Vol. 7, No. 1, January–February 2001 Emerging Infectious Diseases 17

Perspectives

Vector-borne diseases (including a number

that are mosquito-borne) are a major public

health problem internationally. In the United

States, dengue and malaria are frequently

brought back from tropical and subtropical

countries by travelers or migrant laborers, and

autochthonous transmission of malaria and

dengue occasionally occurs. In 1998, 90 confirmed cases of dengue and 1,611 cases of malaria

were reported in the USA (1) and dengue

transmission has occurred in Texas (2). Other

vector-borne diseases continue to pose a public

health threat. Even though the reported

incidence of most of these diseases is low (in 1997,

10 cases of eastern equine encephalitis, 115 of

LaCrosse, and 14 of St. Louis encephalitis [SLE]),

occasional epidemics, e.g., of SLE (1,967 cases in

1975 and 247 cases in 1990, mostly in Florida [3])

have resulted in aerial applications of insecticides, primarily malathion. In addition, new

vector-borne threats continue to emerge. In 1999,

West Nile virus, an Old World flavivirus related

to Saint Louis encephalitis virus, was first

recorded in New York (4). The virus, which is

transmitted by anthropophilic mosquitoes, caused

a serious outbreak (62 cases, 7 deaths) and

signaled the potential for similar outbreaks in

the Western Hemisphere. Pesticides, which

traditionally have been used in response to

epidemics, have a role in public health as part of

sustainable integrated mosquito management

for the prevention of vector-borne diseases. We

assess the future use of pesticides in view of

existing niche markets, incentives for new

product development, Environment Protection

Agency (EPA) registration, the Food Quality

Protection Act (FQPA), and improved pest

management strategies for mosquito control.

Sustainable Integrated Mosquito

Management and Public Health

Mosquito control in the United States has

evolved from reliance on insecticide application

for control of adult mosquitoes (adulticide) to

integrated pest management programs that

include surveillance, source reduction, larvicide,

and biological control, as well as public relations

and education. The major principles of integrated

mosquito management are available at a new

Public Health Pest Control Manual internet

website (5). Adulticides still play a vital role when

flooding causes extreme numbers of nuisance

mosquitoes or when outbreaks of diseases such

as SLE occur.

Surveillance programs track diseases harbored by wild birds and sentinel chicken flocks;

vector-borne pathogens in mosquitoes; adult and

larval mosquitoes and larval habitats (by aerial

photographs, topographic maps); mosquito traps;

biting counts; and follow-up on complaints and

reports by the public. When established mosquito

larval and adult threshold populations are

Pesticides and Public Health:

Integrated Methods of

Mosquito Management

Robert I. Rose

U.S. Environmental Protection Agency, Washington, DC, USA

Address for correspondence: Robert I. Rose, USDA, APHIS,

PPQ, Unit 147, 4700 River Road, Riverdale, MD 20737, USA;

fax: 301-734-8669; e-mail: Bob.I.Rose@usda.gov.

Pesticides have a role in public health as part of sustainable integrated mosquito

management. Other components of such management include surveillance, source

reduction or prevention, biological control, repellents, traps, and pesticide-resistance

management. We assess the future use of mosquito control pesticides in view of niche

markets, incentives for new product development, Environmental Protection Agency

registration, the Food Quality Protection Act, and improved pest management strategies

for mosquito control.
Emerging Infectious Diseases Vol. 7, No. 1, January–February 2001 18

Perspectives

exceeded, control activities are initiated. Seasonal records are kept in concurrence with

weather data to predict seasonal mosquito larval

occurrence and adult flights.

Source reduction consists of elimination of

larval habitats or rendering of such habitats

unsuitable for larval development. Public

education is an important component of source

reduction. Many county or state mosquito control

agencies have public school education programs

that teach children what they and their families

can do to prevent mosquito proliferation. Other

forms of source reduction include open marsh

water management, in which mosquito-producing areas on the marsh are connected by shallow

ditches to deep water habitats to allow drainage

or fish access; and rotational impoundment

management, in which the marsh is minimally

flooded during summer but is flap-gated to

reintegrate impoundments to the estuary for the

rest of the year.

Biological control includes use of many

predators (dragonfly nymphs and other indigenous aquatic invertebrate predators such as

Toxorhynchites spp. predacious mosquitoes) that

eatlarvae and pupae; however, the most commonly

used biological control adjuncts are mosquito fish,

Gambusia affinis and G. holbrooki. Naturally

occurring Fundulus spp. and possibly Rivulus spp.,

killifish, also play an important role in mosquito

control in open marsh water management and

rotational impoundment management. Like

many fish, mosquito fish are indiscriminate

feeders that may eat tadpoles, zooplankton,

aquatic insects, and other fish eggs and fry (6).

However, since they are easily reared, they have

become the most common supplemental biological control agent used in mosquito control. The

entomopathogenic fungus, Laginidium giganteum, has been registered for mosquito control by

EPA under the trade name Liginex, but products

have not become readily available. The pathogenic protozoon, Nosema algerae, has also not

become available for technical reasons. Entomoparasitic nematodes such as Romanomermis

culicivorax and R. iyengari are effective and do

not require EPA registration but are not easily

produced and have storage viability limitations. A

predacious copepod, Mesocyclops longisetus, preys

on mosquito larvae and is a candidate for local

rearing with Paramecium spp. for food.

Mosquito traps (such as the New Jersey and

the Centers for Disease Control and Prevention

designs) have been used for monitoring mosquito

populations for years. New designs using

mechanical control to capture adult mosquitoes

have now become available. These designs use

compressed carbon dioxide, burning propane,

and octenol to attract mosquitoes and fans to

control air flow. The new technology is expensive:

these traps may cost well over $1,000 each.

Electric high-voltage insect traps (“bug zappers”)

with “black” or ultraviolet light sources do not

provide satisfactory adult mosquito control and

kill insects indiscriminately.

Pesticides

Pesticides used by state or local agencies to

control nuisance or public health pests have

warning labels and directions to minimize risks

to human health and the environment. These

pesticides are applied by public health employees

who are specifically trained to follow proper

safety precautions and directions for use. State or

local mosquito control programs are funded by

taxes and subject to public scrutiny. The

environmental hazards precautionary statements on many mosquito insecticide labels state

that insecticides are toxic to birds, fish, wildlife,

aquatic invertebrates, and honeybees. Because of

the low rates of application used to control

mosquitoes and the special public health pest

control training of most applicators, hazard to

nontargeted organisms is limited. However,

honeybees may be killed if exposed when

foraging, so proper precautions are warranted.

Human exposure in residential areas is also

uncommon because of the very low application

rates, ultra low-volume methods (ULV), treatment at night when people are indoors, pesticide

applicator training, and public prenotification

before application. Pesticide applicators who

mix, load, and apply the concentrated insecticides use personal protective equipment to avoid

exposure and closed systems to pump insecticides from storage to spray equipment.

The Federal Food Drug and Cosmetic Act

(FFDCA) 21 USC 9§406 is the regulation that

limits the quantity of any poisonous or

deleterious substance added to food. A pesticide

residue is the pesticide or its metabolites in or on

raw agricultural commodities or processed food

and feed. A tolerance is the maximum limit of a

pesticide residue considered safe. Tolerances are

relevant to adult mosquito control because wind

drift may carry the pesticide over agricultural
Vol. 7, No. 1, January–February 2001 Emerging Infectious Diseases 19

Perspectives

Table. Pesticides used for mosquito control in the United States

Name Trade name Formulation Application Advantage Limitation

Temephos Abate G, EC Larvae Usually lowest Nontarget

 cost effects, some

 resistance

Methoprene Altosid G, B, P, LC Larvae Residual Cannot be

 briquets, non- certain of per-

 target safety formance until

 too late to

 retreat

Oils BVA, Oil Larvae, pupae Acts on pupae Oil film, subsur-

 Golden Bear face larvae

Monomolecular film Agnique Liquid Larvae, pupae Acts on pupae Subsurface larvae

Bacillus thuringiensis Aquabac, WDG, AS, Larvae Nontarget Short window of

 israelensis (Bti) Bactimos, P,G,B safety, treatment

LarvX, Briquets con- opportunity.

Teknar, trol 30+ days pupae

Dunks

Bacillus sphaericus VectoLex G, WDG Larvae Nontarget Pupae, only

 (Bs) safety works in fresh

 water

Malathion Fyfanon, ULV, Adults Tolerances OP, some

Atrapa, thermal fog resistance

Prentox

Naled Dibrom, ULV, EC, Adults Tolerances OP, corrosive

Trumpet thermal fog

Fenthion Batex ULV Adults None specified OP, Florida

 only, RUP,

 tolerances

Permethrin Permanone, ULV, Adults, Low vertebrate None specified

AquaResilin, thermal fog, clothing treat- toxicity

Biomist, clothing ment for ticks

Mosquito- treatment and mosquitoes

 Beater

Resmethrin Scourge ULV, Adults Low vertebrate RUP, no

thermal fog toxicity tolerance for

 residue on crops

Sumithrin Anvil ULV, Adults Low vertebrate No tolerance

thermal fog toxicity

Pyrethrins Pyrenone, ULV, EC Adults, larvae Natural May be costly

Pyronyl pyrethrum,

 tolerances

AS = Aqueous Suspension; B = Briquets; EC = Emulsifiable Concentrate; G = Granules; LC = Liquid Concentrate; P = Pellets;

ULV = Ultra Low Volume; WDG = Water-Dispersible Granule; OP = Organophospate insecticide; RUP = Restricted Use

Product

crops where residues subject to legal tolerance

requirements may occur. Crop tolerances are

listed in the Code of Federal Regulations (7).

 Larvicides

Detection of large numbers of immature

mosquitoes in areas where source reduction or

biological control is not feasible may require

larvicide treatment to prevent the emergence of

adult mosquitoes. Use of larvicides is less

controversial than use of adulticides, although

use of larvicides may lead to public concern about

their effects on untargeted beneficial aquatic

arthropods and vertebrates (Table).

Adulticides

Effective sustainable integrated mosquito

management programs strive to prevent large
Emerging Infectious Diseases Vol. 7, No. 1, January–February 2001 20

Perspectives

flights or swarms of mosquitoes through all the

measures described above, but heavy precipitation, flooding, high tides, environmental constraints, inaccessible larval habitats, missed

breeding sites, human disease outbreaks, as well

as budget shortfalls, absent employees, or

equipment failures, may necessitate use of

adulticides (Table). Some local mosquito control

programs would use an integrated program if

they had adequate resources, but may be so

limited in funding and personnel that adulticiding

trucks are the only means of mosquito

intervention.

Effective adult mosquito control with insecticides requires small droplets that drift through

areas where mosquitoes are flying. The droplets

that impinge on mosquitoes provide the contact

activity necessary to kill them. Large droplets

that settle on the ground or vegetation without

contacting mosquitoes waste material and may

cause undesirable effects on nontargeted organisms. To achieve small droplets, special aerial

and ground application ULV equipment is used.

Insecticides are applied in a concentrated form or

technical grade and at very low volumes such as 1

oz (29.6 mL) per acre. Typically, aerial

applications produce spray droplets of 30 to

50 microns measured as mass median diameter,

with <2.5% of the droplets exceeding 100

microns. Ground ULV applicators produce

droplets of 8 to 30 microns, with none >50

microns mass median diameter. Large droplets

of malathion, naled, and fenthion in excess of 50

to 100 microns can damage automotive or similar

paint finishes.

Adulticide applications, particularly aerial

applications and thermal fogging, are quite

visible and contribute to public apprehension.

Ground ULV application may be less alarming

than aerial application but is not effective over

large or inaccessible areas. Preferable air

currents for ground applications are 3.2 kph to

12.9 kph and not in excess of 16.1 kph. Excessive

wind and updrafts reduce control, but light wind

is necessary for drifting spray droplets. With

insecticide application by air using high-pressure

pumps of 2,500 lbs psi, special nozzles, proper

aerial application altitude and wind drift,

mosquito control is achievable for several miles

downwind with minimal spray deposit below the

aircraft, as a result of improved atomization of

the insecticide. This technology is being

developed and needs validation under different

conditions with different mosquito species before

it can be universally used. Thermal fogging,

which was commonly used before ULV applications became prevalent, continues to be used in a

few areas in the United States and is still widely

used in other countries. The insecticide is diluted

with petroleum oil and vaporized with heat into a

dense, highly visible fog of very small uniform

droplets, which allows tracking the plume

downwind to target areas. Although this fog

reduces visibility, it may also penetrate

vegetation better than a ULV application. Small

electric or propane thermal foggers are available

for consumer use in retail stores at a cost of

approximately $60.00.

Adult mosquitoes are easily controlled with

insecticides applied at extremely low rates. For

example, malathion is applied at 3 fl oz per acre

(219.8 mL/ha) for mosquitoes, while the rate for

agriculture is as much as 16 fl oz per acre (1,172

mL/ha).

 Insecticide Resistance

Vector resistance to certain larvicides and

adulticides has occurred periodically. Failure of

mosquito control indicating resistance must be

verified by laboratory analysis or use of test kits

because other factors (improper equipment

calibration, dilution, timing and other application errors, off-specification products, climatic

factors) can prevent insecticides from providing

satisfactory control in the field. Resistance may

occur between insecticides within a class or could

be passed from immature to adult stages subject

to the same insecticidal mode of action.

Additionally, different species of mosquitoes may

inherently vary in susceptibility to different

larvicides and adulticides. Insecticides with

different modes of action can be alternated to

prevent resistance. Even though source reduction and use of predators such as larvivorous fish

are also used for sustainable integrated mosquito

management, only two chemical classes of

adulticides (organophosphates and pyrethroids)

with different modes of action are available.

Biological controls (including birds and bats) may

be present, but often not in sufficient numbers to

provide satisfactory alternative control, particularly in coastal areas where salt-marsh mosquitoes are abundant or when human disease

outbreaks occur. Therefore, sustained integrated

mosquito management requires alternative use

of different classes of insecticides, in conjunction
Vol. 7, No. 1, January–February 2001 Emerging Infectious Diseases 21

Perspectives

with resistance monitoring, source reduction,

biological control, and public education.

 Repellents

Insect repellents, primarily N,N-diethylmetatoluamide (DEET), are used to prevent

nuisance bites from mosquitoes (as well as ticks,

biting flies, and mites) and may aid in lowering

disease transmission from these pests. However,

they should not be relied upon to prevent disease

transmission, particularly where Lyme disease

or encephalitis are endemic or malaria, yellow

fever, or other vector-borne diseases are

prevalent. Repellents, mosquito coils, and

permethrin clothing treatment products are

subject to EPA pesticide registration performance requirements (8). Information on safe use

of repellents is located at the EPA Office of

Pesticide Programs website (9). Citronella and its

oil for mosquitoes and 30 other active ingredients

are exempted from EPA pesticide registration

(10). However, some of these products may not be

efficacious.

Future of Public Health Pesticides

The past decade has seen a sharp rise in

public apprehension concerning the use of

pesticides, although state and federal regulations are well established for the assessment and

mitigation of their human and environmental

risks. Response to public concern over safety of

pesticides prompted the FQPA, which includes

provisions to protect availability of public health

pesticides. However, public health pesticides are

in jeopardy for the following reasons: In the

United States, mosquito control programs are

often for nuisance rather than disease vector

control and not many insecticides are registered

for this use. None of the mosquito adulticides

commonly used were developed recently; their

registrations are up to 44 years old. Mosquito

control is only a niche market compared with

agricultural pest control, which includes pesticides for use on corn, soybeans, and cotton, as

well as the high-profit home, garden, and

structural pest control markets. As pesticide

companies have merged to form multinational

conglomerates, the most profitable markets are

those that drive corporate decisions. At present,

it may require $50 million or more to develop and

register a new pesticide with EPA. Furthermore,

several years of the patent life elapse before costs

are recouped and profits accrue.

Vector control uses of existing pesticides,

particularly adulticides, often follow agricultural

registration and commercialization as a means of

expanding sales into new markets. Performance

data are not usually required for registration of

agricultural pesticides, but these data are

required for registration of public health

pesticides. For mosquito control, these data are

often obtained under an experimental use

permit, which requires application to EPA,

submission or reference to a portion of the

pesticide registration requirements according to

CFR 40 § 158 Data Requirements for Registration and Reporting (7,8). Testing for mosquito

adulticides or larvicides is typically done by

universities and mosquito control or abatement

districts, although it may be done by companies

or state or federal research organizations, such as

the Department of Defense or the U.S.

Department of Agriculture. In addition to

defining dose rates, formulations, environmental

variables, and effects that must be accommodated, testing under an experimental use permit

provides a means of market introduction through

user and customer experience, presentations at

professional society meetings, and journal

publications.

Pesticide marketing often involves distributors or dealers who specialize in the market if the

manufacturers do not deal directly. Profit

margins that add to price are required by

distribution chains. Public agencies solicit

competitive bids for pesticides, which squeeze

margins further, thus affecting marketing

incentives. Mosquito adulticides are used at very

low rates of active ingredient per acre, which

limits sales volumes and margins. Some seasons

have few mosquitoes, so sales are low. Product

liability also plays an important role in reducing

incentives because of possible personal and classaction lawsuits or court injunctions against

pesticides applied over populated areas.

The Federal Insecticide, Fungicide,

and Rodenticide Act and FQPA

The Federal Insecticide, Fungicide, and

Rodenticide Act 7 USC 136 and FFDCA were

amended by the FQPA of 1996. Amendments

pertinent to mosquito nuisance and vector

control include the following: review of a

pesticide’s registration every 15 years; expediting minor use registrations; special provisions for

public health pesticides; aggregate (all modes of
Emerging Infectious Diseases Vol. 7, No. 1, January–February 2001 22

Perspectives

exposure from a single pesticide) and cumulative

(all pesticides with the same mode of action) risk

assessments; an additional safety factor of up to

10 X for children; collection of pesticide use

information; and integrated pest management.

Special provisions for public health pesticides

include the following: risks and benefits

considered separately from those of other

pesticides; exemption from fees under certain

circumstances; development and implementation of programs to control public health pests;

Department of Health and Human Services

(DHHS)-supported studies required for

reregistration when needed; and appropriations

of $12 million for the first year after enactment

and similar funding as needed in succeeding

years to carry out public health pesticide

provisions of the Act. The Act describes a

consultation process between EPA and DHHS

before any public health pesticide registration is

suspended or canceled and allows additional time

for submission of data. The first group of

pesticides under review are the organophosphate

cholinesterase inhibitors, including temephos,

fenthion, naled, chlorpyrifos, and malathion.

Should risk assessments result in detection of

risk of concern to the Agency, cancellation or

mitigations of use may follow, as exemplified by

recent chlorpyrifos and diazinon use cancellations. Risk assessments may be based on data

from acute and chronic toxicology and exposure

studies, models that simulate exposure scenarios, reports of adverse incidents to humans

and wildlife, extrapolation, maximum label use

rate assumption, and worst-case exposure

scenarios.

Even though the FQPA provisions were

intended by Congress to ensure that existing

public health pesticide uses are not lost without

economically effective alternatives, the provisions may not be adequate. If FQPA results in

cancellation of major agricultural uses of a

pesticide that is also used in public health, it may

become no longer profitable for the manufacturer

to produce small quantities for mosquito control,

thus ending production of the pesticide. Since

adulticides used for mosquito control were

registered decades ago, the data supporting their

registrations may be insufficient to meet current

requirements. The substantial cost involved in

updating the data required for reregistration will

have to be paid by pesticide registrants or the

Federal government though the authorized and

appropriated funding in FQPA. Data to support

reregistration done at public expense are not

proprietary. Registrants need proprietary data to

protect their market shares from generic

pesticide competition from overseas manufacturers that can use public data to support their own

registrations; therefore, they may not consider

requesting public funds to pay for new data to

support existing registrations. However, if

generic safety studies applicable to several public

health pesticides are required by EPA for all

reregistrations, the data could be generated by a

task force of registrants and county, state, and

Federal public health agencies, which would then

request public funding under the provisions of

the Act.

Although the development of new mosquito

insecticides, particularly adulticides, is not

expected to accelerate in the near future,

integrated pest management tools and techniques should improve as a result of FQPA

funding and the need to control continued vectorborne disease outbreaks. Integrated pest management tools have strengths and weaknesses,

and continued availability of adulticides is

critical. Therefore, implementation of the public

health pesticide provisions of FQPA must include

substantial comparative risk-benefit analyses of

the significance of vector-borne disease impacts

versus potential human and environmental toxic

effects of pesticides used to control public health

pests, both in the USA and other countries

affected by EPA pesticide regulatory decisions.

Public information and legislative campaigns

have also become necessary to preserve the

availability and use of pesticides for disease

vector control as FQPA has been implemented

and with the concurrent spread of West Nile

virus.

Dr. Rose is an arthropod biotechnologist with the

Animal and Plant Health Inspection Service of the U.S.

Department of Agriculture.

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RM, Clark GG, Tabony LJ, Patterson MA. Dengue

surveillance in Texas, 1995. Am J Trop Med Hyg

1998;59:95-9.
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