector control specialists.

Overview

In the United States, mosquitoes transmit a variety of arboviruses (arthropod-borne viruses). This document is limited to arboviruses transmitted by Ae. aegypti and Ae. albopictus, the principal vectors of dengue (DENV-1, DENV-2, DENV-3, DENV-4), chikungunya (CHIKV), yellow fever (YFV), and Zika (ZIKV) viruses. Of the above seven arboviruses, DENV, YFV and CHIKV have caused outbreaks within the United States and its territories in the past 110 years. Whereas dengue viruses are endemic throughout territories of the United States, including Puerto Rico, American Samoa, Guam, Northern Mariana Islands and the US Virgin Islands, only sporadic outbreaks of dengue occur in the continental United States. Most recently, focal outbreaks of locally transmitted dengue have occurred in Florida, Hawaii, and Texas. In 2014, 11 cases of locally acquired CHIKV infections were reported in Florida. YFV, once common in the United States, has not caused locally transmitted outbreaks simnce 1905. However, it circulates in tropical forests of Latin America and infected travelers periodically return to the United States. In 2015, ZIKV outbreaks have, for the first time, been reported in the Western Hemisphere, with local transmission occurring in Central and South America, the Caribbean and Mexico. It is expected that ZIKV transmission will increase throughout the region increasing the incidence of infection in returning travelers and the possibility of local transmission in the USA.

Though none of these arboviruses continuously circulate in the continental United States, local outbreaks have and will continue to occur as a result of virus importation by infected, viremic travelers. Any travelers visiting or returning to parts of the United States with established populations of Ae. aegyptior Ae. albopictus mosquitoes could initiate local virus transmission.

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Transmission cycle

In the United States, people serve as primary vertebrate hosts. Viruses: Chikungunya, Dengue, Yellow fever, and Zika. Vectors: Aedes aegypti, Aedes albopictus.

CHIKV, DENV, YFV, and ZIKV are maintained in enzootic transmission cycles in forested areas of Africa, Asia, or South America. YFV is only endemic in Africa and South America. In urban and suburban areas however, these arboviruses are transmitted between people by Aedes mosquitoes in the subgenus Stegomyia especially Ae. aegypti (the main vector worldwide) and potentially, Ae. albopictus.

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Global Distribution

Aedes aegypti most likely originated in Africa; since then, the mosquito has migrated globally throughout the tropical, subtropical, and parts of the temperate world, through global trade and shipping activities (Powell and Tabachnick 2013). Aedes aegypti mosquitoes have a high vectorial capacity (effectiveness of virus transmission in nature) for DENV, CHIKV, ZIKV, and YFV.

Aedes albopictus originated in Asia. Like Ae. aegypti, Ae. albopictus has migrated globally throughout the tropical, subtropical, and temperate world, primarily through international trade in used tires (Reiter and Sprenger 1987, Hawley 1988). Aedes albopictus has adapted to survive in a broader temperature range and at cooler temperatures, which enables them to persist in more temperate climates. These mosquitoes live in close proximity to people, but less so than Ae. aegypti.

Approximate distribution of Aedes aegypti and Aedes albopictus in the United States

Distribution maps of Aedes aegypti and Aedes albopictus mosquitoes in the United States. The Aedes aegypti is in the southern united states while the Aedes albopictus is mainly in the eastern half of the United States.

Life Cycle

Ae. aegypti and Ae. albopictus use natural and artificial water-holding containers (e.g., treeholes, used tires) to lay their eggs. After hatching, larvae grow and develop into pupae and subsequently into a terrestrial, flying adult mosquito. See Mosquito life cycle fact sheet.

Prevention and Control

The prevention or reduction of transmission of DENV, ZIKV, and CHIKV (there is a safe and efficacious vaccine against YFV) is completely dependent on the control of mosquito vectors and limiting person-mosquito contact. Mosquito surveillance is a key component of any local integrated vector management program. The goal of mosquito-based surveillance is to quantify human risk by determining local vector presence and abundance. The principal functions of DENV, CHIKV, and ZIKV mosquito -based surveillance programs are to:

Determine presence or absence of Ae. aegypti and Ae. albopictus in a geographic area
Identify what types of containers are producing the most mosquitoes for targeting vector control efforts
Develop detailed maps to track larval sites if Ae. aegypti or Ae. albopictus are detected in an area
Collect mosquito population data and identify geographic areas of high abundance (high-risk)
Monitor the effectiveness of vector control efforts
Collect data on mosquito infection rates during outbreaks to:
- identify primary/secondary mosquito vectors
- establish thresholds at which humans get infected

Arbovirus transmission ecology varies regionally and surveillance practices vary among programs (e.g., number and type of traps, frequency of sampling, etc.) based on available funding, resources, and trained staff. However, in order to quickly identify and mitigate a mosquito-borne disease outbreak, establishing and maintaining a local vector surveillance program is critical.

Whereas mosquito-based surveillance is the preferred method for monitoring or predicting West Nile virus outbreaks, it is not the preferred method for monitoring or predicting DENV, CHIKV, YFV, or ZIKV outbreaks. For these arboviruses, it is more efficient to detect cases in people. In the United States, dengue and chikungunya are both nationally notifiable conditions. Healthcare providers are therefore required to report any confirmed or suspect cases to local and state health departments. In turn, health departments should immediately notify state/local vector control districts or authorities. Timely identification and response to mosquito-borne disease outbreaks like dengue, chikungunya, yellow fever and Zika require constant communication between healthcare providers, local and state public health departments, and vector control specialists. Effective vector-based dengue, chikungunya, yellow fever and Zika prevention involves initiating control measures such as source reduction (container elimination) and larvicide treatments before the beginning of the mosquito season, and adult reduction measures such as adulticide treatments following detection of human arbovirus activity. Containment, a combination of procedures to prevent DENV, CHIKV, ZIKV and YFV from spreading, may be initiated whenever a suspected/confirmed imported or locally acquired case is detected. During outbreaks a combination of containment and large-scale vector control may be used to minimize vector-human contact.

Vector Surveillance and Control Recommendations

Before mosquito season

Conduct public mosquito education campaigns focusing on reducing or eliminating larval habitats for the Ae. aegypti and Ae. albopictus vectors
Conduct surveys to determine abundance, distribution, and type of containers; large numbers of containers may translate into high mosquito abundance and high risk
Initiate a community wide source reduction campaign – the goal of the campaign is to motivate the community to remove and dispose of any water holding containers
Cover, dump, modify or treat large water-holding containers with long-lasting larvicide

Beginning of mosquito season

Continue public education campaigns focusing on reducing or eliminating larval habitats for Ae. aegypti and Ae. albopictus vectors
Develop and distribute mosquito education materials about Ae. aegypti and Ae. albopictus and personal protection measures
Initiate Ae. aegypti and Ae. albopictus community-wide surveys to:
- determine presence or absence
- estimate relative abundance
- determine distribution
- develop detailed vector distribution maps
- evaluate the efficacy of source reduction and larvicide treatment
Continue/maintain community source reduction efforts.
Initiate adult sampling to identify or confirm areas of high adult mosquito abundance
Initiate preventive adult control to reduce adult populations targeting areas of high mosquito abundance
Concentrate control efforts around places with high mosquito density

Single or several suspected/confirmed imported/locally acquired cases

Begin public mosquito containment education campaigns aimed at preventing or minimizing contact between vectors and suspected or confirmed human cases, especially during the first week of illness when an infected person is viremic and can infect mosquitoes, thereby possibly triggering a local outbreak
- Educate the public to continually dispose of water holding containers to eliminate larval habitats. Or, if funding allows, host a community volunteer/waste disposal program to help facilitate removal of larval habitats.
- Treat with long-lasting larvicide any water-holding containers that cannot be dumped, covered, discarded or otherwise modified.
- Eliminate larval habitats within 100-200 yards/meters around a case’s home.
Initiate community source reduction, adult mosquito, and case containment initiatives to minimize the spread of infected mosquitoes
Educate the public about reported cases of disease and urge them to use:
- Insect repellents
- Window and door screens to prevent mosquitoes from entering the house
- Air conditioning

Adult mosquito control

Treat the outdoors within 100–200 yards/meters around a case’s home with adulticide
Provide outdoor residual and spatial insecticide treatments; repeat as necessary to reduce vector abundance
Initiate/maintain adult sampling to estimate adult mosquito abundance and evaluate effectiveness of insecticide treatments

Outbreak; clusters of suspected or confirmed cases

Divide the outbreak area into operational management areas where control measures can be effectively applied to all buildings and public areas within a few days; repeat as needed to reduce mosquito density
Conduct door-to-door inspections and mosquito control in an area-wide fashion (reach >90% coverage of the control area within a week)
Identify and treat, modify, or remove mosquito-producing containers
Organize area/community clean-up campaigns targeting disposable containers (source reduction), including large junk objects that accumulate water (broken washing machines, refrigerators, toilets) in buildings, public areas, etc.
Combine outdoor spatial or residual spraying with source reduction and larviciding (including residual spraying of container surfaces and adjacent mosquito resting areas). Don’t forget to treat storm drains, roof gutters and other often overlooked cryptic water sources

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Specimen Collection and Types of Traps

Ovitraps: Ovitraps are small metal, glass or plastic containers, usually dark in color, containing water and a substrate (wood, seed germination paper, cloth, plant gel) where female mosquitoes lay their eggs. Ovitraps can be used to detect the presence of gravid Ae. aegypti, Ae. albopictus and a wide variety of other gravid females of container Aedes mosquitoes (Fay and Eliason 1966, Mackay et al. 2013, Reiter et al., 1991). Ovitraps take advantage of the fact that gravid Ae. aegypti and Ae. albopictus females lay their eggs in artificial containers. Adequate sampling requires regular (weekly) trapping at fixed sites, representative of the habitat types, present in the community. Ovitraps should not be deployed in the field for more than a week at a time because they could become larval sites and may begin producing adult mosquitoes, however, some ovitraps are specifically designed not to produce mosquitoes (Chan et al. 1977; Barrera et al. 2013).

Ovitraps have several advantages, including being inexpensive, easily deployed, and not invasive (they can be placed outside of houses, not requiring entry into homes). A small number of ovitraps is usually enough to determine vector presence; less than 100 ovitraps can reliably estimate abundance in a large urban neighborhood (Mogi et al., 1990). Typically, one ovitrap is placed per city block. Lastly, ovitrap data is easy to analyze; it is usually expressed as the percentage of positive ovitraps (ovitraps with eggs). The mean number of eggs per ovitrap can be used to estimate adult mosquito abundance.

Interpreting ovitrap data may require caution, because ovitraps compete with naturally occurring larval habitats and the estimates from oviposition surveys may not accurately reflect the abundance of gravid females under some conditions. For example, oviposition indices may be skewed after source reduction campaigns when gravid females find fewer suitable habitats and lay larger proportions of eggs in the ovitraps confounding the evaluation of control efforts (Focks 2003). Some degree of training in microscopy may be needed for accurate egg counting especially when there is debris on the oviposition surfaces. Lastly, the collected eggs need to be hatched and reared out in the laboratory and the larvae or adults identified to species, which requires trained personnel.

Immature stage (larvae and pupae) surveys

Because of a wide variety in type, size and shapes of water-holding containers, there is no standard equipment for sampling the immature stages of container breeding mosquitoes. If the container is large enough, such as a 55 gallon barrel, a dipper or net may be used. However, the common containers are small cans, tires etc., and usually the entire contents are emptied onto a tray or a pan and the immature stages picked out using a dropper. The immature stages are usually reared out in the lab and identified to species.

Adult mosquito trapping

Ae. aegypti and Ae. albopictus are not efficiently captured by the most commonly used mosquito traps, such as the CDC miniature light trap, CDC gravid trap, or the New Jersey light trap. There are several fan-operated traps designed to capture Ae. aegypti adults, which take advantage of the propensity of this species to be attracted to dark objects (Fay 1968, Fay and Prince 1970, Freier and Francy 1991, Wilton and Kloter 1985). The Fay-Prince trap has been the most widely used, but it is heavy and bulky, making it difficult to use in sufficient numbers to obtain reliable estimates of mosquito abundance. Currently the most commonly used adult traps for Ae. aegypti and Ae. albopictus are BG Sentinel Traps, and a variety of gravid traps such the CDC-Autocidal Gravid Ovitrap (CDC-AGO) (Mackay et al. 2013, Barrera et al. 2014a, b).

The BG Sentinel Trap: The BG Sentinel Traps use a combination of attractive visual and olfactory cues. They have the advantage of being collapsible and light. BG-Sentinel traps are more effective in capturing Ae. aegypti than CDC backpack aspirators, and also collect adult females in all physiological states (Maciel-de-Freitas et al. 2006, Williams et al. 2006, Ball and Ritchie 2010). These traps are also effective for collecting Ae. albopictus (Meeraus et al. 2008, Bhalala and Arias 2009, Farajollahi et al. 2009, Obenauer et al. 2010). The efficiency of BG traps can be increased by baiting them with lures (e.g., CO2, BG-Lure®).

Gravid female traps: There are a number of recently developed traps that use similar principles of attraction as the ovitraps; that is, to attract and capture gravid females. These traps either use funnels (Gomes et al. 2007, Eiras et al. 2014) or sticky boards (Mackay et al. 2013, Chadee et al. 2010, Barrera et al. 2013) to prevent captured mosquitoes from escaping. The advantage of gravid traps is that they are considerably cheaper and easier to operate compared to BG traps.

Mechanical aspirators: Several aspirator devices may be used to collect resting mosquitoes. Collecting resting mosquitoes provides a good representation of vector population structure since un-fed, gravid, and blood-fed females (as well as males) may be collected (Service 1992). Since resting populations typically provide representative samples of the population, they will also provide more representative information on population infection rates. Handheld or backpack mechanical aspirators can be used to remove mosquitoes from natural resting harborage or artificial resting structures (e.g., wooden resting boxes, red boxes, fiber pots and other similar containers) (Service 1992). Aspirators are particularly useful for collecting Ae. aegypti indoors. The data obtained from this collecting technique provide more representative data on mosquito abundance per unit area (e.g., per house, master bedroom, etc.). Sampling indoors can be standardized such as aspirating for 15 minutes per house, etc., but frequently there are large variations in number of mosquitoes collected per house, therefore, this technique requires sampling large numbers of houses in short periods of time. (e.g., 100-200 houses per neighborhood). Due to the wide variety of resting sites and the low density of resting mosquitoes in most locations, sampling resting populations especially outdoors is difficult to standardize, labor intensive, requires trained personnel, and sufficient sample sizes are often difficult to obtain.

Landing –biting counts: This is one of the oldest and most effective, but labor-intensive techniques used to detect, capture, and quantify host-seeking daytime biting mosquito vectors such as Ae. aegypti and Ae. albopictus. However, due to potential health risks to field staff, especially in areas with ongoing arbovirus transmission, CDC does not recommend this technique. Another limitation of this collection method is the inherent variation among collectors both in attracting and collecting specimens. A tent trap has been recently developed, which can provide protection to collectors from mosquito bites (Casas-Martinez et al., 2013).

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Mosquito-Based Surveillance Indicators

Data derived from mosquito surveillance primarily estimates mosquito abundance; estimates are used to indicate levels of risk. The indices derived from those data vary in information content, ability to be compared over time and space, and association with arbovirus transmission levels and levels of human risk. The indicators that are commonly used can be broadly divided into 1) immature stage (larvae and pupae) survey indices, 2) eggs per ovitrap per week, 3) female mosquitoes per sticky gravid trap per week, and 4) adult infection rates (IR).

Immature stage survey indices

Larval surveys (Stegomyia indices): Larval surveys usually involve identifying all or most of the immature mosquitoes found in every container (or a representative sample of containers) in the target area, home(s) community, neighborhood etc. Every water-holding container is inspected and categorized as positive (contains larvae/pupae) or negative otherwise (no larvae/pupae). The second and less used method is single-larva surveys where only a single larva is identified from each container (Sheppard 1969). The container indices below are computed from survey data.

House Index (HI; percentage of houses with at least one positive container)
Container Index (CI; percentage of all containers with water that are larva/pupa positive), and
Breteau Index (BI; number of positive containers per 100 houses (Connor et al. 1923, WHO 2009)).

Mosquito thresholds for DENV, CHIKV, ZIKV and YFV transmission using larval indices should be determined by each local vector control program for each location; state or national wide thresholds should be used with caution. It was proposed that a House Index of 5% (Soper, 1967), a Container Index of 10% (Connor et al., 1923), or a Breteau Index of 5 (Brown, 1977) prevented YFV transmission, and that HI of 1% suppressed DENV transmission (Pontes et al., 2000). Such thresholds may not apply to all locations and to all arboviruses. A recent study in Taiwan reported the following container Aedes threshold values for DENV transmission: BI= 1.2, CI= 1.8%, and HI= 1% (Chang et al. 2015).

Pupal surveys: Pupal surveys (pupae per house, per person, per hectare) are based on the assumption that pupal productivity is a better estimate of the adult population than the traditional indices (HI, CI, and BI) or larval counts (Focks 2003). Pupal surveys can also identify the types of containers that produce the majority of adult mosquitoes; these data can help vector control programs identify target containers for enhanced surveillance and control (Focks and Chadee 1997, Nathan and Focks 2006). Pupal surveys usually involve sampling large numbers of houses and containers to obtain reliable estimates (Reuben et al. 1978, Barrera et al. 2006a, b). However, several methods have been developed to guide sample size requirements for pupal surveys (Alexander et al. 2006, Barrera et al. 2006a, b, Barrera 2009).

As with larval surveys, pupal surveys to determine DENV, CHIKV, ZIKV and YFV transmission thresholds (pupal abundance indices) should be determined by each local vector control program for each location. Currently there is no information on pupal indices on CHIKV and ZIKV transmission, however some models show that it takes between 0.5 and 1.5 Ae. aegypti pupae per person to sustain DENV transmission at 28˚C in a human population with 0 – 67% immunity (Focks et al. 2000).

Eggs per ovitrap per week. Although no specific threshold values have been established for each arbovirus, absence of dengue hemorrhagic fever cases in Thailand was noted when the densities of Ae. aegypti eggs per ovitrap per week was less than two (Mogi et al. 1990). Also, although using a different ovitrap, DENV transmission occurred in Taiwan when the density of eggs per house (2 ovitraps/house) was around two (Wu et al. 2013).

Female adults per sticky trap per week. Sticky gravid traps used for Ae. aegypti surveillance during a dengue outbreak in Australia indicated that a density of two or more females per trap per week was associated with dengue cases, whereas a density of less than one female per trap per week was a safe level (Ritchie et al. 2004). A recent study showed lack of local CHIKV transmission when the density of Ae. aegypti was less than two per sticky AGO trap per week in Puerto Rico (CDC, unpublished).

Adult infection rates

In the past, Ae. aegypti and Ae. albopictus surveillance has relied heavily on immature indices because until recently it has been difficult to monitor adult mosquito abundance. However, the BG Sentinel Trap and a variety of gravid traps make it possible to accurately estimate adult mosquito abundance and to track infected mosquitoes. Tracking adult infected mosquitoes may help establish entomological infection rate thresholds for human disease risk for DENV, CHIKV, ZIKV and YFV transmission similar to work performed for West Nile, St. Louis, and Eastern equine encephalitis viruses (CDC 2013). The infection indices used are the same as those used for other arboviruses: Minimum Infection Rate (MIR), Maximum Likelihood Estimates of the Infection Rate (MLE), and Vector Index (VI) (CDC 2013). However, adult mosquito infection rates cannot be used to predict outbreaks in DENV, CHIKV, ZIKV and YFV surveillance programs because of the very limited data on infection rates and prevalence of human infections. Data obtained in DENV surveillance programs show that, in some cases, an elevation in mosquito infection rates precede outbreaks or increased transmission (Chow et al. 1998, Mendez et al 2006) but not in others (Chen et al., 2010). These mixed results make it difficult to establish threshold mosquito infection rates for human infections and outbreaks for DENV. However, these studies used different mosquito collection methods and there is a chance data obtained from BG Sentinel traps and gravid traps may improve abundance and infection rate estimates, and provide timely risk assessment.

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Handling of field-collected adult mosquitoes

Because virologic surveillance relies on identifying DENV, CHIKV, ZIKV, and YFV in the collected mosquitoes through detection of viral proteins, viral RNA, or live virus, efforts should be made to handle and process the specimens in a way that minimizes exposure to conditions (e.g., heat, successive freeze-thaw cycles) that would degrade the virus. It has been shown that DENV and CHIKV RNA could be detected by RT-PCR in dead mosquitoes exposed in sticky cards or dried at ambient temperature for several weeks (Bangs et al. 2001; Mavale et al. 2012).

Optimally, a cold chain should be maintained from the time mosquitoes are removed from the traps to the time they are delivered to the processing laboratory, and through any short-term storage and processing.
Transport mosquitoes from the field in a cooler either with cold packs or on dry ice. Sort and identify the mosquitoes to species on a chill-table or tray of ice if available.
If arbovirus screening is not done immediately after mosquito identification and pooling, the pooled samples should be stored frozen, optimally at -70OC, but temperatures below freezing may suffice for short-term storage.

Mosquitoes are generally tested in pools no greater than 50 and only female mosquitoes are tested in routine arbovirus surveillance programs. Arboviruses can be detected in mosquito pools by using RT-PCR assays (Lanciotti et al. 1992, Lanciotti et al. 2007, Lanciotti et al. 2008, Laurent et al. 2007, Ummul Haninah et al. 2010, Santiago et al. 2013 Savage et al. 2015, Chow VTK et al. 1998, Shu et al. 2003, Chien et al. 2006, Santos et al. 2008, Chen et al. 2010, Balm et al. 2012, Faye et al. 2013, Dash et al. 2012).

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Limitations to mosquito-based surveillance

Currently available information on adult infection rates and larval/pupal indices may not predict risk for human infection.
Larval/pupal surveys may miss cryptic, often overlooked habitats (e.g. gutters, broken septic tanks, sprinkler heads/assemblies, storm drains, etc.) and fail to provide accurate data on the relative abundance of the vector species.
Larval/pupal indices may not correlate with adult mosquito abundance.
Developing useful thresholds requires consistent effort to assure the surveillance indices and their association to human risk is comparable over time. Mosquito surveillance and human disease incidence data collected over several transmission seasons is required to produce useful predictive indicators. However, this is challenging to obtain with only sporadic arboviral outbreaks.

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Vector control

General guidelines for the diagnosis, treatment, prevention, and control of DENV and CHIKV have been published (PAHO 2011; WHO 2009).

Control of immature stages

An important step in Ae. aegypti and Ae. albopictus control operations is identifying the types and abundance of containers producing mosquitoes and their productivity. Different containers require specific control measures that depend on the nature of the container and how it is used. There are five general types of containers producing Ae. aegypti and Ae. albopictus:

Phytotelmata (treeholes, leaf axils, etc.)
Non-essential or disposable containers (food and drink containers, tires, broken appliances)
Useful containers (water-storage vessels, potted plants and trivets, animal drinking pans, paint trays, toys, pails, septic tanks)
Cavities in structures (fence poles, bricks, uneven floors and roofs, roof gutters, air-conditioner trays)
Outdoor underground structures (storms drains, water meters, public wells, septic tanks)

Commonly used control methods

Environmental sanitation: This is the permanent elimination of containers producing Ae. aegypti and Ae. albopictus such as establishing reliable supplies of piped water, municipal refuse recycling programs (glass, metal, and plastic), used-tire recycling operations, replacing septic tanks with sewerage, etc.

Larvicides: This is the use of chemicals or biological agents to kill or prevent development of mosquito immature stages. There are a number of agents that can be used to control mosquito production in containers:

Chemical larvicides (temephos)
Biological larvicides: These include products containing Bacillus thuringiensis var. israelensis(B.t.i.), spinosad, and Insect Growth Regulators (IGR’s) such as juvenile hormone analogs (methoprene, pyriproxyfen) and chitin synthesis inhibitors (Diflubenzuron, Novaluron). Biological larvicides have little or no impact on non-target organisms and do not accumulate in the environment.
Monomolecular films and oils. These products spread on the water surface forming a thin film that causes suffocation of immature mosquitoes by preventing gas exchange.

Evaluation of the effectiveness of pre-adult mosquito control may be accomplished by comparing the presence/absence and abundance of immature stages in treated containers before and after treatment or by comparing treated and untreated areas (Chadee 2009).

Biological control: A variety of aquatic predators may be used especially in large containers. These include carnivorus copepods and larvivorous fish (Gambusia affinis). However, biological control may not be practical especially since Ae. aegypti and Ae. albopictus often develop in small containers.

Control of adult mosquitoes

Chemical control:

Chemical control of adult mosquitoes includes space spraying, residual spraying, barrier spraying, and using attractive toxic baits.
Barrier spraying of residual insecticides on external walls of houses and vegetation has been effectively used to reduce exposure to exophilic mosquito species (Anderson et al. 1991, Perich et al. 1993, Cilek 2008), including Ae. albopictus (Trout et al., 2007).
Residual insecticides are used on surfaces that adult mosquitoes frequently visit and land on, such as walls and ceilings, discarded containers, vegetation, curtains, covers for water-storage vessels, lethal ovitrap oviposition strips, etc. There is evidence that indoor residual spraying (IRS) is particularly effective for controlling Ae. aegypti (Chadee 1990) primarily due to its indoor resting behavior. However, there are concerns about continuous insecticide exposure for the residents and currently, no residual insecticides are registered in the US for widespread spraying of indoor areas to control of adult mosquitoes.
Space spraying of insecticides is carried out by backpack, truck- or air-craft mounted equipment.

Attractive toxic sugar baits have been shown to reduce adult populations of Ae. albopictus in Florida (Naranjo et al. 2013, Revay et al. 2014). Eugenol (a component of clove oil) and boric acid have been tested as toxicants in these studies. It is not clear whether these baits would work against Ae. aegypti in tropical urban areas because it has been reported that females of this species do not commonly consume sugars (Costero et al. 1998).

Using insecticide to control adult mosquitoes should always include insecticide resistance monitoring and management. Insecticide resistance has been demonstrated in almost every class of insecticide, including microbial pesticides and IGRs (Brogdon and McAllister 1998a). Insecticide resistance, which is an inheritable trait, usually leads to significant reduction in the susceptibility of insect populations which renders insecticide treatments ineffective. Insecticide resistance may be monitored using bioassays in larvae and adult mosquitoes (WHO 2009, Brogdon and McAllister 1998b[PDF - 28 pages]).

Physical control (non-insecticidal mosquito traps): Gravid female mosquitoes can be lured to traps baited with an oviposition medium and captured using sticky glue while attempting to lay eggs (CDC Autocidal Gravid Ovitrap, AGO trap; Barrera et al. 2014a, b; Mackay et al. 2013). The use of three AGO traps per home in more than 85% of houses in neighborhoods in southern Puerto Rico has shown sustained and effective reductions of Ae. aegypti populations (80%).

Personal Protection

Repellents: CDC recommends the use of products containing active ingredients which have been registered by the U.S. Environmental Protection Agency (EPA) for use as repellents applied to skin and clothing. EPA registration of repellent active ingredients indicates the materials have been reviewed and approved for efficacy and human safety when applied according to the instructions on the label. For more details go to Insect Repellent Use & Safety.

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References

Alexander N, Lenhart AE, Romero-Vivas CME, Barbazan P, Morrison AC, Barrera R, Arredondo-Jimenez JI, Focks DA. 2006. Sample sizes for identifying the key types of container occupied by dengue-vector pupae: the use of entropy in analyses of compositional data. Annals of Tropical Medicine and Parasitology 100:S5-S16.

Anderson AL, Apperson CS, Knake R. 1991. Effectiveness of mist-blower applications of malathion and permethrin to foliage as barrier sprays for salt marsh mosquitoes. Journal of the American Mosquito Control Association 7:116-117.

Ball TS, Ritchie SR. 2010. Evaluation of BG-sentinel trap trapping efficacy for Aedes aegypti (Diptera: Culicidae) in a visually competitive environment. Journal of Medical Entomology 47:657-663.

Balm MN, Lee CK, Lee HK, Chiu L, Koay ES, Tang JW. 2012. A diagnostic polymerase chain reaction assay for Zika virus. Journal of Medical Virology84(9):1501-1505.

Bangs MJ, Tan R., Listiyaningsih E., Kay BH, Porter KR. 2001. Detection of dengue viral RNA in Aedes aegypti (Diptera: Culicidae) exposed to sticky lures using reverse-Transcriptase Polymerase Chain Reaction. Journal of Medical Entomology 38:720-724.

Barrera R, Amador M, Clark GG. 2006a. Sample-size requirements for developing strategies, based on the pupal/demographic survey, for the targeted control of dengue. Annals of Tropical Medicine and Parasitology 100:S33-S43.

Barrera R, Amador M, Clark GG. 2006b. Use of the pupal survey technique for measuring Aedes aegypti (Diptera: Culicidae) productivity in Puerto Rico. American Journal of Tropical Medicine and Hygiene 74:290-302.

Barrera R. 2009. Simplified pupal surveys of Aedes aegypti (L.) for entomologic surveillance and dengue control. American Journal of Tropical Medicine and Hygiene 81:100-107.

Barrera R, Mackay AJ, Amador M. 2013. A novel autocidal ovitrap for the surveillance and control of Aedes aegypti. Journal of the American Mosquito Control Association. 29: 293-296.

Barrera R, Amador M, Acevedo V, Hemme RR, Felix G. 2014a. Sustained, area-wide control of Aedes aegypti using CDC autocidal gravid ovitraps.American Journal of Tropical Medicine and Hygiene 91:1269-1276.

Barrera R, Amador M, Acevedo V, Caban B, Felix G, Mackay A. 2014b. Use of the CDC Autocidal Gravid Ovitrap to Control and Prevent Outbreaks ofAedes aegypti (Diptera: Culicidae). Journal of Medical Entomology 51:145-154.

Bhalala H, Arias JR. 2009. The Zumba mosquito trap and BG-Sentinel trap: novel surveillance tools for host-seeking mosquitoes. Journal of the American Mosquito Control Association 25:134-139.

Brogdon WG, McAllister JC. 1998a. Insecticide resistance and vector control. Emerging Infectious Diseases 4:605-613.

Brogdon WG, McAllister JC. 1998b. Simplification of adult mosquito bioassays through use of time-mortality determinations in glass bottles. Journal of the American Mosquito Control Association 14:159-64.

Brown AWA. 1977. World wide surveillance of Aedes aegypti. Proceedings of Annual Conference California Mosquito Control Association; NY, USA,Academic Press;. p. 20-25.

Casas-Martinez M, Orozco-Bonilla A, Munoz-Reyes M, Ulloa-Garcia A, Bond JG, Valle-Mora J, Weber M, Rojas JC. 2013. A new tent trap for monitoring the daily activity of Aedes aegypti and Aedes albopictus. Journal of Vector Ecology 38:277-288.

CDC. 2013. West Nile Virus in the United States: Guidelines for Surveillance, Prevention, and Control. 2013. 4th Edition[PDF - 69 pages].

Chadee DD. 1990. Methods for evaluating Aedes aegypti populations and insecticide treatment in a town of Trinidad, West Indies. Boletin Oficina Sanitaria Panamericana 109:350-9.

Chadee DD. 2009. Impact of pre-seasonal focal treatment on population densities of the mosquito Aedes aegypti in Trinidad, West Indies: A preliminary study. Acta Tropica 109:236-240.

Chadee DD, Ritchie SA. 2010. Oviposition behaviour and parity rates of Aedes aegypti collected in sticky traps in Trinidad, West Indies. Acta Tropica116:212-216.

Chan KL, No SK, Tan KK. An autocidal ovitrap for the control and possible eradication of Aedes aegypti. Southeast Asian J Trop Med Pub Hlth. 1977; 8(1): 56-62.

Chang FS, Tseng YT, Hsu PS, Chen CD, Lian IB, Chao DY. 2015. Re-assess vector indices threshold as an early warning tool for predicting dengue epidemic in a dengue non-endemic country. PLoS Negl Trop Dis 9(9): e0004043. doi:10.1371/journal.pntd.0004043.

Chen CF, Shu PY, Teng HJ, Su CL, Wu JW, Wang JH, Lin TH, Huang JH, Wu HS. 2010. Screening of dengue virus in field-caught Aedes aegypti andAedes albopictus (Diptera: Culicidae) by one-step SYBR green-based reverse transcriptase-polymerase chain reaction assay during 2004-2007 in Southern Taiwan. Vector Borne and Zoonotic Diseases 10:1017-1025.

Chien LJ, Liao TL, Shu PY, Huang JH, Gubler DJ, Chang GJ. 2006. Development of real-time reverse transcriptase PCR assays to detect and serotype dengue viruses. Journal of Clinical Microbiology 44:1295–1304.

Chow VTK, Chan YC, Yong R, Lee KM, Lim LK, Chung YK, Lam-Phua SG, Tan BT. 1998. Monitoring of dengue viruses in field-caught Aedes aegyptiand Aedes albopictus mosquitoes by a type-specific polymerase chain reaction and cycle sequencing. American Journal of Tropical Medicine and Hygiene 58:578-586.

Cilek JE. 2008. Application of insecticides to vegetation as barriers against host-seeking mosquitoes. Journal of the American Mosquito Control Association 24:172-176.

Connor ME, Monroe WM. 1923. Stegomyia indices and their value in yellow fever control. American Journal of Tropical Medicine and Hygiene 3:9-19.

Costero A, Attardo GM, Scott TW, Edman JD. 1998. An experimental study on the detection of fructose in Aedes aegypti. Journal of the American Mosquito Control Association 14:234-242.

Dash PK, Boutonnier A, Prina E, Sharma S, Reiter P. 2012. Development of a SYBR green I based RT-PCR assay for yellow fever virus: application in assessment of YFV infection in Aedes aegypti. Virology Journal 9:27.

Eiras AE, Buhagiar TS, Ritchie SA. 2014. Development of the gravid Aedes trap for the capture of adult female container-exploiting mosquitoes (Diptera: Culicidae). Journal of Medical Entomology 51:200-209.

Farajollahi A, Kesavaraju B, Price DC, Williams GM, Healy SP, Gaugler R, Nelder MP. 2009. Field efficacy of BG-Sentinel and industry-standard traps for Aedes albopictus (Diptera: Culicidae) and West Nile virus surveillance. Journal of Medical Entomology 46:919-925.

Fay RW, Eliason DA. 1966. A preferred oviposition site as a surveillance method for Aedes aegypti. Mosquito News 26:531-535.

Fay RW. 1968. A trap based on visual responses of adult mosquitoes. Mosquito News 28:1-7.

Fay RW, Prince WH. 1970. A modified visual trap for Aedes aegypti. Mosquito News 30:20-23.

Faye O, Faye O, Diallo D, Diallo M, Weidmann M, Sall AA. 2013. Quantitative real-time PCR detection of Zika virus and evaluation with field-caught mosquitoes. Virology Journal 10:311.

Focks DA, Chadee DD. 1997. Pupal survey: An epidemiologically significant surveillance method for Aedes aegypti: An example using data from Trinidad. American Journal of Tropical Medicine and Hygiene 56:159-167.

Focks DA, Brenner RJ, Hayes J, Daniels E. 2000. Transmission thresholds for dengue in terms of Aedes aegypti pupae per person with discussion of their utility in source reduction efforts. American Journal of Tropical Medicine and Hygiene 62:11-18.

Focks DA. 2003. A Review of Entomological Sampling Methods and Indicators for Dengue Vectors. Geneva, Switzerland.

Freier JE, Francy DB. 1991. A duplex cone trap for the collection of adult Aedes albopictus. Journal of the American Mosquito Control Association7:73-79.

Gomes ADC, Da Silva NN, Bernal RTI, Leandro ADS, De Camargo NJ, Da Silva AM, Ferreira AC, Ogura LC, De Oliveira SJ, De Moura SM. 2007. Specificity of the Adultrap for capturing females of Aedes aegypti (Diptera: Culicidae). [Portuguese]. Revista da Sociedade Brasileira de Medicina Tropical 40:216-219.

Gratz NG. 2004. Critical review of the vector status of Aedes albopictus. Medical and Veterinary Entomology 18:215-27.

Hawley WA. 1988. The biology of Aedes albopictus. Journal of the American Mosquito Control Association Suppl 1:1-39.

Lanciotti RS, Calisher CH, Gubler DJ, Chang GJ, Vorndam AV. 1992. Rapid detection and typing of dengue viruses from clinical samples by using reverse transcriptase-polymerase chain reaction. Journal of Clinical Microbiology. 30:545–551

Lanciotti RS, Kosoy OL, Laven JJ, Panella AJ, Velez JO, Lambert AJ, Campbell GL. 2007. Chikungunya virus in US travelers returning from India, 2006.Emerging Infectious Diseases 13: 764–767.

Lanciotti RS, Kosoy OL, Laven JJ, Velez JO, Lambert AJ, Johnson AJ, Stanfield SM, Duffy MR. 2008. Genetic and serologic properties of zika virus associated with an epidemic, Yap State, Micronesia, 2007. 14:1232-1239.

Laurent P, Le Roux K, Grivard P, Bertil G, Naze F, Picard M, Staikowsky F, Barau G, Schuffenecker I, Michault A. 2007. Development of a sensitive real-time reverse transcriptase PCR assay with an internal control to detect and quantify chikungunya virus. Clinical Chemestry 53:1408-14.

Maciel-De-Freitas R, Eiras AE, Lourenco-De-Oliveira R. 2006. Field evaluation of effectiveness of the BG-Sentinel, a new trap for capturing adultAedes aegypti (Diptera: Culicidae). Memorias do Instituto Oswaldo Cruz 101:321-325.

Mackay A, Amador M, Barrera R. 2013. An improved autocidal gravid ovitrap for the control and surveillance of Aedes aegypti. Parasites & Vectors6:225.

Mavale M, Sudeep A, Gokhale M, Hundekar S, Parashar D, Ghodke Y, Arankalle V, Mishra AC. 2012. Short Report: Persistence of viral RNA in chikungunya virus-infected Aedes aegypti (Diptera: Culicidae) mosquitoes after prolonged storage at 28°C. American Journal of Tropical Medicine and Hygiene 86:178–180.

Meeraus WH, Armistead JS, Arias JR. 2008. Field comparison of novel and gold standard traps for collecting Aedes albopictus in Northern Virginia.Journal of the American Mosquito Control Association 24:244-248.

Mendez F, Barreto M, Arias JF, Rengifo G, Munoz J, Burbano ME, Parra B. 2006. Human and mosquito infections by dengue viruses during and after epidemics in a dengue-endemic region of Colombia. American Journal of Tropical Medicine and Hygiene 74:678-683.

Mogi M, Choochote W, Khamboonruang C, Suwanpanit P. 1990. Applicability of presence-absence and sequential sampling for ovitrap surveillance of Aedes (Diptera: Culicidae) in Chiang Mai, Northern Thailand. Journal of Medical Entomology 27:509-514.

Monath TP, Tsai TF. 1987. St. Loius Encephalitis: Lessons from the last decade. American Journal of Tropical Medicine and Hygiene 37(3) Suppl:40S–59S.

Morris CD. 1988. Eastern equine encephalomyelitis. In: Monath, TP, ed. The Arboviruses: Epidemiology and Ecology. Boca Raton, FL: CRC Press: 1–20.

Naranjo D, Qualls W, Mueller G, Samson D, Roque D, Mã¼Ller G, Alimi T, Arheart K, Beier J, Xue R-D. 2013. Evaluation of boric acid sugar baits against Aedes albopictus (Diptera: Culicidae) in tropical environments. Parasitology research 112:1583-1587.

Nathan MB, Focks DA. 2006. Pupal/demographic surveys to inform dengue-vector control. Annals of Tropical Medicine and Parasitology 100:S1-S3.

Obenauer PJ, Allan SA, Kaufman PE. 2010. Aedes albopictus (Diptera: Culicidae) oviposition response to organic infusions from common flora of suburban Florida. Journal of Vector Ecology 35:301-306.

Pan American Health Organization. 2011. Preparedness and response for chikungunya virus introduction in the Americas.

Perich MJ, Tidwell MA, Dobson SE, Sardelis MR, Zaglul A, Williams DC. 1993. Barrier spraying to control the malaria vector Anopheles albimanus: laboratory and field evaluation in the Dominican Republic. Medical and Veterinary Entomology 7:363-368.

Pontes RJS, Freeman J, Oliveira-Lima JW, Hodgson JC, Spielman A. 2000. Vector densities that potentiate Dengue outbreaks in a Brazilian city.American Journal of Tropical Medicine and Hygiene 62:378-383.

Powell JR, Tabachnick WJ. 2013. History of domestication and spread of Aedes aegypti--a review. Memórias do Instituto Oswaldo Cruz Suppl 1:11-17.

Reiter P, Sprenger D. 1987. The used tire trade: a mechanism for the worldwide dispersal of container breeding mosquitoes. Journal of the American Mosquito Control Association 3:494-501.

Reiter P, Amador MA, Colon N. 1991. Enhancement of the CDC ovitrap with hay infusions for daily monitoring of Aedes aegypti populations. Journal of the American Mosquito Control Association 7:52-55.

Reuben R, Das PK, Samuel GD, Brooks GD. 1978. Estimation of daily emergence of Aedes aegypti (Diptera: Culicidae) in Sonepat, India. Journal of Medical Entomology 14:705-714.

Revay E, Mueller G, Qualls W, Kline D, Naranjo D, Müller G, Arheart K, Kravchenko V, Yefremova Z, Hausmann A, Beier J, Schlein Y, Xue R-D. 2014. Control of Aedes albopictus with attractive toxic sugar baits (ATSB) and potential impact on non-target organisms in St. Augustine, Florida.Parasitology Research 113:73-79.

Ritchie SA, Long S, Smith G, Pyke A, Knox TB. 2004. Entomological investigations in a focus of dengue transmission in Cairns, Queensland, Australia, by using the sticky ovitraps. Journal of Medical Entomology 41:1-4.

Service MW. 1992. Importance of ecology in Aedes aegypti control. Southeast Asian Journal of Tropical Medicine and Public Health 23:681-90.

Santiago GA, Vergne E, Quiles Y, Cosme J, Vazquez J, Medina JF, Medina F, Colon C, Margolis H, Munoz-Jordan JL. 2013. Analytical and clinical performance of the CDC real time RT-PCR assay for detection and typing of dengue virus. PLoS Neglected Tropical Diseases 7:e2311.

Santos HWGd, Poloni TRRS, Souza KP, et al. 2008. A simple one-step real-time RT-PCR for diagnosis of dengue virus infection. Journal of Medical Virology 80:1426–1433.

Savage HM, Ledermann JP, Yug L, Burkhalter KL, Marfel M, Hancock WT. 2015. Incrimination of Aedes (Stegomyia) hensilli Farner as an epidemic vector of Chikungunya virus on Yap Island, Federated States of Micronesia, 2013. Am J Trop Med Hyg 92:429-436.

Sheppard PM, Macdonald WW, Tonn RJ. 1969. A new method of measuring the relative prevalence of Aedes aegypti. Bulletin of the World Health Organization (WHO) 40:467-468.

Shu, PY, Chang, SF, Kuo, YC, Yueh, YY, et al. 2003. Development of group- and serotype-specific one-step SYBR Green I-based real-time reverse transcription-PCR assay for dengue virus. Journal of Clinical Microbiology 41:2408–2416.

Soper FL. 1967. Aedes aegypti and yellow fever. Bulletin of the World Health Organization 36:521-527.

Staples JE, Breiman RF, Powers AM. 2009. Chikungunya fever: an epidemiological review of a re-emerging infectious disease. Clinical Infectious Diseases 49:942-948.

Trout RT, Brown GC, Potter MF, Hubbard JL. 2007. Efficacy of two pyrethroid insecticides applied as barrier treatments for managing mosquito (Diptera: Culicidae) populations in suburban residential properties. Journal of Medical Entomology 44:470-477.

Ummul Haninah A, Vasan SS, Ravindran T, Chandru A, Lee HL, Shamala Devi S. 2010. Development and evaluation of a one-step SYBR-Green I-based real-time RT-PCR assay for the detection and quantification of
Chikungunya virus in human, monkey and mosquito samples. Tropical Biomedicine 27:611-623.

Williams CR, Long SA, Russell RC, Ritchie SA. 2006. Field efficacy of the BG-Sentinel compared with CDC Backpack Aspirators and CO2-baited EVS traps for collection of adult Aedes aegypti in Cairns, Queensland, Australia. Journal of the American Mosquito Control Association 22:296-300.

Wilton DP, Kloter KO. 1985. Preliminary evaluation of a black cylinder suction trap for Aedes aegypti and Culex quinquefasciatus (Diptera: Culicidae). Journal of Medical Entomology 22:113-114.

Wu HH, Wang CY, Teng HJ, Lin C, Lu LC, Jian SW, et al. 2013. A dengue vector surveillance by human population-stratified ovitrap survey for Aedes(Diptera: Culicidae) adult and egg collections in high dengue-risk areas of Taiwan. Journal of Medical Entomology 50:261-269.

World Health Organization. 2009. Dengue guidelines for diagnosis, treatment, prevention and control : new edition. Geneva: World Health Organization.

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