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Chapter 4

Public Health Pesticides


Robert J. Novak1 and Richard L. Lampman2
1
University of Alabama at Birmingham, Birmingham, Alabama
2
Illinois Natural History Survey, Champaign, Illinois

4.1 Introduction economically acceptable levels using a variety of long-


term and short-term interventions that are environmentally
The spectacular success with synthetic insecticides in the and socially sound. With the advent of IPM, it is no longer
decade immediately following World War II generated wide- proper to discuss the use of pesticides without including
spread enthusiasm that the major scourges of mankind, such the context in which they are to be used and their potential
as yellow fever, malaria, and typhus, could be conquered. detrimental side effects (WHO, 1995). However, pesti-
From 1955 to 1969, the World Health Organization (WHO) cides remain a critical component of vector management
Global Malaria Eradication Program eliminated malaria programs because they provide a rapid and highly effica-
from 36 countries, primarily by spraying inside human habi- cious means of reducing arthropod populations, particu-
tats with a relatively inexpensive residual insecticide, DDT larly when the potential for disease transmission is high. In
(Metcalf and Novak, 1994). The annual number of malaria developing countries, approximately 10% of total pesticide
cases in India was reduced from 75 million to 150,000 and use is for vector management (Leng, 1999). In the United
deaths from 750,000 to 1500 during the period from 1952 to States, it has been estimated that $150 million is spent on
1966, largely due to the use of organochlorine insecticides vector control and surveillance for arboviral encephalitides
(Metcalf, 1998). Unfortunately, by the late 1960s, govern- (see http://www.cdc.gov/ncidod/dvbid/Arbor/arbofact.htm).
ments throughout the world were forced to reevaluate vec- To provide a general review of public health pesticides,
tor and pest control techniques. In addition to insecticide we briefly cover the following topics: (1) common terms
resistance, there was a precipitous decline in beneficial and concepts in medical entomology in order to introduce
insect species, outbreaks of secondary pests, contamina- the diverse relationships among humans, arthropods, and
tion of the environment and foodstuffs, and bioaccumula- disease pathogens; (2) the historical and current impact of
tion of pesticide residues in nontarget organisms, including arthropods on human health; (3) the basic concepts of vector
humans (Brogdon and McAllister, 1998; Brown et al., 1976; management; (4) a brief list of noninsecticidal alternatives;
National Academy of Sciences, 1980; WHO, 1972, 1992). (5) the classification schemes and general properties of pub-
Furthermore, once malaria seemed to be under control, there lic health pesticides and repellents; and (6) specific examples
was a loss of trained vector control specialists in some coun- of pesticides in vector management, particularly mosquito
tries, and in other countries pathogens started to develop control. Our approach to vector management is analogous
resistance to antimalarials (Gubler, 1996, 1998). The esca- to that of modern medicine. Vector control specialists should
lating problems with agricultural pests and public health have the same degree of understanding about insecticides
vectors sparked a conceptual change in insect control, which and acaricides as a physician has for prescription drugs. The
shifted from an almost exclusive reliance on insecticides to impact of these chemicals on wellness of a human body or
a blend of cultural, physical, biological, and chemical meth- an ecosystem has to be addressed before and after treatment.
ods (Curtis, 2001; Luckmann and Metcalf, 1994; WHO, The prevailing doctrine should be “Do no harm.”
1995). Thus, currently the goal of WHO is disease manage-
ment through a combination of site-specific integrated pest
management (IPM) techniques in coordination with medi- 4.2 Definition of terms in
cal diagnosis, treatment, and epidemiological trend analysis vector-borne diseases
(see http://www.who.int/health-topics/malaria/en).
In general, IPM is an applied ecological approach to The science that deals with the impact of arthropods on
curtailing the damage of injurious plants and animals to humans is typically called medical entomology, despite

Hayes’ Handbook of Pesticide Toxicology


Copyright © 2010 Elsevier Inc. All rights reserved 231
232 Hayes’ Handbook of Pesticide Toxicology

the fact that noninsect species such as ticks, mites, and spi- head and pubic lice, horse flies and deer flies, stable flies,
ders are generally included. The interaction of humans and mosquitoes, ticks, and various species of ants, bees, cater-
arthropod pests can be categorized into direct and indirect pillars, and wasps.
effects (Harwood and James, 1979). Direct effects are phys- Indirect effects are those where arthropods serve as car-
ical, physiological, or psychological responses of humans riers (vectors) of etiological agents (pathogens) to humans
to the actions or the presence of arthropods. Direct effects and animals (hosts). The pathogen transfer may be by
include blood loss, ectoparasitic skin irritations (dermatitis), mechanical transmission, carried on the outside of the
allergic reactions, envenomization, urticating hairs of cat- arthropod, or by biological transmission, carried internally
erpillars, invasion of tissues and organs as with endoparasites and typically transmitted through some arthropod product
(such as myiasis with dipterans), and a wide range of such as salivary secretions or feces. In biological trans-
mental disturbances that range from prevention of normal mission, the pathogen may undergo partial or complete
activities to delusional parasitosis (Table 4.1). Common development, as well as multiplication, within the vector.
arthropods that cause direct effects include cockroaches, The principal vectors worldwide are flies and mosquitoes
bedbugs, blister beetles, spiders, scabies and chigger mites, (Diptera), ticks (Acarina), fleas (Siphonaptera), sucking

Table 4.1 Examples of Arthropods by Order and Family That Cause Indirect Annoyances to Humans and Animals
through Venoms and Toxins, Allergens, and Pests
Blood loss—prevention of normal activities
Culicidae (mosquitoes): Aedes vexans, Ae. sollicitans, Ae. dorsalis, Culex tarsalis, Psorophora columbiae
Simuliidae (black flies): Simulium vittatum, S. venustrum, Prosimulium hirtipes
Ceratopogonidae (no-see-ums): Culicoides canithorax, C. melleus, C. furens, C. obsoletus
Muscidae: Stomoxys (stable flies): Stomoxys calcitrans, S. irritans
Tabanidae (deer and horse flies): Chrysops sp., Tabanus sp.
Cimicidae (bedbugs): Cimex lectularis
Ixodidae (hard ticks): Dermacentor andersoni, D. variabilis, Rhipicephalis sanguineus
Dermatosis/dermatitis (skin irritations)
Pediculidae (head and pubic lice): Pediculis humanis capitus, Phthirus pubis
Sarcoptidae (scabies mites): Sarcoptes scabiei, Sarcoptes sp.
Trombiculidae (chigger mites): Trombicula autumnalis, T. alfreddugesi, T. splendens
Occupational mites: Pyemotis tritici, Tyrophagusputrescentiae, Glycyphagus domesticus
Liparidae (tussock moth)
Meloidae (blister beetles) and Oedemeridae (false blister beetle)
Invasion of tissues and organs
Flies (myiasis), beetles, and other insects
Hippoboscidae (louse flies): Melophagus ovinus
Muscidae (house, horn, stable flies): Haematobia irritans
Oestridae (bot flies): Gastrophilus equi, G. intestinalis, Hypoderma lineatum
Calliphoridae (blue bottle flies): Cochliomyia hominivorax (screw worm)
Envenomization, bites, and urticating hairs (wasps, ants, bees, spiders, caterpillars, stings, bites, localized reactions)
Apidiae (honeybees, bumblebees): Apis mellifera, Apis mellifera scutellata
Vespidae (wasp, yellow jackets, hornets): Vespula sp., Dolichovespula sp.
Mutillidae (velvet ants): Ephuta, Photomorphus, Pseudomethoca, Sphaeropthalma, and Timulla sp.
Formicidae (ants): Solenopsis sp. (fire ants), Camponotus sp. (carpenter ants), Formica sp. (wood ants)
Lepidoptera (caterpillars or larvae, urticating hairs)
Chapter | 4 Public Health Pesticides 233

Table 4.1 (Continued)


Saturniidae: Hemileuca oliviae, Automeris sp. (Io moths)
Lymantriidae: Nygmia phaeorrhoes (brown-tailed moth)
Megalopygidae (flannel moths): Megalopyge lanata
Arctiidae: Lithosa caniola, Arctia caja, Euchaetias egle
Nymphalidae: Nymphalis antiopa
Noctuidae: Acronicta lepusculina, A. oblinita, Catocala sp.
Thysanoptera (thrips): Thrips tabaci, Chirothrips aculeatus, Heliothrips jumipennis, H. sudanensis, H. indicus
Coleoptera (beetles): Meloidae (blister beetles): Lytta vesicatoria; Oedemeridae (false blister beetle)
Injection of toxin
Acarina: Metastigmata (can cause tick paralysis)
Ixodidae (hard-bodied ticks): Amblyomma sp., Dermacentor sp., Hyalomma sp., Rhipicephalus sp., Boophilis sp.
Argasidae (soft-bodied ticks): Ornithodorus sp.
Araneida (spiders): ������Phoneutria nigriventer (banana spider), Loxoceles reclusa (brown recluse spider), Lactrodectans mactans (black
widow spider)
Chilopoda (centipedes): Scolopendra subspinipes
Scorpiones (scorpions): Centruroides sp.
Allergic reactions (localized and systemic), insect body parts, by-products, bites, anaphylactic shock
Apidae (honeybees, bumblebees): Apis mellifera, A. mellifera scutellata
Vespidae (wasp, yellow jackets, hornets): Vespula sp., Dolichovespula sp.
Mutillidae (velvet ants): numerous species
Formicidae (ants): Solenopsis sp. (fire ants)
Culicidae (mosquitoes): numerous species
Simuliidae (black flies): numerous species
Acarina (house dust mites): Dermatophagoides pteronyssuss, D. farinae, numerous other species
Blattidae (cockroaches): ingested feces, numerous species
Acarina: Ixodidae and Argasidae (soft- and hard-bodied ticks)
Entomophobia and delusionary parasitosis
Numerous examples for all insects, spiders, ticks, and mites

lice (Anoplura), and true bugs (Hemiptera). The major causing greater hardships worldwide, than all the other
pathogens include viruses, rickettsia, bacteria, helminths, vector-borne diseases combined (Busvine, 1993). Examples
and protozoa. Viruses transmitted by arthropods are called of vectors and associated diseases include Anopheles mos-
arboviruses. Zoonoses are diseases in which the pathogens quito species and the different types of malaria; the human
are maintained in vertebrate hosts other than humans (i.e., body louse, Pediculus humanus humanus L., and epi-
yellow fever and arboviral encephalitis). Anthroponoses demic typhus; the mosquito, Aedes aegypti L., and yellow
are those diseases in which humans are the only known fever and dengue; the oriental rat flea, Xenopsylla cheopis
vertebrate host (i.e., malaria and epidemic typhus). (Rothschild), and plague; the tsetse flies, Glossina spp.,
Common vectors and pathogens for several important and African trypanosomiasis; the Triatominae bugs and
tick- and mite-borne diseases are listed in Table 4.2. Insect- American trypanosomiasis; Simulium species and onchocer-
borne pathogens and vectors are listed in Table 4.3, and ciasis; Leptotrombidium tick species and scrub typhus; and
those transmitted by mosquitoes are listed in Table 4.4. the black-legged tick or deer tick, Ixodes scapularis, and
Mosquitoes deserve special recognition because they are Lyme disease (Eldridge and Edman, 2000). Arthropods may
responsible for transmitting more pathogens to humans, be both nuisance pests (direct effects) and disease vectors
234 Hayes’ Handbook of Pesticide Toxicology

Table 4.2 Vector-Borne Pathogens Transmitted by Mites and Ticks

Disease Pathogen Vector

Mites

Bacteria

Rickettsial pox Rickettsia akari Liponyssoides sanquineus


Scrub typhus R. tsutsugamushi Trombiculidae and Leptotrombium species

Ticks

Arboviruses

Tick-borne encephalitis Flavivirus Ixodes ricinus


Omsk hemorrhagic fever Flavivirus Dermacentor pictus
D. marginalis
Ixodes persulcatus
Kyasanur forest disease Flavivirus Haemaphysalis species
Powassan encephalitis Flavivirus Dermacentor andersoni
Russian spring–summer fever Flavivirus Ixodes persulcatus
Haemphysalis concinna H. japonica douglasi
Crimean–Congo hemorrhagic fever Bunyaviridae, Nairovirus Hyalomma marginatus and other tick genera
Colorado tick fever Reoviridae and other tick species Dermacentor andersoni

Bacteria

Tick-borne relapsing fever Borrelia recurrentis Ornithodorus spp.


Tularemia Francisella tularensis Ixodes and Dermacentor sp.
Rocky Mountain spotted fever Rickettsia rickettsia Dermacentor andersoni
D. variabilis
Lyme disease Borrelia burgdorferi Ixodes scapularis
Dermacentor variabilis
Ehrlichiosis Ehrlichia sp. D. variabilis, Amblyomma americanum

Protozoa
Texas cattle fever Babesia bigemina Boophilus annulatus
East coast fever Theileria parva Rhipicephalus appendiculatus
Babesiosis Babesia microti Ixodes sp.

(indirect effects). For example, the forest day (Asian tiger) transferred from the eggs to the different developmental
mosquito, Aedes albopictus Skuse, which was introduced stages (transtadial transmission). Adult males may also
into the United States presumably in used tires from Japan, transmit pathogens to females during mating (venereal
is a potential vector of several arboviruses; however, even transmission). A key concept in medical entomology is
in the absence of disease transmission, it is an aggressive that all species of arthropods are not capable of transmit-
daytime biter, making it a major pest wherever it becomes ting all possible pathogens. Evolutionarily, a pathogen has
established (Hawley, 1988; Hawley et al., 1987; Mitchell, adapted by various means to the biological and ecological
1991, 1995; Moore and Mitchell, 1997; Novak, 1995; barriers associated with its invertebrate vectors and verte-
Shroyer, 1986). brate hosts. Thus, mosquitoes, in general, do not transmit
The transmission of a pathogen may be classified as the human immunodeficiency virus, Culex species are not
either horizontal or vertical. Horizontal transmission is vectors of malaria, and Anopheles species are not a con-
from an infected animal host via vector to a new, unin- cern for arboviral encephalitis. For a pathogen to pass from
fected animal host. Some pathogens, particularly viruses, an infected host to a blood-feeding vector, there must be
are also transmitted vertically. Vertical transmission may a relatively high level of circulating pathogens in the host
be between an infected female host and her offspring or because of the extremely small percentage of total blood
between developmental stages of a vector arthropod. An taken in the blood meal. Many disease agents, such as
infected female insect may transfer pathogens to the eggs arboviruses and the malaria parasite, have overcome this
(transovarial transmission) and the pathogens may be hurdle by causing either a viremia or a periodic release of
Chapter | 4 Public Health Pesticides 235

Table 4.3 Vector-Borne Pathogens Transmitted by Nonmosquito Insects

Insect species Disease Pathogen Distribution

Arboviruses
Phlebotomus papatasi Sand fly fever Bunyaviridae Africa, Asia, Europe
and other species
Culicoides sp. Bluetongue virus Reoviridae Africa, Asia, United States

Bacteria
Xenopsylla cheopis and Plague Yersinia pestis Worldwide
other rodent fleas
Xenopsylla cheopis, Murine typhus Rickettsia typhi North America, Europe
various species
Pediculus humanus Epidemic typhus Rickettsia prowazekii Worldwide, scattered foci

Pediculus humanus Louse-borne relapsing fever Borrelia recurrentis Mainly Africa


Phlebotomus spp. Bartonellosis Bartonella bacilliformis South America
Chrysops spp. Tularemia Francisella tularensis Worldwide

Protozoa
Glossina spp. African trypanosomiasis, African Trypanosoma gambiense, Africa
sleeping sickness T. rhodesiense
Triatominae spp. American trypanosomiasis Trypanosoma cruzi Central and South America
(Chagas disease) Panstrongylus spp.
Rhodnius spp.
Phlebotomus spp. Visceral leishmaniasis Leishmania spp. Mediterranean, North Africa,
L. donovani Middle East, Asia, Central and
South America

Phlebotomus spp. Cutaneous leishmaniasis Leishmania spp. North Africa, Middle East
L. tropica
Lutzomyia spp. American leishmaniasis L. braziliensis Central and South America
Psychodopygus spp.

Nematodes
Simulium spp. Onchocerciasis Onchocerca volvulus Central and South America, Africa
Chrysops spp. Loiasis, eye worm Loa loa West and central Africa

an infective stage in their hosts, respectively. For example, and eastern equine encephalitis virus (Monath, 1988).
Plasmodium parasites must pass through several biological Transmission does not invariably lead to disease in hosts
barriers in the mosquito vector, including the midgut and because many sylvatic hosts are asymptomatic. The patho-
hemolymph, in order to eventually concentrate in internal gen also faces the possibility of being introduced by a com-
organs such as the salivary glands where they are trans- petent vector into a host capable of clearing the invading
mitted to a host with the next blood-feeding cycle (Beier, pathogen or a previously infected host with a stimulated
1998). If the pathogen completes this passage and can immune system. Often, vertebrate hosts become immune
infect a host, the arthropod carrier is called a competent for an extended period of time after an initial infection;
vector, even if it has not been demonstrated to be an eco- however, there are also cases of recrudescence (in which
logically significant one. Transmission efficiency may vary the host exhibits clinical symptoms of a disease from a
considerably among species, and their role in transmission previous infection after a prolonged period of recovery).
in an area may depend on their abundance, longevity, and Pathogens can also evade the immune response of hosts by
feeding behavior. Animal hosts that do not produce a high changing the antigen signal presented to the host’s immune
level of circulating pathogens for a biologically significant system (Mandell, 1990; Manson-Bahr and Bell, 1987). The
period of time are dead-end hosts. They may contract the time from the introduction of the pathogen into the host
disease but are not important in maintaining the transmis- to the first clinical expression of the disease is called the
sion cycle. Such is the relationship of humans and many intrinsic incubation period. The extrinsic incubation period
arboviruses, such as St. Louis encephalitis virus (SLEV) is the time from which the vector acquires the pathogen
236 Hayes’ Handbook of Pesticide Toxicology

Table 4.4 Major Vector-Borne Pathogens Transmitted by Mosquitoes

Mosquito species Disease/agent Distribution

Arboviruses—Togaviridae
Aedes and Culex species Venezuelan equine encephalitis (VEEV) Tropical Americas
Culiseta melanura and Aedes species Eastern equine encephalitis (EEEV) Americas, Southeast Asia, eastern
Europe
Culex tarsalis and Culiseta species Western equine encephalitis (WEEV) United States
Arboviruses—Flaviviridae
Aedes aegypti Dengue (DENV-1, -2, -3, -4) Worldwide Tropics
Culex tritaeniorhynchus Japanese encephalitis (JEV) Asia, Japan
Culex pipiens, Cx. quinquefasciatus, Cx. St. Louis encephalitis (SLEV) North and South America
tarsalis,
Cx. Nigripalpus West Nile virus (WNV) Israel, Europe, Russia, northern Africa
Culex, Anopheles, and Aedes species
Aedes aegypti Yellow fever (YFV) South and Central America, Africa

Arboviruses—Bunyaviridae
Aedes triseriatus LaCrosse encephalitis (LACV) United States
Culex quinquefasciatus Rift Valley fever (RVF) Africa

Protozoa
Anopheles species Malaria Worldwide, Tropics and
An. gambiae, An. funestris, Plasmodium falciparum Subtropics
An. stephensi, An. albimanus, P. vivax
An. darlingi, An. darius, An. P. malariae
arabiensis, and others P. ovale

Nematodes
Aedes, Anopheles, and Brugian filariasis Southeast Asia
Mansonia species Brugia malayi Subtropics and Tropics,
Aedes, Culex, and Anopheles Bancroftian filariasis Worldwide
species Wuchereria bancrofti
Various mosquito species Dog heartworm, dirofilariasis, Dirofilaria Worldwide
immitis

to the point at which it can be transmitted to a new host carbon dioxide-baited traps for hematophagous arthropods,
(Eldridge and Edman, 2000; Harwood and James, 1979). chemical- and visual-baited traps for tsetse flies and black
Vectorial capacity is the effectiveness of a vector popu- flies, oviposition and gravid traps for mosquito eggs and
lation to transmit a pathogen at a specific time and loca- females, dippers for mosquito larvae, and dragging and
tion. Measuring vectorial capacity means quantifying the flagging for ticks (Bidlingmeyer, 1974; Calvin and Gibson,
key biological interactions of the vector, host, and patho- 1992; Reeves, 1990; Service, 1993). Note that most moni-
gen under different environmental conditions (Metcalf and toring techniques collect both vector and nonvector species
Novak, 1994). It generally represents a composite of patho- and that accurate taxonomic description of the specimens
gen virulence, host and vector susceptibility, vector ecol- can be critical. For example, within the genus Anopheles,
ogy (longevity, feeding preferences, mobility, abundance, there are considerable species-specific differences in vec-
diurnal activity, etc.), and the influence of local ecological tor competency and feeding behavior (Curtis and Townson,
variables and meteorological parameters (primarily rainfall 1998). Some species avidly blood-feed on humans (anthro-
and temperature) on vector population dynamics (Lehane, pophagy); however, their importance in transmission in a
1991; Walker et al., 1996). Understanding vector ecol- particular area may be related to their occurrence inside or
ogy provides the basis for determining when and where to outside of human habitats (endophily and exophily, respec-
apply control interventions, and it is particularly important tively). Refinement of surveillance techniques comes with
for selective pesticide application (Service, 1993). a better understanding of vector ecology and behavior.
To determine the spatial and temporal distribution Almost all of these techniques provide a relative estimate
of vector species, effective surveillance techniques are of population abundance rather than an absolute estimate
required. Light traps are used for many flying insects, (number per unit area or volume), and they are best used
Chapter | 4 Public Health Pesticides 237

as indicators of the presence or absence of the vector or for Epidemiology is the study of the determinants, occur-
seasonal changes in relative abundance (e.g., an increase in rence, and distribution of diseases in a defined population
oviposition or blood-feeding activity). (Nutter, 1999). It attempts to discover the linkage between
The transmission cycles of vector-borne diseases can the environment and three aspects of disease transmission:
range from simple insect–man–insect transmission (e.g., host–pathogen, pathogen–vector, and vector–host interac-
malaria) to complex interactions with multiple hosts, res- tions. The goal is to define the determinants and risk fac-
ervoir species, and vectors that may vary in different eco- tors in order to develop the most effective measures for
logical habitats (Eldridge and Edman, 2000; Harwood prevention and control. For example, control tactics aimed
and James, 1979). Vector and host interactions also vary at reducing yellow fever epidemics had only marginal suc-
between arthropod developmental stages. For example, cess until it was determined that the mosquito Ae. aegypti
ticks generally have larval and nymphal stages associated transmitted the virus (Karlen, 1995; McGrew, 1995). In
with small mammal and bird hosts, whereas the adults are general, the more quantifiable information available about
often found on larger wild and domestic mammals and the dynamics of the pathogen, vector, and host interactions,
humans. Ixodes scapularis, the black-legged tick or deer tick, the greater the opportunities are for disrupting the trans-
requires a blood meal for each developmental stage, which mission cycle (Metcalf and Novak, 1994).
takes approximately 2 years from larva to adult (Hinrichsen
et al., 2001; U.S. Armed Forces Pest Control, 1990). Each
stage feeds only once and each takes several days to ingest 4.3 Impact of arthropods on
the blood. Larvae and nymphs typically become infected human health
with the Lyme disease bacteria, Borrelia burgdorferi, when
they feed on infected white-footed mice (Peromyscus leu- In addition to the emotional burden, vector-borne dis-
copus) or chipmunks (Tamias striatus). The adult stage is eases impose a huge economic encumbrance on families
found on larger animals and is often extremely abundant and governments worldwide through lost productivity and
on white-tailed deer that are usually asymptomatic for the health care costs. For example, there are 300–500 mil-
disease. Most Lyme disease cases in humans are associated lion clinical cases of malaria annually, with 1.5–2.7 mil-
with the bite of the nymphal stage of I. scapularis, which lion deaths each year, including approximately 1 million
are difficult to detect because of their small size. Humans deaths among children younger than 5 years of age (WHO,
primarily contract Lyme disease when they invade the tick 1995; see http://www.who.int/tdr/diseases/malaria/default.
habitat either for work or for recreation and due to close htm). In sub-Saharan Africa, malaria accounts for 20% of
proximity of housing to natural areas with an abundance of all childhood deaths. Lymphatic filariasis, another mos-
vectors and small, medium, and large blood hosts. quito-borne disease, is second only to mental illness as
Transmission cycles that occur in the absence of humans, the world’s leading cause of long-term disability, disfigur-
generally under natural or sylvatic conditions, are called ing more than 40 million people. Onchocerciasis, or river
enzootic or maintenance cycles, and those involving an blindness, transmitted by black flies, places more than 85
increase in transmission to domestic and peridomestic hosts, million people in Africa, Latin America, and the Arabian
as well as humans, are called epizootic or epidemic cycles Peninsula at risk for visual impairment, blindness, and
(Eldridge and Edman, 2000). Transmission cycles of a skin lesions. Sleeping sickness, transmitted by the tsetse
pathogen can vary geographically. St. Louis encephalitis in fly, threatens 55 million people in 36 countries of sub-
the United States has at least three distinct vector–pathogen Saharan Africa. In Latin America, up to 18 million people
relationships in the western, east central, and southeast- are infected with Chagas disease, a parasitic disease trans-
ern parts of the United States (Monath, 1988; Tsai and mitted by blood-sucking true bugs. The chronic stage of
Mitchell, 1989). Evidence indicates that genetic variability Chagas disease can last for years as parasites invade the
in the pathogen, some of which may relate to virulence, internal organs. Leishmaniases, caused by flagellate pro-
can be found between large-scale geographic areas, such tozoans transmitted by Old and New World phlebotomine
as the eastern and western United States, as well as small- sand flies, affects more than 12 million people, damaging
scale areas, such as differences in SLEV within a single internal organs and producing skin lesions and mutilations
county in Texas (Chandler and Nordoff, 1999; Charrel of the nose and mouth. Approximately two-thirds of the
et al., 1999; Trent et al., 1980). Furthermore, an insect or tick world’s inhabitable land mass is at risk for vector-borne
may transmit more than one pathogen, such as I. scapularis, diseases, although it is undeniable that the Tropics have
which has been implicated as the main vector for Lyme the greatest hardship.
disease (Borrelia burgdorferi), babesiosis (Babesia There can be little doubt that vector-borne diseases
microti), and ehrlichiosis (Ehrlichia chafeensis), or have been instrumental in shaping human history, deter-
Ae. aegypti, which transmits different serotypes of dengue, mining the outcome of wars and limiting human expan-
as well as the yellow fever virus (Calisher and Monath, sion into potentially habitable tropical areas. The reader
1988; Lederberg et al., 1992; Zeidner et al., 2000). is referred to several texts about the historical impact of
238 Hayes’ Handbook of Pesticide Toxicology

vector-borne diseases on human society (Busvine, 1993; been reduced in the temperate zones of Europe and North
Karlen, 1995; Mandell, 1990; McGrew, 1995). It appears America, conditions do exist for their emergence and
that the Eurasian cradle of civilization in the Old World reemergence (Childs et al., 1999; Mellor and Leake, 2000).
was also the cradle of infectious and vector-borne dis- In the past 40 years, the leading industrialized nations have
eases, which is not surprising considering that the factors been overconfident that new technologies, such as vacci-
favoring domestication of livestock and the development nations, pharmaceuticals, synthetic pesticides, and genetic
of a stratified society also favored disease transmission engineering, will eventually manage vector-borne diseases
(Diamond, 1999). When Europeans started to conquer (Gubler, 1998). Although the benefits of technology have
and colonize the Americas, far more natives died due to not always been as anticipated, they have provided consid-
the introduction of lethal microbes (smallpox, measles, erable insight into the evolutionary processes governing the
influenza, mumps, pertussis, tuberculosis, etc.) than on co-adaptations of pathogens, vectors, and hosts.
any battlefield. Of approximately 12 infectious diseases Recent events have made us aware that even major
of exotic origin that became established in the Americas, industrialized nations can be poorly prepared for the intro-
4 were vector-borne – epidemic typhus, malaria, plague, duction of new pathogens. For example, the West Nile
and yellow fever (Diamond, 1999). However, Europeans virus (WNV), a flavivirus in the Japanese encephalitis sub-
and their progeny in the New World were not immune to group, was introduced by unknown means into New York
2 vector-borne diseases introduced through slave trade City in 1999 and was perceived as two separate epidem-
from tropical Africa, namely yellow fever and malaria ics, one in humans and the other in zoo and feral birds
(Manson-Bahr and Bell, 1987). Yellow fever was intro- [Centers for Disease Control and Prevention (CDC), 1999].
duced to the New World in the 1500s, and in some cases, Apparently, by the time the pathogen was correctly identi-
cities suffered a 10–15% mortality rate. Colonists and fied from the different host sources and vector control was
slaves in the 16th and 17th centuries introduced two spe- implemented, the epidemic was already declining. Mosquito
cies of Plasmodium malarial parasites (P. vivax and P. fal- pools positive for the virus implicated Culex pipiens as the
ciparum) into the Americas. During the Lewis and Clark main vector and possibly the overwintering reservoir (CDC,
expedition across the Louisiana Purchase in the early 19th 2000a–c). By the end of the following year, the virus had
century, Peruvian bark powder (containing quinine and spread to 12 states, with 21 human cases from Connecticut,
quinidine) was considered essential to fight the inescapable New Jersey, and New York; 4323 birds documented to be
fevers of malaria (Ambrose, 1996). Many of these malari- infected in 12 states; and 60 horse cases in 7 states. The
ous areas had never been visited by Europeans or African number of mosquito species implicated as potential vectors
slaves; however, the disease had spread through native grew to approximately 12 (CDC, 2001a,b). This human
American trade routes from areas of initial contact. Many and wildlife threat may severely challenge the public
of the same vector-borne diseases remain as major impedi- health and vector management infrastructures in the United
ments to the economic development of tropical areas in States.
both the New World and the Old World.
The decline of several vector-borne diseases during
the 20th century in the United States was due to a com- 4.4 Integrated pest management
plex mix of variables, including changes in housing con- and vector management
ditions, demographics, nutrition, medical diagnosis and
treatment, outdoor exposure times, and mosquito abate- The concepts and practices of IPM, which were largely
ment. However, North America is far from being free of developed in response to crop pests, were found to be read-
vector-borne diseases. The vector-borne pathogens in the ily adaptable to arthropod public health pests (Dent, 1995;
United States are the arboviral encephalitis viruses trans- Kogan, 1998; Metcalf and Novak, 1994). The initial step
mitted by mosquitoes and the tick-borne borrelial and in vector management is to identify and define, as best as
rickettsial disease agents. Malaria cases do occur in the possible, the components of the pest management unit for
United States, but they are primarily imported, brought in a specific area. Once the transmission cycle of the patho-
by travelers from endemic areas. Occasionally, autochtho- gen and the life histories of the vector, host, and reservoir
nous transmission does occur, especially in areas near air- or maintenance species are identified, the cornerstone of
ports and areas where large groups of exposed individuals vector pest management is surveillance. An IPM program
congregate (Zucker, 1996). Competent vectors of malaria, can be initiated for almost any public health pest, even
An. quadrimaculatus and An. freeborni, are still present in with a limited knowledge of the transmission dynamics,
the United States. This is true for several arthropod-borne by implementing a monitoring strategy. Surveillance deter-
diseases. Outbreaks of dengue in Mexico annually threaten mines potential risk, when and where to treat, and the basis
Gulf Coast states such as Texas because they also have the for adapting management interventions to a particular area
major vector, Ae. aegypti. It is important to realize that (Service, 1993). Monitoring typically focuses on the inci-
although the incidence of major vector-borne diseases has dence of the vector and pathogens. Pathogen surveillance
Chapter | 4 Public Health Pesticides 239

may be in vectors, sentinel hosts, or humans (disease sur- Monitoring trends in vector populations and disease
veillance). The detection of pathogens can be broadly incidence in humans and animal hosts is the basis for
classified into direct and indirect methods (Duvallet et al., developing and refining predictive epidemiological mod-
1999; Hoeprich et al., 1994; Mandell, 1990; Manson-Bahr els, as well as for determining intervention failures and the
and Bell, 1987). Direct pathogen surveillance includes any development of insecticide and/or pharmaceutical resis-
method that isolates the disease agent, in vivo or in vitro, tance. In general, operational failures (e.g., the incorrect
or some characteristic biochemical or structural compo- amount of pesticide applied to the target vector) are more
nent of the pathogen. This includes visual detection, bio- common than cases of pesticide resistance, especially with
chemical response to the pathogen, and identification of the advent of biodegradable carbamates and organophos-
DNA/RNA sequences or fragmentation patterns. Indirect phorous and pyrethroid insecticides and acaricides (note
pathogen surveillance includes methods that rely on an that not all pesticides within each of these classes can be
in vivo or in vitro response to the pathogen, including considered biodegradable) (Bloomquist, 2001; Ware, 1991,
detection of characteristic pathology or antibody response 2001; WHO, 1997). However, the possibility of resistance
(host serology or various immunoassay methods) (Coyle, should never be ignored (Brogdon and McAllister, 1998;
1997). Federal, state, and/or local public health agencies in Hemingway and Ranson, 2000). It has been estimated that
the United States are usually responsible for pathogen or 56 of the 66 important Anopheles vectors of human malaria
disease surveillance and measuring trends in disease inci- are resistant to three residual insecticides (DDT, lindane,
dence. However, human disease surveillance is seldom an and dieldrin) that were widely used for malaria eradica-
effective tool for managing an outbreak (Teutsch, 1994). tion. At least 31 of these species have additional resistance
For example, the response to the WNV outbreak in New to the organophosphates malathion and fenitrothion, and
York City included distribution of repellents to the public, another 14 species have multiple resistance to the carbar-
aerial applications of malathion and sumithrin, and a vast nate propoxur. Eight Anopheles species are resistant to
public relations effort to warn and advise residents how pyrethroids (Metcalf, 1989a,b). Any management pro-
to avoid pesticide and mosquito exposure. An examina- gram that relies heavily on a limited number of chemicals
tion of the 1999 case data and onset dates indicates that the for vector abatement should be concerned about resistance
epidemic had already peaked before the majority of these (Brown and Pal, 1971).
actions were taken (CDC, 1999). In contrast, vector con- Integrated pest management attempts to minimize the
trol may have reduced the number of human WNV cases development of insecticide resistance by reducing the
in 2000, although it was unable to contain the spread of the selection pressure from a specific chemical agent through
virus (CDC, 2001b). the application of physiological, ecological, and/or behav-
Most mosquito abatement districts (MADs) in the ioral specificities (Metcalf, 1998, 1999). Specificity can
United States focus on monitoring vector species (MADs include the selection of pesticides that are more active
generally focus on mosquito management; however, their against the target organism than nontargets. It also includes
mandate frequently includes other nuisance and vector rotating chemicals of different classes and/or different vec-
arthropods and vertebrate pests). The goal of vector man- tor detoxification mechanisms within and between vector
agement is to implement control techniques to reduce developmental stages. For example, in mosquito control,
pest abundance below the levels necessary for the transi- an early season treatment with an organophosphorous com-
tion from enzootic transmission to epizootic or epidemic pound may be rotated with a later season treatment with a
transmission. Unfortunately, due to the ecological and bio- pyrethroid or by not using the same pesticide for adult and
logical complexities of pathogen transmission, predictive immature stages (e.g., malathion ULV for mosquito adults
models are few (CDC, 1993; Monath, 1988; Reiter, 1988). and temephos liquid formulations for mosquito larvae).
Thus, most MADs attempt to prophylactically reduce vec- Selection pressures can also be reduced by mixing chemi-
tor populations without knowing whether they are disrupt- cal and nonchemical control techniques and by targeting
ing a pathogen transmission cycle or not. Typically, they the placement of pesticides to maximize impact on the vec-
rely on seroconversion of sentinel animal hosts (e.g., chick- tor. This includes treating specific areas where there is a
ens for SLEV) or public health bulletins of human cases concentration of the target vector, such as larval habitats or
before they implement emergency control measures, such resting sites of adults, and adjusting the seasonal and diur-
as ultra-low-volume (ULV) spraying for adult mosqui- nal timing of applications to vector population dynamics
toes. For several vector-borne diseases, the ability to detect and flight periodicity.
pathogens in low concentration, as well as identify vector Despite the similarities of vector management to crop
and pathogen species and species subgroups by molecular pest management, there are significant differences between
techniques, has revolutionized epidemiological studies and the two, many of which impact insecticide use. For example,
provided vector management groups with an early warning a pathogen transmission cycle may include enzootic and epi-
system (Crabtree et al., 1995; DeBrenner-Vossbrinck et al., zootic cycles, involving multiple hosts, reservoirs, and vectors
1996; Howe et al., 1992; Munstermann and Conn, 1997). that exhibit considerable habitat, seasonal, and/or bionomic
240 Hayes’ Handbook of Pesticide Toxicology

variation (Harwood and James, 1979). Transmission cycles capabilities of local areas, thus requiring a governmental
may be unknown, not apparent, or difficult to detect and presence. Unfortunately, those countries at greatest risk
predict. In general, the number of confirmed cases of a for vector-borne diseases are also among the poorest, per
vector-borne disease underestimates the number of people capita, countries in the world.
infected with a pathogen. Furthermore, action thresholds in The arsenal of insecticides registered for public health
vector management (the level of tolerance of disease trans- pests is relatively limited compared to crop pesticides and,
mission before a management intervention is taken) are in areas with protected wildlife, consists of less than two or
lower than economic thresholds for crop pests (the level three alternatives. The WHO Pesticide Evaluation Scheme
of damage tolerance before an intervention is taken). For (WHOPES) lists less than 30 insecticides and acaricides
these reasons, public health management programs rely on for use in public health (http://www.who.int/whopes/qual-
long-term and short-term prophylactic treatments to reduce ity/en). Despite a WHO evaluation program to identify
vector populations and eliminate breeding sites before new pesticides during the past 30 years, less than 5 have
pathogen transmission has been detected, unlike crop pest been introduced in the past decade. One of the basic con-
management (Curtis, 1990; Metcalf and Metcalf, 1993; cepts of IPM is the sagacious use of insecticides and acari-
Mulla, 1994; Reeves, 1990; WHO, 1995). This approach cides. This strategy preserves the pesticide’s efficacy and is
allows the use of natural enemies, source reduction, sani- essential for maintaining the limited arsenal. An unforeseen
tation and sewage management, vegetation and water-flow dilemma in early attempts at vector eradication was the
(salt, water, and freshwater) management, growth regula- loss of insecticides and acaricides to resistance. The loss of
tors, microbial control agents, and relatively host-specific public health insecticides is also due to a conflict between
insecticides (Beidler, 1995; Carlson et al., 1999; Dale projected profit, based on anticipated usage, and the cost of
et al., 1998; Kramer et al., 1995; Russell, 1999; Wolfe, meeting federal registration requirements. Legislation that
1996). Prophylactic interventions are generally habitat and regulates registration of a pesticide, such as the Federal
vector specific, whereas emergency interventions tend to Insecticide, Fungicide, and Rodenticide Act, has produced
rely on insecticides dispensed over broader areas that affect tremendous benefits for U.S. citizens; however, many
a greater number of nontarget organisms. Insecticides will chemical industries often conclude that the profit/cost mar-
probably always be an important component of vector gins are too small (or negative) and do not attempt to reg-
management programs because of their ease of applica- ister new products or reregister old ones for vector species.
tion, efficacy, and rapid action. The benefit:cost ratio for Furthermore, the possible elimination of broad classes of
pest control is $3 to $5 per $1 invested in agriculture and, insecticides, such as the organophosphorous compounds
for vector control, approximately $2.7 per $1 invested by the U.S. Environmental Protection Agency (EPA) under
(Metcalf, 1998). Direct treatment of humans with insec- the Food Quality Protection Act, has sparked considerable
ticides for vector control is rare, except for ectoparasites discussion about the future of vector abatement (DiFonzo,
such as head lice and scabies mites. Personal protection 2001). Undoubtedly, the management of arthropod public
includes repellents, antibacterials, vaccines (few are avail- health pests will become increasingly more important in
able for arthropod-borne diseases), and physical avoidance the future but considerably more challenging.
of the vector. Integrated pest management for public health
pests is an areawide problem, involving public and private 4.4.1 Noninsecticidal Methods in Vector
lands in urban, agricultural, and natural habitats. Therefore,
vector abatement programs often require the cooperation
Management
of several agencies and/or quasi-legal groups at the local, The optimal vector control program has several basic compo-
regional, and national levels. Vector management also deals nents that include an IPM program planning group, seasonal
with several potentially volatile topics, such as human and and full-time employees, facilities and equipment, vector
animal health, pesticide application in urban environments, surveillance, disease detection, chemical and nonchemical
insecticide impact on feral and domestic wildlife, and mod- intervention activities, public education and public relations
ification of human behavior to avoid exposure. Therefore, it activities, intergovernmental coordination, data record-
typically requires the cooperation of the public and various ing and analysis, applied research, emergency contingency
governmental bodies. In the United States, the MADs are plans, and a continuing education component for staff.
area specific, taxing bodies that focus on monitoring and Most vector management programs employ a wide range of
controlling the vector within a county, suburb, or metro- chemical and nonchemical methods to reduce pest arthropod
politan area. Pathogen and/or disease surveillance by local populations before the transmission of a pathogen occurs.
or state public health departments and the CDC assists in The noninsecticidal methods include environmental
detection, trend analysis, standardization of techniques, manipulation; physical, behavioral, and chemical avoidance
and training in vector and disease management. Primary methods; biological control; the burgeoning field of trans-
caregivers generally control prophylactic and/or therapeutic genics and molecular biology; vaccines and therapeutic
drugs. The cost of vector management may exceed the medicine; and legislative actions. It is beyond the scope of
Chapter | 4 Public Health Pesticides 241

this chapter to cover noninsecticidal control methods; there- et al., 1999; Kokoza et al., 2000; Marshall, 1998; Riebe,
fore, we provide a brief annotated list of possible interven- 1999). However, some have challenged the utility of
tions that vary in compatibility with insecticide treatments: transgenics as a method of managing major vector spe-
cies (Jacobslorena and Lemos, 1995; Spielman, 1994).
1. Environmental manipulation or habitat alteration:
Environmental manipulation temporarily or permanently Carriers of toxic genes
changes the environment to eliminate or reduce the num- Altered vector competence
ber of breeding areas, or the habitat is altered to make Symbionts
the breeding areas less hospitable for the arthropod 5. Medical treatment: Vaccines are not available for many
vector or host (Carlson et al., 1999; Hagmann, 1981; of the major protozoan and arboviral diseases, although
Nayar, 1985; O’Meara, 1992; Shroyer, 1989; TVA, considerable work has been done with malaria vaccine
1947; Wolfe, 1996). (Brown et al., 1999; Heppner and Ballou, 1998; Kaslow
Source reduction et al., 1999) and experimental vaccines for eastern
Removal (drainage) equine encephalitis (Wilson et al., 1992). Antibiotics
Sanitation and hygiene successfully treat some protozoan and bacterial patho-
Temperature treatment of infested materials gens (Strickland, 2000).
Source modification Antibacterials
Saltwater marsh management and tidal flooding Vaccines
Stormwater and river management Convalescent care
2. Avoidance methods: Several cultural control techniques 6. Regulatory or legislative actions:
attempt to physically or chemically prevent or at least Local, state, and federal laws and policy statements
reduce the likelihood of contact between humans and
the vector (WHO, 1995). Probably one of the most suc-
cessful cultural controls of flying insects has been the
use of physical barriers to make the home a “vector- 4.4.2 Chemicals in Vector Management
free zone” (Gubler, 1998). Pesticides are important components of most IPM pro-
Quarantines and inspections grams. They are the pharmaceuticals of vector management,
Timing human activities or place and their application should be done on a case-by-case basis
Physical barriers with emphasis on doing no harm to nontarget organisms or
Housing characteristics (screens, air-conditioning, and the environment.
internal sprays)
Bed nets 4.4.2.1 Categorizing Insecticides
Chemical repellents and Acaricides
3. Biological control: Biological control refers to all of
Pesticides are divided into different classes or catego-
the natural biotic causes of mortality, including preda-
ries based on target organism, chemistry, general nature
tors, parasites, and pathogens (Beidler, 1995; Couch
or source, the developmental stage affected, acute and
and Bland, 1985; Courtenay et al., 1989; Kerwin and
chronic toxicity, general action on pests, biochemical or
Washino, 1985; Mulla and Chao, 1991; Petersen, 1985;
physiological activity, application method, and formu-
Porter et al., 1993; Rupp and Rupp, 1995; Steelman and
lation. For a more comprehensive review of the mode of
Meisch, 1990; Woodring et al., 1996). The terms biolog-
action and formulation of pesticides, several texts are rec-
ical and biorational insecticides are sometimes used to
ommended (Barlow, 1985; Bloomquist, 2001; CDC, 1981;
group microbial insecticides with chemical products that
Curtis, 1990; Goss et al., 1997; Metcalf, 1989b; Metcalf
are arthropod specific and have minimal environmental
and Novak, 1994; Sukumar et al., 1991; Tomlin, 1994;
impact, such as insect growth regulators (juvenile hor-
Ware, 1991, 2001; WHO, 1985, 1988, 1990, 1997, 2001;
mone analogs) or chitinase inhibitors. These are grouped
Worthing and Hance, 1991).
together in the section on chemical control methods.
The main classification of pesticides is based on the tar-
Predators and natural enemies (vertebrates and get organism: herbicides, fungicides, rodenticides, bacteri-
invertebrates) cides, nematicides, piscicides, avicides, insecticides, and
Parasites (nematodes and arthropods) acaricides. Insecticides and acaricides can be grouped by
Pathogens (viruses, bacteria, fungi, and protozoa) specific target insects, such as termiticides (termites), pedic-
Microbial insecticides ulicides (lice), and miticides (mites). For mosquitoes, the
4. Transgenics: The refinement of molecular techniques major vector of arboviruses in the United States, insecticides
made possible the use of transgenics to control insects are generally divided into categories based on the develop-
(Brousseau et al., 1999; Crampton et al., 1990; James mental stage they affect (i.e., adulticides and larvicides).
242 Hayes’ Handbook of Pesticide Toxicology

Insecticides and acaricides are commonly grouped into


categories based on a combination of their chemistry and Table 4.5 Insecticides by Category for Arthropods of
general nature or source (Table 4.5). Insecticides may be Medical Importancea
grouped into inorganic compounds, microbial insecticides, Inorganic compounds
oils and surfactants, compounds of botanical origin, insect
Arsenical insecticides
growth regulators (IGRs), organochlorines, carbamates,
organophosphorous compounds, pyrethroids, pyridine Copper acetoarsenite (Paris green)
insecticides, and a general group of unclassified insec- Fluorine insecticides
ticides. Each of these groups can be subdivided based on
Barium hexafluorosilicate
chemistry or mode of action. For example, the organophos-
phorous compounds are subgrouped based on their specific Cryolite
chemical structure, such as the organophosphates, organo- Sodium fluoride
thiophosphates, and organophosphonates. Alternatively,
Sodium hexafluorosilicate
the IGRs are subgrouped by the natural compounds they
mimic – that is, juvenile hormone analogs and chitin syn- Sulfluramid
thesis inhibitors. Microbial insecticides
The U.S. EPA groups pesticides derived from natural
Bacillus thuringiensis israelensis
materials, such as animals, plants, bacteria, and some inor-
ganics, as biopesticides. Biopesticides have three major Bacillus sphaericus
categories: transgenic organisms with pesticidal genes, Lagenidium species
microbial pesticides, and biochemical pesticides such as Mosquito larvicidal films
IGRs and behavior-modifying chemicals. In vector control,
the majority of the research has focused on creating a car- Larvicidal oils
rier for Bacillus thuringiensis var. israelensis endotoxin Golden bear oils (GBOs)
genes that provides a slower settling rate, better uptake rate Bonide
by mosquito larvae, and photostability.
Categorizing insecticides by their mode of action yields Surfactants
several different groups, depending on whether the focus is BVA larvicides
their selectivity, their route of entry, or their site of action. Arosurf/Agnique
Insecticides may be broad spectrum, impacting many ani-
Plant essential oils
mal groups, or specific, primarily active against the target
group of arthropods. Based on route of entry, insecticides Botanical insecticides
are divided into contact, stomach, systemic, or respiratory Neem
poisons. They can be persistent (residual insecticides) or
Azadirachtin
short term (biodegradable). Unfortunately, within the bio-
degradable synthetic insecticides (e.g., carbamates, pyre- Pyrethrins
throids, and organophosphorus compounds), there are often Cinerin I, II
exceptions to the rule regarding persistence and acute tox-
Jasmolin I, II
icity. Probably the most informative classification system
is that based on the biochemical and physiological systems Pyrethrin I, II
attacked, which provides a better indication of the target Rotenone
specificity. For example, insecticides may be divided into
Ryania
neurotoxins, muscle poisons, metabolic inhibitors, and
physical toxicants. These can be even further subdivided. Sabadilla
Neurotoxins include chemicals that interfere with nerve Numerous toxic phytochemicals
transmission (acting on sodium or chloride channels), such
Insect growth regulators
as DDT, the pyrethroids, and -aminobutyric acid antago-
nists; neurotransmitter mimics, such as the nicotinoids and Chitin synthesis inhibitors
octopamine-related synthetics; and synaptic enzyme inhibi- Diflubenzuron
tors, such as the carbamate and organophosphorous anti-
Juvenile hormone analogs
acetylcholinesterases. A detailed discussion of insecticides
and their mode of action can be found in Metcalf (1989b) or Fenoxycarb
on the World Wide Web (Bloomquist, 2001; Ware, 2001). Hydroprene
Grouping pesticides based on toxicity also yields sev- Kinoprene
eral categories. A key decision that must be made by the
U.S. EPA during the registration process is determining the
Chapter | 4 Public Health Pesticides 243

Table 4.5 (Continued) Phoxim


Methoprene Phosphonate insecticides
Unclassified IGRs Trichlorfon
Azadirachtin Pyrethroid insecticides
Dicyclanil
First generation
Organochlorine insecticides
Allethrin
Chlorinated diphenyls
Second generation
DDT
Bioresmethrin
Methoxychlor
Bioallethrin
Chlorinated benzene
Phenothrin  sumithrin
-HCH, lindane
Resmethrin
Cyclodiene insecticides
Third generation
Chlordane
Fenvalerate
Dieldrin
Permethrin
Endosulfan
Fourth generation
Carbamate insecticides
Bifenthrin
Bendiocarb
-Cyhalothrin
Carbaryl
Cypermethrin
Propoxur
Organophosphorous insecticides Cyfluthrin

Organophosphate insecticides Deltamethrin

Dichlorvos Tralomethrin

Naled Etofenprox

Aliphatic organothiophosphates Pyridine insecticides

Malathion Acetamiprid

Heterocyclic organothiophosphates Imidacloprid

Coumaphos Thiacloprid
Pyridine organothiophosphates Unclassified insecticides
Chlorpyrifos Borax
Chlorpyrifosmethyl Crotamiton
Pyrimidine organothiophosphates Diafenthiuron
Diazinon a
Not all chemicals are currently registered.
Pirimiphosmethyl
Phenyl organothiophosphates
Fenitrothion
effect a pesticide will have on the environment and nontar-
get organisms. If a formulated pesticide will not generally
Fenthion
cause unreasonable effects, it is classified as “general use.”
Temephos Conversely, a pesticide that may cause adverse effects on
Fensulfothion the environment, including injury to the applicator and
wildlife, is usually classified as “restricted use.” Restricted-
Iodofenphos
use pesticides may be applied only by or under the direct
Aliphatic amide organothiophosphates supervision of a licensed applicator. The level of toxicity
Dimethoate of a pesticide is measured by the response to oral, dermal,
Oxime organothiophosphates or respiratory doses of the pure or technical-grade com-
pound. The measurements can be either acute (single dose)
or chronic (repeated exposure). Acute toxicity is usually
244 Hayes’ Handbook of Pesticide Toxicology

reported as the dose of a compound that causes the death of 4.4.2.2 Examples of Pesticides for Public
50% of the test organisms (LD50). Tests on nontarget organisms Health Pests
often include rodents, birds, and fish. Pesticide labels reflect
the toxicity of these formulations, based on signal words such (a) Ectoparasites (Scabies Mite, Head Louse, Body
as “Danger – Poison” on highly toxic compounds (oral LD50, Louse, and Crab Louse)
50 mg/kg), “Warning” on moderately toxic compounds (oral It has been estimated that more than 2 million school-age
LD50, 50–500 mg/kg), “Caution” on slightly toxic compounds children develop a lice or scabies infestation each year
(oral LD50, 500–5000 mg/kg), and “Caution” on compounds (Adams, 1996; Brown et al., 1995; Downs, 2000). Scabies
with low toxicity (oral LD50, 5000 mg/kg). Chronic tox- is caused by Sarcoptes scabiei mites, which burrow under
icity is the effect of a substance following prolonged and the skin, leaving a trail of feces and eggs and causing a
repeated exposure. Dose is expressed as weight of the test rash and intense itching. The eggs hatch in 3–8 days, and
substance per unit body weight of test animal (milligram the larvae move to the surface of the skin, where they
per kilogram) or as weight of the test substance in parts per molt to two nymphal stages and finally to adults. From
million in an aqueous solution. For inhalation exposure, egg hatch to adult can take 10–14 days. The scabies mite
dose is expressed as weight of the test substance per unit is generally spread by direct contact and from the clothes
volume of air (milligrams per liter) or as parts per million or bed linens of an infected individual (Strickland, 2000;
per day. For dermal exposure, dose is expressed as weight van Neste, 1988). Ivermectin is being tested for the treat-
of the test substance per unit body weight of the test ani- ment of human scabies (Chouela et al., 1999; Yeruham and
mal or as weight of the substance per unit of surface area Hadani, 1998). Lindane is still commonly used to control
(milligrams per square centimeter). In chronic toxicity scabies in Third World countries, along with sulfur com-
studies, the no-observed-effect level (NOEL) is the maxi- pounds and permethrin (Kenawi et al., 1993).
mum dose used in testing that produces no adverse effects The infestation of the body with head or body lice
in the test animals (usually mice). The NOEL is usually (Pediculus capitis and Pediculus humanus, respectively)
expressed in terms of the weight of a test substance given is termed pediculiasis, and the condition of having head
daily per unit weight of test animal (milligrams per kilo- or body lice is called pediculosis. Infestation with pubic
gram per day). (“crab”) lice (Pthirus pubis) is known as pthiraisis. Head
The formulated pesticide, the commercial product, sel- lice and crab lice are not believed to be important vectors,
dom contains only technical-grade chemicals. The mar- although they may cause intense itching (Burgess, 1990;
keted product typically consists of the active ingredients Harwood and James, 1979; Strickland, 2000). In general,
and sometimes synergists, as well as several inert ingredi- head lice are readily spread by physical contact particularly
ents that are responsible for improving storage, handling, among schoolchildren, whereas pubic lice are characteris-
ease of application, efficacy, and safety. The inert ingredi- tic of adults and spread is often by venereal contact. The
ents include surfactants or emulsifiers, stickers, diluents, body louse, a vector of typhus, trench fever, and epidemic
encapsulants, and other adjuvants. The carrier is the main relapsing fever, is less common in the United States than
constituent of the final product and is usually water or oil the other two species. A number of insecticides formulated
in the case of sprays, inorganic clays or talcs in the case for topical application are available for these pests, includ-
of dusts or granules, and organic material such as corncob ing the following:
grits in the case of some granules. Most pesticide com-
pounds are relatively insoluble in water and require an Crotamiton (Eurax) (Burkhart et al., 1998; Ragheb et al.,
emulsifier for them to be mixed with water. Common for- 1995)
mulations of insecticides and acaricides include emulsifi- Lindane (Kwell, Scabene) (Fusia et al., 1987; Robinson
able concentrates, wetable powders or water-dispensable and Shepherd, 1980)
powders, flowable suspensions, oil solutions, dusts, gran- Malathion (Prioderm) (Brown et al., 1995)
ules, aerosols, fumigants, microencapsulated formulations, Permethrin (Elimite, Nix-OTC) (Fusia et al., 1987; Nassif
and baits. Sprays and dusts allow small amounts of pesti- et al., 1980)
cide to be applied directly onto the pest or its immediate RID A-200 Pyrinate (Culver et al., 1988)
environment, but both of these formulations tend to have
a problem with spray drift. Use of granules is one way (b) Acaricides
to overcome problems with drift if the pesticide does not Humans generally encounter ticks on paths and trails in
have to be applied directly onto the pest. Granule formu- parks or natural areas. The best methods of control are
lations are common for several mosquito larvicides, such through prevention tactics of the individual. People going
as methoprene and Bacillus thuringiensis var. israelensis. to these areas should wear appropriate clothing, including
Insecticides and acaricides for ectoparasites of humans, long-sleeved shirts, trousers, and socks. High-top boots
such as lice and mites, are typically formulated as creams, should be worn with the trouser legs tucked into either the
lotions, or shampoos. socks or the boots. Shirts should be tucked into the trousers
Chapter | 4 Public Health Pesticides 245

and the long sleeves buttoned. Repellents, such as diethyl- It is important that larvicides are applied according to label
toluamide (DEET) or permethrin, applied to the clothing specifications and only where larvae are present. Control per-
will also provide additional protection from ticks, although sonnel should also be aware that a single larvicide might not
permethrin-based products are generally considered better be suitable for every mosquito-producing habitat. For exam-
for ticks. Typically, the repellent only needs to be applied ple, Bti is only effective against certain species of mosquito,
as a band around the ankles and waistband. Attached ticks especially floodwater species such as Aedes vexans where the
should be carefully removed with tweezers. Pets should water is relatively clean with little or no organic pollutants. For
be regularly checked for tick attachment and treated as polluted sites with heavy organic contents, Bsph should be the
prescribed by a veterinarian. When local premises are microbial insecticide of choice. Methoprene is the basic com-
infested, a variety of insecticides have been employed suc- pound for registered IGRs for mosquito control. Because this
cessfully to control ticks. compound impairs or stops arthropod growth and molting, it
The following acaricides have been used for the control should be used only in habitats where mosquitoes are the pre-
of ticks in turf, ornamental, and recreational areas: carbaryl dominant species or where other beneficial arthropods would
(Sevin), chlorpyrifos (Dursban), cyfluthrin (Tempo), diazi- not be affected adversely. All insecticides should be used
non (Diazinon,), s-fenvalerate (Zema Lawn Spray), fluval- in accordance with the registered label instructions, which
inate (Mavrik Aquaflow, Yardex), and permethrin (Aziz and include the amount (dose) in pounds or gallons per acre (or
Osman, 1985; Baxter et al., 1999; Goddard, 1998; Khan, kilograms/liters per hectare) and a list of aquatic habitats.
1999; Monsen et al., 1999; Schuurman, 1988). Several of A variety of equipment is available for mosquito-
these pesticides are hazardous to humans and nontarget larviciding operations, ranging from simple hand-pressurized
insects. All pesticides should be applied only as directed on spray cans to complex equipment mounted on either
the label. In some cases, licensed personnel are required. vehicles or aircraft. The type and quantity of equipment
A commercially available permethrin product (Damminix) depend on the size of the community and the number
targets the larvae and nymphs of I. scapularis on and different types of larval habitats. A small community
white-footed mice by filling tubes with insecticide-treated can run an effective program with handheld equipment,
cotton, which mice collect as nesting material (Fehrenbach, whereas larger communities or communities with large
1990; Mejlon et al., 1995). Ticks on the mice are killed, tracts of inaccessible habitats such as salt marshes, large
which in turn is supposed to ultimately reduce the flood plains of rivers, or irrigated farmland require more
number of infected ticks on a treated property; however, sophisticated application equipment and techniques. More
mixed results have been reported (Daniels et al., 1991; information about larval insecticides and specific products
Stafford, 1992). and equipment can be found on the American Mosquito
Control Association website at http://www.mosquito.org or
from WHOPES at http://www.who.int/whopes.
4.4.2.3 Insecticides in Mosquito Management
The method of mosquito control most familiar to the
Mosquito pesticides are generally classified into two cat- public is space spraying, employing vehicle-mounted or
egories: those used to manage the immature stages, or aircraft-mounted spray equipment to kill flying adult mos-
larvicides, and those used to manage the adult stages, or quitoes. A list of registered adult mosquito pesticides is
adulticides. An effective pesticide targeting the egg stage, shown in Table 4.6. When space spraying is the principal
or ovicide, for mosquitoes has not been developed. or only mosquito control activity, good IPM principles are
A variety of larvicides are available to kill mosquitoes, not being followed. In many instances, reliance on space
including petroleum and mineral oils, as well as organo- spraying indicates a failure or the lack of proper preven-
phosphate compounds, which have been used for decades. tative larvicidal measures against the nuisance or vector
In recent years, several effective new insecticides have been mosquito species. Adulticide treatments for mosquitoes
used that are less harmful and less persistent in the aquatic must be based on sound ecological and behavioral infor-
environment. These include the microbial insecticides mation about the species to be treated. Mosquitoes exhibit
Bacillus thuringiensis var. israelensis (Bti) and Bacillus different periods of activity; for example, Ae. vexans and
sphaericus (Bsph) and the IGR methoprene. A new min- Ae. sollictians are crepuscular with primary activity after
eral oil coupled with a surfactant is also being used in sev- sunset and before dawn (Bidlingmeyer, 1974; Horsfall
eral areas of the United States. This lightweight surfactant et al., 1973), whereas Ae. triseriatus, Ae. aegypti, and
has negligible adverse effects on plants and other aquatic Ae albopictus are active primarily during daylight hours
organisms. Table 4.6 lists the current mosquito larvicides (Hawley, 1988; Novak et al., 1981). The spraying of har-
registered by the U.S. EPA. There are numerous reports borage or aggregation sites can be very effective, as are
about natural products for mosquito control; however, few barrier sprays to minimize mosquitoes moving into an
have been evaluated for efficacy under field conditions area (Groves et al., 1994; Ham et al., 1999; Mount, 1998;
(Dennett et al., 2000; Eckenbach et al., 1999; Lampman Mount et al., 1996). However, the effectiveness of the
et al., 2000; Sukumar et al., 1991). treatment is based on good surveillance methods.
246 Hayes’ Handbook of Pesticide Toxicology

Table 4.6 Insecticides Registered in the United States for Use in Mosquito Control
Product Description of use

Larval control insecticides

Temephos Available in several formulations, including emulsifiable concentrate and on sand or corn cob
granules. Higher application rates may be necessary in polluted water. This product is also
registered for use against mosquitoes in artificial containers (cans, tires, bird baths, rain gutters,
etc.).
Methoprene Available in liquid, pellet, briquet, and granular formulations. The briquets are suitable for
use in small depressions and containers. The insect growth regulator kills mosquito larvae by
interfering with the insect hormones that regulate growth. This compound also affects the growth
of arthropods and should be used only in habitats as designated on the registered label.
Bacillus thuringiensis Both Bti and Bsph are microbial larvicides formulated from extracts of bacterial cultures. They
var. israelensis (Bti) are available in liquid, granular, and briquet formulations. Liquid formulations have also been
Bacillus sphaericus (Bsph) successfully used for ULV ground and air application. Bti is used primarily in unpolluted waters,
and Bsph is most effective in polluted and high organic waters
Oils Larvicidal oils that are formulated to spread and cover a water surface function by preventing the
larvae/pupae from reaching the air at the water’s surface or by causing internal toxinosis via the
air tube. Particular care should be taken when using an oil in areas where fish, aquatic animals,
and plants could be harmed.

Adult control insecticides


Naled An organophosphate insecticide available as a liquid concentrate. It is generally used as a ULV spray
from aircraft and ground ULV equipment.
Malathion An organophosphate available in several liquid formulations. It is generally used as a ULV spray from
aircraft and ground ULV equipment.
Pyrethyrins [and piperonyl A botanically derived insecticide generally formulated with PBO. This insecticide has a quick knock-
butoxide, (PBO)] down action on flying mosquitoes.
Permethrin A synthetic pyrethroid insecticide that can be formulated with a synergist (PBO). It is used primarily
as a ULV application or as a perimeter treatment around buildings, parks, etc. to kill resting adults.
Pyrethroids have high bee and fish toxicity; follow label directions.
Resmethrin A synthetic pyrethroid formulated insecticide with PBO. The product has a quick knock-down action
on adult mosquitoes. It is more effective at lower temperatures than some other products.

Phenothrin  sumithrin A synthetic pyrethroid often formulated with other pyrethroids and PBO (used in New York City for
West Nile virus vector control).

Adult control treatments must be conducted under envi- The ULV technique is the most frequently used method
ronmental and climatological conditions suitable for the of adult mosquito control [see Mount (1998) for a review
application of insecticides using thermal fogs, cold aero- of ground ULV applications]. This technique does require
sols, or ULV techniques. These treatments should not be special training in the use and especially the maintenance
conducted if the temperature is below 55°F or above 85°F. of ULV equipment. Moreover, training for the application
These treatments should also be done when wind speed is of pesticides is mandatory because highly concentrated
low (5 mph). When adulticides are sprayed on windy days, insecticides are used. For ULV techniques to be effective,
turbulence makes a uniform pattern difficult to achieve, the droplets must strike the mosquitoes either in flight or
resulting in poor control. Also during windy days, the insec- during exposure when resting. Droplets that are too small
ticide may be dispersed into areas that are not desirable. will not affect active mosquitoes, nor will droplets that are
Ideally, wind speed should be calculated using an anemom- too large because they will settle out of the air too rapidly.
eter. The manufacturer of both the adulticiding equipment Large droplets can also cause spotting on painted surfaces,
and the insecticide will provide recommendations for wind, especially those containing malathion or a corrosive carrier
temperature, and, in many cases, relative humidity for deter- such as oils and synergists. Therefore, the droplets must
mining the limits for ground-applied adulticides. stay within a specific range in order to achieve maximum
Chapter | 4 Public Health Pesticides 247

effect. It is essential that the applicators using this technique clothing that lacks contrasts (i.e., solid colors are better
consult and adhere to the pesticide’s label and follow the than patterned). Loose-fitting long-sleeve shirts and long
operating instructions for the ULV unit so that the machine pants offer a great deal of protection against mosquitoes
is calibrated properly to produce the correct droplet size. and other biting flies. A complete bibliography of repel-
Aircraft have been used for many years to apply insec- lents for blood-sucking arthropods can be found in Gerberg
ticide dusts, granules, sprays, and aerosols [see Mount and Rutledge (2001).
et al. (1996) for a review of aerial applications]. Some Personnel repellents containing DEET are consid-
mosquito control personnel consider it better to use a large ered to be some of the best mosquito repellents (Elston,
volume of low concentrate (e.g., 2 quarts of 55% spray per 1998; Rutledge et al., 1999). However, their effective-
acre) to obtain better coverage, whereas others believe it ness depends on the surface area covered and on climatic
is preferable to use a small volume of higher concentrate conditions. On hot, humid summer days, perspiration can
(e.g., 1 pint of 20% spray per acre). The standard used effectively wash off the repellent, thus necessitating fre-
today assumes that large areas can be covered more eco- quent reapplication. Also, differential repellency by gender
nomically, especially with a reduction of expensive aircraft has been studied by Golenda et al. (1999). It is not recom-
downtime, by using small volumes of highly concentrated mended that DEET be applied to the bare skin of preteen
spray. This led to the development of the ULV spray tech- children (Garrettson, 1997), and even for adults the appli-
nique, defined as a method that uses less than 2 quarts of cations should be concentrated on clothing and not the bare
liquid per acre. For example, using malathion at 3 ounces skin (Chou et al., 1997; Goodyear and Behrens, 1998; Qiu
of technical-grade material per acre, 1 gallon (128 ounces) et al., 1998; Young and Evans, 1998). All repellents should
would treat 43 acres. The ULV technique was modified be kept away from the eyes, lips, and nasal membranes.
and adapted for the application of 0.5–3 ounces of highly Synthetic chemical repellents that are combined with other
concentrated insecticide per acre for the control of mosqui- skin products and sunscreens should be used sparingly.
toes by aerial application. It is very important to read the label and use each product
Aerial ULV spraying is used for both nuisance and accordingly. For a clinician’s guide to mosquito repellents,
disease management of mosquitoes. For example, it was see Fradin (1998).
used against Culex species during an outbreak of SLEV in Area repellents are available to repulse mosquitoes and
Texas in 1966; in New England in 1973, 1974, and 1990 other biting flies from a limited area such as patios, gar-
to control mosquitoes transmitting EEEV (Monath, 1988); dens, and porches. Many of these products include naph-
and for pest management during the major floods in the thalene granules, which can be spread on lawn and foliage,
Midwest in 1993. Aerial applications have also been used and others contain citronella delivered as smoke or from a
very effectively during disasters, for example, in 1989 in candle. Many stores carry a variety of electric bug zappers
South Carolina following Hurricane Hugo and in 1992 that the manufacturers claim will prevent mosquitoes from
in Florida following Hurricane Andrew. For a complete biting. These devices also have a “black” (ultraviolet) light
review of aerial applications for adult and larval treatment, that attracts mosquitoes to an electric grid where they are
see Mount et al. (1996). killed. Field trials of these and other devices, such as sonic
Because of the highly technical nature of this control repellers and mosquito-repellent plants, have been shown
method, mosquito control agencies should consult with the not to work against mosquitoes. For more information on
manufacturers of the insecticides and application equipment as these products, see Jensen et al. (2000). Following is a
well as the appropriate regulatory agencies before conducting list of synthetic repellents produced commercially or for
aerial adulticiding. For more information, see the American military, public health emergency applications: diethyltolu-
Mosquito Control Association website at http://www.mosquito. amide or N,N-diethyl-3-methylbenzamide (DEET); buto-
org or the WHOPES at http://www.who.int/whopes. pyronoxyl; dibutyl phthalate; dimethyl carbate; dimethyl
phthalate; ethyl hexanediol; hexamide; methoquin-butyl;
4.4.2.4 Personal Protection: Vector and oxamate; and piperidine analogs (Bayrepel).
A complete list of phytochemicals and essential oils
Pest Repellents
reported to have repellent activity toward vectors and other
Even the most effective mosquito abatement program can- arthropods is beyond the scope of this chapter; see Curtis
not totally eliminate the nuisances caused by mosquitoes. et al. (1990) for a complete review of natural repellents. The
Therefore, it is necessary at times and in certain environ- following list contains chemicals that have been reported
ments (picnics, fishing trips, nature trails, natural areas, in the literature as repellents, although in some cases
etc.) to employ personnel protection geared toward mini- their efficacy is unsupported (e.g., the use of vitamin B1).
mizing biting mosquitoes. This can be done in a number We have made no attempt to rate their effectiveness based
of ways, including screens in windows and doors, protec- on the literature, and they are presented merely as a ref-
tive clothing, and repellents. Mosquitoes are generally less erence to the variety of natural products claimed to have
attracted to white clothes than darker colored clothes and repellency. In general, natural products are considerably
248 Hayes’ Handbook of Pesticide Toxicology

less effective than synthetic repellents, such as DEET, at order for the U.S. EPA to rely on the best scientific stan-
equivalent concentrations. Several chemicals and essential dards for registration, the use of repellents for reducing
oils do provide relatively short periods of mosquito repel- arthropod-borne diseases must be determined.
lency (Rutledge and Gupta, 1999). Repellency should be
considered to have several components. The first compo-
4.4.2.5 Indoor Residual Spraying
nent is whether it affects the entire sample population; in
laboratory and field tests with mosquitoes, DEET often Indoor residual spraying (IRS) is one of the primary vector
shows a 100% repellency with initial exposure. control interventions that have been employed to reduce or
A U.S. EPA Scientific Advisory Panel found that “no interrupt the transmission of malaria. However, for many
claim” should be made regarding repellent efficacy for years it has received relatively little attention. Recent data
protection against transmission of arthropod-borne dis- reconfirm the efficacy and effectiveness of IRS in malaria
ease pathogens. The reasons for this strong response were control in countries where it has been implemented. For
numerous because most arthropods that interact with example, the application of IRS consistently over time
humans and animals are capable of transmitting pathogens. in large areas has changed vector distribution and thus
altered the epidemiological pattern of malaria in Botswana,
Natural products – identified (Hwang et al., 1985; Matsuda Namibia, South Africa, Swaziland, and Zimbabwe.
et al., 1996; Saxena and Sumithra, 1986): The results of these studies and reports have shown that
Anopheles funestus, a major vector, has been either elimi-
Limonene Vitamin B1
nated or reduced to very low levels. The major vector, An.
Linalool Geraniol gambiae s.s., which rests and bites mostly indoors, was
also controlled primarily due to its proclivity to move into
Camphor Rotundial
houses. Anopheles arabiensis, which does not move or rest
Cineole indoors as much as An. gambiae, is less affected by IRS.
This was found even in areas where high levels of cover-
age occurred (Hansford, 1972; Sharp et al., 1990; Southern
Plant essential oils (Ansari and Razdan, 1995; Barnard, African Malaria Control, 2000).
1999; Curtis et al., 1992; Das et al., 1999; Jensen et al., Anopheles malaria vectors that land and rest inside
2000; Leal and Uchida, 1998; Mulla and Su, 1999; houses after taking a blood meal (endophilic) are particu-
Thorsell et al., 1998): larly susceptible to control through IRS with contact insec-
Neem oil Garlic oil ticides. IRS techniques involve coating the walls and other
surfaces within a house with a long-lasting residual insec-
Aniseed oil Thyme oil ticide. The insecticide of choice should remain active for
Geranium oil Eucalyptus oil 1–3 months, killing mosquitoes and other insects on con-
tact. Note that IRS does not directly prevent people from
Bergamot oil Pyrethrum being bitten by mosquitoes because mosquitoes are usu-
Lavender oil Coconut oil ally killed after they have fed when they rest on the sprayed
surface. The rationale for using IRS is to reduce the
Birchwood tar Soybean oil vector population to prevent transmission of malaria to
Nutmeg oil Pine oil other human hosts. Therefore, for this technique to be effec-
tive, it must be applied to a large number of households to
Orange blossom oil Clove oil reduce the vector population to transmission levels or lower.
Cinnamon oil Pennyroyal oil Several ongoing programs have seen dramatic results using
IRS as a tactic to reduce malaria transmission in Africa,
Peppermint oil Citronella oil Asia, and Central America (Arredondo-Jiménez et al., 1993;
Charlwood et al., 2001; Doke et al., 2000; Rodríguez et al.,
For example, we are constantly seeing new worldwide 2006; Rowland et al., 2000; Sharp et al., 2007).
invasions of exotic arthropod-borne diseases such as West IRS with DDT and dieldrin was the primary malaria
Nile virus due to the increasing movement of humans, ani- control method used during the Global Malaria Eradication
mals, and domestic goods. Also, individual factors such Campaign (1955–1969). Based on its historical impact,
as proper application, individual variability and suscep- several countries have reinitiated DDT as the insecticide of
tibility, and environmental factors all affect the degree of choice for IRS (Gunasekaran et al., 2005; Sharma et al.,
protection afforded by the repellent. In fact, in Gupta and 2005). Although several African countries have adopted
Rutledge (1994), the use of repellents to reduce human– the use of DDT, it is still controversial and has not been
vector contact and reduce the transmission of mosquito- endorsed (Casimiro et al., 2007; Kapp, 2004; Sadasivaiah
borne diseases was not scientifically proven. Therefore, in et al., 2007).
Chapter | 4 Public Health Pesticides 249

Currently, 12 insecticides are recommended by WHO 2. Take all necessary steps to ensure effective implemen-
for IRS, belonging to four chemical groups (1 organo- tation of IRS interventions – including selecting the
chlorine, 6 pyrethroids, 3 organophosphates, and 2 carba- appropriate insecticide, spraying where and when nec-
mates). The choice of insecticide must be informed by the essary and sustaining a high level of coverage – and to
following considerations: prevent unauthorized or unrecommended use of public
l Insecticide susceptibility and vector behavior health insecticides.
l Safety for humans and the environment 3. Strengthen the managerial capacity of national malaria
l Efficacy and cost-effectiveness control programs and improve human, technical, and
financial resources for the timely delivery and high
IRS will only be effective if the target vectors are suscep-
coverage of effective interventions including IRS, with
tible to the insecticide in use. The development of resistance
adequate monitoring and evaluation.
to insecticides constitutes a major threat to the chemical
control of malaria vectors because it compromises the insec- Effective implementation of IRS with DDT or other rec-
ticide’s efficacy. In the past, countries deploying IRS have ommended insecticides should be a central part of national
often been forced to switch to alternative and more expen- malaria control strategies where this intervention is appro-
sive insecticides due to the development of vector resistance. priate. It is implemented with the objective of reducing
Outside Africa, the prevalence and distribution of insecticide malaria morbidity and mortality and accelerating progress
resistance in malaria vectors have not been major impedi- toward global and national malaria targets. However, there
ments to insecticide-based interventions, except in some are important considerations that must be taken into account
areas of India, the Middle East, and Central America. when determining whether to introduce or scale up IRS. In
However, in Africa, the potential threat of resistance particular, there must be sufficient capacity to deliver the
to public health insecticides appears to be significant. intervention effectively, prevent unauthorized and unrecom-
Resistance to DDT and pyrethroids in major malaria vec- mended use of public health pesticides, and manage insec-
tors has been found throughout West and Central Africa, ticide resistance. Intensified research efforts are needed, for
in some areas at a high level, as well as in several areas of example, to develop new insecticides, long-acting formula-
eastern and southern Africa. Resistance to carbamates has tions, and improved application technologies.
been found in countries of West Africa, with a mechanism Along with producing IRS manuals and guidelines,
that also induces cross-resistance to organophosphates. The WHO will support countries with collecting and analyzing
selection of resistance in most malaria vectors is thought data to determine the potential effectiveness and feasibility
to be largely the result of past and present use of insecti- of IRS in the national context and with planning and imple-
cides in agriculture. The precise operational implications menting the intervention. WHO requests countries report on
of insecticide resistance are not fully understood. coverage and impact as IRS is implemented or scaled up.
A comprehensive assessment of resistance at the local This position statement is intended for public health
level must be carried out before planning any IRS program, policymakers, malaria control program managers, develop-
especially in West and Central Africa. The possibility of ment agencies, development banks, academic and research
insecticide resistance calls for the careful monitoring of the institutions, and private sector corporations involved in
susceptibility of malaria vectors to insecticides throughout scaling up malaria control programs.
the world and the sound management of resistance.
There are specific interactions between insecticides and 4.4.2.6 Insecticide-Treated Bed Nets
malaria vectors. Some insecticides tend to repel more than to
Insecticide-treated bed nets (ITNs) are a form of personal
kill vector mosquitoes. Changes in vector behavior induced
protection that has been shown to reduce severe disease
by insecticides may have important operational implica-
and mortality, especially in children, due to malaria. In
tions, and it is important to be aware of them when selecting
communitywide trials in several African settings, ITNs
insecticides for IRS. DDT is the only insecticide that is used
have been shown to reduce all-cause mortality by approxi-
exclusively for public health; therefore, unlike with other
mately 20% (D’Alessandro et al., 1995; Gimnig et al.,
insecticides, resistance development to it is no longer influ-
2003; Wiseman et al., 2007).
enced by other uses such as in agriculture. In the context of
The use of untreated bed nets to form a protective barrier
resistance management, it is therefore advisable to maintain
around the people using them has been employed for years
the use of DDT until a suitable alternative is available. WHO
to prevent the transmission of malaria via anopheline mos-
recommends that national governments do the following (see
quito bites. However, mosquitoes can feed on people through
http://malaria.who.int/docs/IRS-position.pdf):
the nets, and nets that have holes no matter the size provide
1. Introduce and/or scale up coverage of targeted IRS as a little protection. The development and implementation of
primary malaria control intervention in countries where bed nets impregnated with a residual insecticide has greatly
available data indicate that it can be effective toward enhanced their protective efficacy. The insecticides that
achieving malaria targets. have been employed kill the mosquitoes and other insects
250 Hayes’ Handbook of Pesticide Toxicology

on contact. Some of the insecticides, especially DDT, also Conclusion


have repellent properties that reduce the number of mosqui-
toes that enter houses (Roberts, 1998). In addition, if high The spectacular success of synthetic insecticides in the
numbers of nets are deployed and used within a community, decade immediately following World War II generated wide-
the numbers and longevity of mosquitoes will be reduced. spread enthusiasm that the major scourges of mankind, such
In these circumstances, even those who do not use a bed net as yellow fever, malaria, and typhus, could be conquered.
will afford protection from biting anopheline mosquitoes This in fact did occur, with major reductions in malaria and
(Etang et al., 2007). However, to achieve such effects, high yellow fever and a significant reduction in other arthropod-
community coverage is required (Fernando et al., 2008a,b). borne pathogens such as typhus and plague. However, these
Early programmatic implementation of ITNs required short-term successes resulted in major increases in disease
a reapplication of insecticide at intervals ranging from transmission primarily due to resistance in both the arthro-
6 to 12 months. Moreover, nets had to be retreated every pod to insecticides and to drugs by the pathogen. The result
time they were washed. Retreatment was accomplished by of these failures has forced the public health community to
simply dipping them in a mixture of water and insecticide reevaluate strategies and has resulted in the development of
and allowing them to dry in an area protected from direct evidence-based management or integrated disease manage-
sunlight. This process was considered a major logistical and ment. Employing this management strategy, both insecti-
economic barrier to full implementation of ITNs in countries cides or drugs are used in a targeted manner that results in
within malaria (Kroeger et al., 2004; Rafinejad et al., 2008). a significant increase in efficacy, environmental safety, and
Currently, several types of nets are available for use cost-effectiveness. The challenge for the future is to better
in malaria control programs. Nets can vary by size, mate- understand the natural history and bionomics of arthropod-
rial, and/or insecticide treatment. The majority of nets are borne disease systems and to use this information to target
made of polyester, but nets are also available in cotton, effective control measures. In short, the when, where, and
polyethylene, or even polypropylene (Sharma et al., 2006; how, coupled with the principle of addressing where the
Skovmand et al., 2008). arthropods or pathogens are the most concentrated, immo-
WHO has approved only pyrethroid insecticides for bile, and accessible, should form the basis for future investi-
use on ITNs, primarily due to their very low mamma- gations and management programs.
lian (human) toxicity but high toxicity to mosquitoes and
other insects (N’Guessan et al., 2001; Snow et al., 1999).
Pyrethroid insecticides also exhibit a rapid knock-down References
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