The Changing Role of Insecticides in Structural Pest Control

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Chapter 5

The Changing Role of Insecticides in


Structural Pest Control
Michael K. Rust
University of California, Riverside, California

5.1 Introduction environmental and health concerns have become an


important consideration in urban pest management, espe-
The widespread use and need for pest management in and cially as it relates to water quality issues. The detection
around structures can be directly attributed to the dislike of pesticides, particularly pyrethroids, in urban water-
of insects and arthropods by urban residents. Some insects ways has raised concerns about their use, especially for
such as termites and wood-destroying beetles pose a seri- ant control. Certainly the resurgence of the bedbug, Cimex
ous economic threat to structures and a few such as cock- lectularius L., has focused attention on finding effective
roaches, fleas, mosquitoes, and ticks may present a real residual insecticides and alternative pest control strate-
medical or veterinary threat. Even though bedbugs do not gies. Wherever possible, information on the efficacy and
vector human diseases, their recent reemergence as a pest residual activity of new active ingredients, improved for-
worldwide has already dramatically influenced pest man- mulations, and alternative strategies will be provided. The
agement practices and consumer attitudes about structural chapter concludes with some thoughts regarding the future
pest control. Surveys indicate that only 10% of respon- directions of urban pest management.
dents could recognize bedbugs, and individuals 60 years
old did somewhat better with 20% identifying them
(Reinhardt et al., 2008). Many other urban insects may 5.2 Pest problems: real or perceived
be classified as occasional intruders and nuisance pests.
Surprisingly, some of these such as spiders are considered The mere presence of insects and arthropods in and around
by homeowners to be a major problem that requires treat- structures is of concern to homeowners and is generally
ment (Rust, unpublished data). perceived as a pest problem (Rust, 2001). In recent years,
In recent years, there has been an increased awareness there has been a resurgence in the number of bedbugs found
of the potential hazards of pesticides in urban environ- worldwide, including Canada (Hwang et al., 2005), Israel
ments and demand for more integrated pest management (Mumcuoglu, 2008), Italy (Masetti and Bruschi, 2007),
(IPM) and so-called “green pest control.” Even though Korea (Lee et al., 2008), the United Kingdom (Boase,
green pest control lacks a clear definition and is largely a 2001), and the United States (Anderson and Leffler, 2008).
marketing tool, it has generated considerable attention. It In 2003, Orkin Inc. reported treating 390 cases of bedbugs
has revitalized urban IPM, especially strategies that utilize in 33 different states in the United States (McGinnis, 2004).
less insecticides, and has stimulated the development of Public health officials documented 46 locations in Toronto
several different training programs for pest management infested with C. lectularius in 2003 and PMPs reported
professionals (PMPs). The increased use of container- treating another 847 locations (Hwang et al., 2005). Single-
ized and gel baits, insect growth regulators (IGRs), natural family dwellings and apartments made up 70 and 18% of the
products, and alternative strategies such as extreme tem- locations treated, respectively. Even in an area endemic for
peratures, modified atmospheres, and physical barriers is malaria, 33% of those surveyed in Tanzania felt that the
indicative of the public’s increased interest in IPM. tropical bedbug, Cimex hempiterus F., was more troublesome
This chapter expands on the use patterns of insecti- than mosquitoes. Respondents from houses infested with
cides in and around structures to control the major urban bedbugs always thought them more of a problem than mos-
insect pests reviewed by Rust (2001). In recent years, quitoes (Temu et al., 1999). In fact, there was a significant

Hayes’ Handbook of Pesticide Toxicology


Copyright © 2010 Elsevier Inc. All rights reserved 257
258 Hayes’ Handbook of Pesticide Toxicology

correlation between bedbug infestations and the purchase increased (TDC Environmental, 2008). In a suburb of
and use of pyrethroid-treated bed nets. It is easy to see why Sacramento, CA, bifenthrin was implicated as the primary
the topic of bedbugs shares center stage at urban pest man- cause of toxicity to the amphipod Hyalella azteca Saussure
agement conferences worldwide. with additional toxicity from cyfluthrin and cypermethrin
In agriculture, the decision to apply an insecticide or (Weston et al., 2005). They identified the probable sources
treatment strategy (action threshold) is often based on some of the pyrethroids to structural pest control applications and
economic injury level (EIL; Flint and van den Bosch, 1981). homeowners’ use of lawn care products. In a study involv-
In urban settings, economic thresholds have not been estab- ing 15 creeks in California and 12 creeks around Nashville,
lished and action thresholds are often based on a perceived TN, 12 of the 15 creeks in California had sediments or
economic damage or an aesthetic injury level. The aesthetic water toxic to H. azteca (Amweg et al., 2006). Bifenthrin
injury level (AIL) is highly variable and is based on expe- was suggested as the most likely pesticide causing the tox-
rience, education, and accompanying attitudes of the target icity because of its high concentration at each of the sites.
audience (Zungoli and Robinson, 1984). Consequently, the Probable sources of the bifenthrin, cypermethrin, and del-
presence of a single bedbug, cockroach, spider, or cat flea tamethrin may have been applications made by PMPs.
indoors may result in an insecticide treatment. However, However, eight different products containing bifenthrin were
attempts to establish procedures by which EIL and action available to homeowners in California and they may have
thresholds can be established have been proposed (Pinto, also contributed to its detection in the creeks. Pyrethroids
2000; Pinto and Kraft, 2000). Five criteria proposed to were detected in water runoff and sediments in storm water
establish an EIL are economics, health and safety, esthetics, drains in residential neighborhoods in Sacramento (Weston
public opinion, and legal issues (Pinto, 2000). These action et al., 2009). Bifenthrin was of greatest toxicological con-
thresholds are typically not based on any scientific method cern with up to 73 ng/l in water and 1211 ng/g in sediment,
and are simply educated guesses. Thus, the action threshold with cypermethrin and cyfluthrin being of secondary impor-
is not zero and the EIL or AIL should be higher (Stejskal, tance. Dry season irrigation was less important than intense
2002). Preventive treatments should be justified based on the storm events in discharging pyrethroids into the storm
comparison of preventive versus responsive pest control and drains. The total consumer sales of bifenthrin in California
the cost of forecasted/expected damages (Stejskal, 2003). in 2005 was 4759 kg AI, 69% of this being purchased from
Justifying preventive treatments and adopting nonzero tol- June to September when ants were most active. The total
erances will result in fewer calendar-based treatments. If amount applied by PMPs was 19,271 kg AI, 39% being
adopted by PMPs, this could have a substantial impact on applied from June to September. The patterns of bifenthrin
future urban IPM programs, especially in the reduction of detection were primarily attributed to professional use. One
insecticide applications. of the major problems with the pyrethroids in these urban
Pesticides are frequently used and stored in homes (Rust, systems is that they are primarily particle-bound, smaller
2001). This is especially true in low-income housing where particles containing higher concentrations. The concentra-
cockroach and mice problems commonly exist. In a study of tions on particles decline slowly over the first year and then
urban minority women, 85% reported pest control measures persist for a long time (Berger-Preiss et al., 1997).
conducted during their pregnancy and 35% reported their Indoor applications of insecticides are routinely made to
homes being sprayed for pests (Whyatt et al., 2002). Greater control cockroaches. In a study of minority women and pes-
than 90% of the pesticides used were to control cockroaches. ticides used during their pregnancy, 90% of the pesticides
Most residents in inner city public housing reported using used were for cockroach control (Whyatt et al., 2002). As
insecticides to control cockroaches and 15% reported using the level of housing disrepair increased, there was an increase
illegal pesticides (Chew et al., 2006). in pesticide use. Air monitoring revealed that diazinon (2–
6010 ng/m3), chlorpyrifos (0.7–193 ng/m3), and propoxur
(3.8–1380 ng/m3) were found in residences of all the women
5.3 Environmental and health monitored in the study. Some women’s exposure to diazinon
concerns may have exceeded health-based levels. Urine samples of
children in a long-term study were analyzed for the common
In recent years, there has been an increasing concern about metabolites of pyrethroids and Lu et al. (2006, 2009) reported
pesticides in urban watersheds. In the San Francisco Bay continuous exposure to pyrethroids in their diet all year and
area, it has been suggested that “spraying pesticides on periodic episodes of high exposure, especially in children in
and around buildings to control Argentine ants has histori- homes where pesticides were applied seasonally. The intensive
cally been among the most problematic pesticide uses for use of household pyrethroids in the fall and increased con-
water quality” (TDC Environmental, 2006). The amount sumption of imported produce in the winter and spring may
of organophosphate insecticides used in urban areas in have contributed to the high seasonal levels. Pest control
California significantly decreased from 2000 to 2006, but applications increased the levels of pyrethroids such as cyflu-
the use of bifenthrin, cyfluthrin, and permethrin dramatically thrin, cypermethrin, deltamethrin, and permethrin in house
Chapter | 5 The Changing Role of Insecticides in Structural Pest Control 259

dust and airborne particles and permethrin and cyfluthrin apartments sampled had detectable levels of cockroach
remained above background levels in house dust for 1 year allergen (0.4 U/g Bla g 1), 52% had 2 U/g, and 33% had
(Leng et al., 2005). The levels of permethrin and piperyonl 8 U/g. Of the 1173 residents in those units, 13 and 9%
butoxide in air samples were highly associated with self- had medically diagnosed asthma and allergy, respectively.
reported use of spray cans and total release aerosols by In a study of New York City public housing, cockroaches
pregnant women (Williams et al., 2008). Even up to 5 years were found in 77% of the apartments and 15% of the resi-
after chlorpyrifos and diazinon were eliminated for residen- dences had used illegal pesticides, cockroach chalk, and
tial use, 92% of the personal air samples contained them. Tempo (cyfluthrin registered for professional use only;
Seventeen different pesticides were analyzed from Chew et al., 2006). Dust samples containing cockroach
farm, rural, and urban households (Obendorf et al., 2006). allergen (Bla g 2) were 8 U/g in 36% of the kitchens and
Chloryprifos, resmethrin, and tetramethrin were found in 15% of the bedrooms sampled. Apartments with one or
higher levels in urban households. Higher residues were more asthmatic patients were characterized by beds with
found on carpets compared with smooth surfaces and set- high cockroach allergen, cockroaches in the kitchen, and
tled dust. In general, the amount of residues from indoor resident reports of seeing cockroaches. Most residents
pest control practices was lower than those in agricul- reported using cockroach baits, but 66% indicated that
ture and horticulture landscapes. In Boston public hous- they had used total release aerosols or foggers, insecticidal
ing, permethrin, chlorpyrifos, diazinon, and cypermethrin chalk, sprays, and Tempo.
were detected in 100, 100, 98, and 90% of kitchen floor Environmental interventions including sealing cracks
swipes in all units tested, respectively (Julien et al., 2008). and small holes, applications of gel baits to cracks and crev-
Cyfluthrin, restricted to professional use only, was found ices, boric acid, and vacuuming cockroach fecal material
in 70% of the homes even though they did not hire pro- and debris in a Boston public housing project resulted in
fessional pest control service. Residents were appar- clear reductions of cockroach allergens (Levy et al., 2006).
ently applying the formulated wettable powder to control The greatest reduction in cockroach allergens corresponded
cockroaches. to the greatest improvement in asthma health conditions in
Appropriately performed pest control applications of the apartments. The Bla g 1 allergens were reduced by 71
pyrethroids such as cyfluthrin, permethrin, cypermethrin, and 53% in the kitchen and bedroom, respectively, and Bla
and deltamethrin led to significantly increased pyrethroid g 2 allergens by 86 and 70%, respectively, within 6 months
metabolite concentrations in occupants at days 1 and 3 (Peters et al., 2007). After 6 months, the concentrations of
post-treatment compared with pretreatment levels (Leng allergens began to increase indicating that the intervention
et al., 2003). However, metabolite levels did not exceed must be sustained. In a study comparing a baiting program
published background levels. Studies of German PMPs conducted by university-based entomologists and service
indicated no expected health effects after occupational provided by PMPs, the baiting program provided 90%
applications of pyrethroids as long as label directions were reductions in cockroaches trapped, whereas the PMPs
followed (Hardt and Angerer, 2003). achieved between 62 and 81% reductions (Sever et al.,
Asthma induced by insects and other arthropods is of 2007). There were significant reductions in allergens (Bla g
major importance in structures, especially low-income 1) at all locations in homes baited by university personnel.
apartments. The prevalence of cockroach allergens and Even though there was an 83% reduction in cockroaches
their mitigation have been reviewed by Arruda (2005), in kitchens in PMP treatments, the level of allergen only
Gore and Schal (2007), and Perzanowski et al. (2008). In decreased by 35.7%. Clearly, very substantial reductions or
a national survey and sampling of residents in apartments near elimination of cockroaches is needed to make signifi-
in the United States, 11% of living room floors and 13% cant reductions in the allergens present.
of kitchen floors had concentrations of cockroach allergen In addition to living with cockroaches in housing,
(Bla g 1) exceeding 2.0 U/g (level associated with allergic occupational risks also occur. In a survey of seamen,
sensitization) (Cohn et al., 2006). In 3% of living rooms 68.3% reported exposure to cockroaches on board ship
and 10% of kitchens the levels exceeded 8.0 U/g (level (Oldenburg et al., 2008). Of them, 26.9% were cockroach
associated with asthma morbidity). Elevated concentra- sensitive to a skin prick test. Seamen from tropical coun-
tions were associated with high-rise apartments, homes tries (37.3%) were significantly more sensitive than sea-
built before 1940, urban areas, low-income households, men from temperate countries (21.3%).
and multifamily structures. Residents (86%) reporting A new source of indoor allergens in structures is the
cockroach problems had considerably higher levels of invasive Asian ladybird beetle, Harmonia axyridis Pallas
allergen, 58% having 2.0 U/g and 38% having 8.0 U/g (Nakazawa et al., 2007). Adult ladybird beetles enter struc-
in their homes, than did those not reporting cock- tures in the fall, frequently overwintering in large numbers.
roaches. In low-income housing, 81% of the apartments Patients primarily exposed to allergens from the German
were infested with cockroaches, mice, and other insects cockroach, Blattella germanica (L.), had a significant
(Wang et al., 2008). Kitchen dust samples in 98% of the cross-reaction to two proteins isolated from H. axyridis.
260 Hayes’ Handbook of Pesticide Toxicology

5.4 Insecticide applications


Table 5.1 Active Ingredients Which May be in
5.4.1 Nonresidual Insecticides Minimum-Risk Pesticide Products Exempted under
Section 25(b) of FIFRA
When insecticides are applied to kill existing infestations
and do not provide long-lasting effects, they are typically Castor oil (U.S.P. or Linseed oil
equivalent)
classified as nonresidual applications (Anonymous, 1989).
These can be defined as follows: Cedar oil Malic acida
Nonresidual insecticides are those products applied to Cinnamona and cinnamon Minta and mint oila
obtain insecticidal effects only during the time of treatment oila
and are applied either as space treatments or as contact Citric acida Pepperminta and peppermint oila
treatments:
Citronella and citronella oil 2-Phenethyl proprionate
a. Space treatment is the dispersal of insecticides into the air (2-phenylethyl proprionate)
by foggers, misters, aerosol devices, or vapor dispensers Clovesa and clove oila Potassium sorbate
for control of flying insects and exposed crawling insects. a
Corn gluten meal Putrescent whole egg solids
b. Contact treatment is the application of a wet spray for
a
immediate insecticidal effect. Corn oil Rosemarya and rosemary oila
Cottonseed oila Sesamea and sesame oila
The nonresidual insecticides are most typically applied
Dried blood Sodium chloridea
as aerosol or spray formulations of allethrin, esfenvalerate,
resemethrin, and synergized pyrethrins (Braness, 1997). Eugenol Sodium lauryl sulfate
Considering the popularity of aerosol sprays, there is a a
Garlic and garlic oil a
Soybean oil
paucity of data concerning their efficacy. A review of some
Geraniol Thymea and thyme oila
earlier studies is provided by Rust (2001).
Alternative low-impact chemical treatments are popular Geranium oil White peppera
especially among those interested in so-called green pest Lauryl sulfate Zinc metal strips
control. High-viscosity foams produced with air or CO2 a
Lemon grass oil
killed significantly more German cockroaches than did low-
viscosity foams (Choi et al., 1997). Baldwin and Koehler a
These active ingredients are exempt for use on all food commodities
from the requirement of a tolerance on all raw agricultural commodities
(2007) reported that contact sprays of various commercially at 40 CFR 180.1164(d) (EPA, 2009).
available dishwashing liquids and household cleaners were
toxic to adult male German cockroaches. Topical sprays of
a 0.54% solution provided 50% kill of adult males.
In recent years, the use of the exempt products that con- cinnamic alcohol were neuro-insecticides and their toxicity
tain ingredients listed in Table 5.1 has become popular with was species-dependent. The octopaminergic system medi-
PMPs. In contact toxicity studies against German cock- ated the insecticidal activity of eugenol and -terpineol,
roaches, pulegone, camphor, and verbenone were comparable but not cinnamic alcohol. Eugenol has been reported to
to permethrin (Jang et al., 2005). Eucalyptus, marjoram, pen- affect octopamine receptors and mimicks octopamine,
nyroyal, and rosemary oils had more pronounced contact and thereby increasing cellular calcium levels, and causes
vapor activity against human head lice, Pediculus humanus toxicity (Enan, 2001). However, Price and Berry (2006)
capitis De Geer, than did -phenothrin and pyrethrum (Yang reported that eugenol and octopamine had opposing effects
et al., 2004). In vapor phase toxicity tests, verbenone, -thujone, on dorsal median neurons in the American cockroach,
thymol, -terpineol, camphor, linalool, and marjoram oil were Periplaneta americana L., inferring that eugenol must
toxic to cockroaches, but considerably less active than dichlor- interact on a different subtype of octapmine. Geraniol and
vos. Monoterpenoids such as 1,8-cineole, anisole, limonene, citral showed some similarities to octopamine. Inhibition of
and -pinene showed vapor activity against eggs and adult P. acetylcholinesterase (AchE) has been proposed as a mode
humanus capitis (Toloza et al., 2008). Deposits of basil, cit- of action for the essential oils. However, Picollo et al.
ronella, lemon, peppermint, and tea tree oils were not highly (2008) found the vapor activity of 1,8-cineole and toxicity
toxic to Argentine ants, Linepithema humile (Mayr), and red to P. humanus capitis greater than dichlorvos but found no
imported fire ants, Solenopsis invicta Buren, but deterred them correlation with inhibition of AchE activity.
from crossing barriers (Wiltz et al., 2007). Only citronella oil Even though there has been considerable interest in
provided 50% kill of Argentine ants in 34 min and 100% kill these essential oils and compounds exempt from U.S.
within 24 h. Environmental Protection Agency (EPA) registration, there
The mode of action of the essential oils remains unclear. has been very little published about their use in pest man-
Enan (2001) reported that eugenol, -terpineol, and agement programs and effectiveness. With limited residual
Chapter | 5 The Changing Role of Insecticides in Structural Pest Control 261

activity, additional structural modifications and cultural malathion, deltamethrin, and cypermethrin (Pantoja et al.,
controls may be necessary to provide satisfactory control, 2000). A field-collected strain of German cockroach was
especially for PMPs providing every other month or quar- highly resistant to permethrin and deltamethrin, had low
terly pest control. cross-resistance to imidacloprid, and had no cross-resistance
to fipronil (Wei et al., 2001). German cockroaches collected
5.4.2 Residual Insecticides from 29 different locations in North Carolina exhibited resis-
Insecticides applied to provide control over a longer period tance to cyclodienes and cross-resistance to fipronil, and
of time are typically referred to as residual insecticides there was a direct relationship between survivors exposed
(Anonymous, 1989). These are defined as follows: to dieldrin and fipronil (Holbrook et al., 2003). These cock-
Residual insecticides are those products applied to obtain roaches were resistant to ingested fipronil bait. In urban
insecticidal effects lasting several hours or longer and are areas of Taiwan, patterns of resistance in B. germanica pop-
applied as general, spot, or crack and crevice treatments: ulations were propoxur  chlorpyrifos  cypermethrin in
hospitals, and propoxur  cypermethrin  chlorpyrifos in
a. General treatment is an application to broad expanses houses (Pai et al., 2005). Resistance patterns reflected the
of surfaces such as walls, floors, ceilings, or as an out- overall insecticide use in both hospitals and homes. Two
side treatment. field-collected strains in Denmark were resistant to dieldrin
b. Spot treatment is an application to limited areas on and the most resistant strains were homozygous for A302S
which insects are likely to occur but will not contact mutation, imparting 1000-fold resistance to dieldrin and
food or utensils or ordinarily contact workers. These 15-fold resistance to fipronil (Kristensen et al., 2005). In
areas may occur on floors, walls, and bases or under- Iran, 11 field-collected strains of German cockroaches were
sides of equipment. For this purpose a “spot” will not resistant to permethrin and showed no cross-resistance to
exceed 2 square feet. fipronil (Nasirian et al., 2006). Field-collected strains of B.
c. Crack and crevice treatment is an application of small germanica were shown to have multiple resistance mecha-
amounts of insecticides into cracks and crevices in nisms to permethrin, namely kdr-type and metabolic resis-
which insects hide or through which they may enter the tance (Limoee et al., 2007). The presence of pyrethroid
building. Such openings commonly occur at expansion resistance must be taken into account when developing an
joints, between different elements of construction, and IPM program to control German cockroaches.
openings that may lead to voids such as hollow walls, The use of inorganic dust formulations, silica aerogels,
equipment legs and bases, conduits, motor housings, and boric acid to treat wall voids, attics, and other areas
and junction or switch boxes. likely to harbor cockroaches and silverfish has been advo-
Residual insecticides have been the primary chemicals cated for decades (Ebeling, 1995). Our understanding of
used by PMPs because they allow for less frequent visits the mode of action of boron remains unclear, and a review
and applications. Consequently, they are routinely applied of the literature on boron toxicity in insects is provided by
according to a schedule in a preventive manner. Typically Gentz and Grace (2006) with special emphasis on termites.
insecticides only account for 3–5% of the costs of treat- Subterranean termites were confined to borate-treated
ments provided by PMPs and thus labor and travel are wood surfaces for 5 days, then removed, and placed on
much more important in reducing costs. untreated wood. They excreted or metabolized about 60%
of the boron and survived the exposure (Gentz and Grace,
2008). This clearly supports the use of borate-treated
5.4.2.1 General Treatments
lumber in a preventive role in IPM programs but not as a
Sprays are frequently applied around structures as barri- remedial treatment.
ers to prevent the accumulation of insect pests and their Even though diatomaceous earth and silica aerogel are
movement into structures. Typically, treatments consist of principally silica, the high sorptivity of insect wax by silica
high volumes (0.5–1.0 gal/100 ft2) of low concentrations aerogels makes them much more effective as a desiccant
of insecticides applied in bands 2.4–3 m wide on and adja- than diatomaceous earth. Diatomaceous earth principally
cent to the structure (Klotz et al., 2008; Rust, 2001). In the acts as an abrasive (Ebeling, 1995). Diatomaceous earth
past few years, this practice has been questioned because treated with dichlordimethyl-saline significantly increased
of the potential for insecticide runoff from hard surfaces the insecticidal activity against German cockroaches even
into urban surface waters. Consequently, more targeted at high humidities (Faulde et al., 2006). Contrary to com-
and site-specific application techniques for ant control are mon knowledge, insecticidal dust deposits including boric
being promoted (Klotz et al., 2007, 2009). acid, Drione, silica gel, silica gel with pyrethrins, and
Physiological insecticide resistance is still an impor- organic dusts can be used in high-humidity environments
tant problem in situations in which residual insecticides (Appel et al., 2004).
are widely applied for the control of German cockroaches. The application of perimeters sprays, especially
Strains of B. germanica collected in Cuba were resistant to for the control of ants, is a widespread and standard
262 Hayes’ Handbook of Pesticide Toxicology

approach to controlling pests outdoors. Barrier sprays Even though the treatment of these sensitive areas rep-
of cyfluthrin, imidacloprid, and fipronil gave varying resents a significant income to PMPs, there has been very
degrees of control against several species of ants (Scharf little published on the efficacy of spot treatments. Nothing
et al., 2004). However, this approach has become a better highlights this situation than the lack of data regarding
major concern because of potential pesticide runoff spot treatments of insecticides for the control of bedbugs.
into urban waterways. Reduced application techniques The resurgence of C. lectularius has stimulated a renewed
to ant trails and structural guidelines provided equiva- interest in finding residual insecticide treatments that can be
lent control to full perimeter treatments and reduced applied inside structures. Continuous exposure on residual
the volume of spray applied by 67% (Klotz et al., 2007, deposits of a probable susceptible strain of bedbugs provided
2009). The effectiveness of perimeter sprays against the following lethal times required to kill 50%: -cyhalo-
ants is enhanced by delayed toxicity and horizontal thrin  bifenthrin  deltamethrin  permethrin  chlorfena-
transfer of insecticides by necrophoresis (Soeprono pyr (Moore and Miller, 2006). None of the insecticides was
and Rust, 2004a). When ants exposed to fipronil die repellent. By contrast, Romero et al. (2009) found that bed-
and are removed by nestmates, lethal doses of insecti- bugs avoided filter paper treated with deltamethrin. However,
cide are transferred to nestmates (Choe and Rust, 2008; a field-collected strain of C. lectularius resistant to deltame-
Soeprono and Rust, 2004b). This horizontal transfer thrin did not avoid harborages treated with deltamethrin.
clearly explains the outstanding results achieved with Chlorfenapyr deposits failed to prevent bedbugs from mat-
perimeter sprays of fipronil (Klotz et al., 2007, 2009). ing and laying eggs (Moore and Miller, 2006). Barriers of
Perimeter spray applications around structures similar to deltamethrin or chlorfenapyr failed to prevent bedbugs from
those applied against ants with microencapsulated cyflu- reaching feeding sources (Romero et al., 2009).
thrin resulted in low but measurable levels of cyfluthrin The development of insecticidial resistance and world-
up to 9.1 m from the structure (Stout and Leidy, 2000). wide human travel and commerce may be the primary fac-
No cyfluthrin was measured in the air indoors, but it was tors leading to the resurgence of bedbugs. Resistance to
detected on some indoor surfaces. Treated soil around permethrin and -cypermethrin has been documented in the
the structure was probably the source of the indoor resi- tropical bedbug, C. hemipterus, possibly resulting from bed
dues. Application techniques that reduce the likelihood net programs to control malaria (Myamba et al., 2002). Anti-
that pesticides move from the target site will become the malarial programs in Sri Lanka may have been an important
new standard in the future. factor contributing to broadscale resistance in C. hemipterus
(Karunaratne et al., 2007). Karunaratne et al. (2007) reported
populations resistant to DDT, malathion, permethrin, and
5.4.2.2 Spot Treatments deltamethrin. A field-collected strain of C. lectularius tested
More precise applications of insecticides are often necessary against deltamethrin required 343 h to provide 50% kill
in environmentally sensitive areas such as food preparation compared with only 1 h in the susceptible strain (Moore and
areas, hospitals, offices, nursing homes, computer facili- Miller, 2006). Considerably more research is needed to find
ties, and museums. The area to be treated and the amount effective chemical alternatives to the pyrethroids.
of residual insecticide to be applied are often important Various microencapsulated formulations (CS) were
considerations. In areas where food is being prepared, pest tested against B. germanica for their bioavailability from
management strategies require the judicious and safe use porous and nonporous surfaces (Stejskal et al., 2007).
of insecticides. The following definition specifically delin- Larger microcapsules were more readily available on
eates such areas (Anonymous, 1989): porous substrates than were smaller microcapsules. The
research suggests that increasing the size of the micro-
A food handling establishment is an area or place other capsules would improve the toxicity of those pyrethroid
than a private residence in which food is held, pro- CS formulations applied to porous substrates. This would
cessed, prepared. and/or served. be especially important for outdoor barrier treatments and
a. Nonfood areas of food handling establishments indoor treatments on greasy and oily surfaces (Rust, 1995).
include garbage rooms, lavatories, floor drains
(to sewers), entries and vestibules, offices, locker
5.4.2.3 Crack and Crevice Treatments
rooms, machine rooms, boiler rooms, garages, mop
closets, and storage (after canning or bottling). It is generally accepted that crack and crevice applica-
b. Food areas of food handling establishments include tions reduce the amount of insecticides in the indoor envi-
areas for receiving, serving, storage (dry, cold, fro- ronment compared with aerosols and sprays. Crack and
zen, raw), packaging (canning, wrapping, boxing), crevice applications of chlorpyrifos in the kitchen resulted
preparing (cleaning, slicing, cooking, grinding), edi- in transport of chlorpyrifos to all locations in the house
ble waste storage, and enclosed processing systems because it is a semivolatile compound with a vapor pres-
(mills, dairies, edible oils, syrups). sure of 1.7  105  mm  Hg at 25°C (Stout and Mason 2003).
Chapter | 5 The Changing Role of Insecticides in Structural Pest Control 263

Air conditioning in the structure may have contributed to the monitoring with traps clearly revealed that most of the conven-
movement. The pin-stream application also produced localized tional spray treatments were totally unnecessary because of
splashing and higher deposition of chlorpyrifos. As expected, extremely low numbers of cockroaches trapped in the schools
a total release application of a similar amount of chlorpy- (Williams et al., 2005). Overall the costs of the services were
rifos produced much higher amounts throughout the struc- similar and the IPM eliminated using propetamphos sprays.
ture. Pyrethroids are not very volatile and translocation may
be more influenced by movement of particle-bound residues.
When applied indoors according to label directions, concentra- 5.5 Soil treatments for
tions of permethrin and deltamethrin were low in the air and subterranean termites
mainly particle bound (Berger-Preiss et al., 1997). Smaller par-
ticles contained higher concentrations of each pyrethroid. The For nearly 50 years, the application of organochlorine insec-
concentrations on particles declined slowly over the first year ticides such as chlordane, heptachlor, aldrin, and dieldrin to
and then persisted for a long time. soil was the primary preconstruction treatment or remedial
In a year-long study comparing a conventional monthly strategy to protect structures from subterranean termites.
baseboard spray (0.025% cyfluthrin) and crack and crevice These insecticides provided an inexpensive and persistent
treatment (boric acid aerosol) with an IPM approach incor- barrier to termites (Su and Scheffrahn, 1998). With the loss
porating vacuuming and monthly or quarterly applications of of organochlorine chemistry, there has been a progression of
baits (2.15% hydramethylnon bait) and IGR devices (90.6% insecticides registered for termite control as partially reviewed
hydroprene), Miller and Meek (2004) found that the conven- by Rust (2001) and Kard (2003). Over the past 20 years, the
tional treatment cost $1.05 per unit treated whereas the IPM water solubility and contact toxicity of many of these insec-
approach was $4.06. However, the average trap catches (15.3) ticides against subterranean termites have increased, whereas
in the conventional routes were significantly higher than the the Kow (octanol water coefficient), Koc (soil organic car-
IPM route (9.2) at 12 months. In another study comparing bon-water coefficient), and soil half-lives have decreased
spray and crack and crevice treatments with baiting programs, (Table 5.2). Consequently, the paradigm about soil applications

Table 5.2 Insecticides that have been Registered for Preventive and Remedial Applications to Soil for the Control of
Subterranean Termites

Insecticide Classa Water solubility Log Koc Log Kow Soil half-life
(g/l)

Chlordaneb OC 0.0001 4.19–4.39 2.78 ~4 years


c
Chlorpyrifos OP 0.002 3.78 4.7–5.11 11–141 days
d
Isofenphos OP 0.018–0.024 2.89 3.30 59–127 days
e
Permethrin PY 0.0002 4.93 2.88 21–42 days
f
Cypermethrin PY 0.000009 5.20 6.6 8–16 days
g
Esfenvalerate PY 0.00002 3.72 6.22 15–90 days
h
Bifenthrin PY 0.0001 5.10–5.48 6.0 65–156 days
i
Imidacloprid NE 0.51 2.12–2.49 3.7 48–190 days
j
Chlorfenapyr CP 0.00014 3.32–3.69 4.83 146–730 days
k
Fipronil PP 0.0019 2.92 5.0 122–128 days
l
Acetamiprid NE 3.5–4.2 2.12–2.43 0.8 1–8 days
a
OC  organochlorine; OP  organophosphate; PY  pyrethroid; NE  neonicotinoid; CP  cyanopyrrole; PP  phenylpyrazole.
b
extoxnet.orst.edu/pips/chlodan.htm; www.eps.gov/ogwdw/dwh/t-soc/chlordan.html
c
pmep.cce.cornell.edu/profiles/extoxnet/carbaryl-dicrotophos/chlorpyrifo-ext.html
d
www.ars.usda.gov/util/download.cfm?file  SP2userFiles/ad_hoc/12755100DatabaseFiles//isofenphos.txt
e
pmep.cce.cornell.edu/profiles/extoxnet/metiram-propoxur/permethrin-ext.html
f
pmep.cce.cornell.edu/profiles/extoxnet/carbaryl-dicrotophos/cypermet-ext.html; www.flouridealert.org/pesticides/msd/flutriafol.armour.c.seed.dress.pdf
g
pmep.cce.cornell.edu/profiles/extoxnet/dienochlor-glyphosate/esfenvalerate-ext.html
h
www.pw.ucr.edu/textfiles/bifentn.pdf; pmep.cce.cornell.edu/profiles/extoxnet/24d-captan/bifenthrin-ext.html
i
pmep.cce.cornell.edu/profiles/extoxnet/haloxyfop-methylparathion/imidacloprid-ext.html; www.cdpr.ca.gov/docs/emon/pubs/fatememo/imid.pdf
j
pmep.cce.cornell.edu/profiles/insect-mite/cadusafos-cyromazine/chlorfenapyr/chlorfenapyr_DECletter_102.html
k
npic.orst.edu/factsheets/fipronil.pdf
l
www.epa.gov/opprd001/factsheets/acetamiprid.pdf
264 Hayes’ Handbook of Pesticide Toxicology

of insecticides to protect and remediate termite infestations authors suggest that as the concentration increases the
has dramatically changed. Remedial treatments provide adsorption coefficient decreases, increasing the amount
shorter residual control, but their activity against termites of toxicant available to kill termites (Kamble and Saran,
has increased. 2005). In general, the residual activity of the newer non-
For decades the U.S. Forest Service has been testing repellent termiticides is significantly less than previously
insecticides in two different field tests as potential soil registered organochlorine, organophosphate, and pyre-
treatments against subterranean termites (Kard, 2003; throid insecticides.
Wagner et al., 2003). Seven different organophosphate and With the advent of the slow-acting nonrepellent chem-
pyrethroid termiticides were applied to two different soil istries, it was suggested that the insecticides were trans-
types in Mississippi and soils were extracted and analyzed ferred horizontally through the colony providing area-wide
over 5 years (Jarratt et al., 2004). The initial concentra- effects and colony kill (Potter and Hillery, 2001). Ninety-
tions at both sites were two times higher than expected three percent of monitoring stations 0.3–4 m away from
according to label directions. Only isofenphos failed to fipronil-treated structures had no termite activity or had
meet minimum thresholds at 5 years. However, with the dead termites. It was suggested that the use of nonre-
advent of the new slow-acting nonrepellent insecticides, pellent slow-acting termiticides might make dogmatic
the utility of these two study designs has come under mandatory full treatments of interior perimeter expan-
closer scrutiny. In other field situations, the residual activ- sion joints and other indoor sites unnecessary (Potter and
ity of some of the insecticides has been considerably less Hillery, 2002). There has been very little direct evidence
than reported in the U.S. Forest Service studies. Organic to support this claim. The perimeters of buildings were
matter content, silt and clay proportions, pH, and cation treated with 0.05% imidacloprid, and termites collected in
exchange capacity affected the bioavailability of imidaclo- traps within 1–3 m from the treated zone were not affected
prid to subterranean termites (Ramakrishnan et al., 2000). by the treatment (Osbrink et al., 2005). When only the
It was not detectable at 0.05 ppm at several homes 1 year perimeters of structures were treated with 0.125% fipro-
after treatment with 0.05% imidacloprid (Osbrink et al., nil, 36% of the structures were still infested at 6 months
2005). Soil residual studies in Arizona found that insec- postreatment (Waite et al., 2004). No area-wide effects on
ticides degraded as follows: chlorpyrifos  imidacloprid the colonies were observed. Similarly, Ripa et al. (2007)
 bifenthrin  permethrin  zeta-cypermethrin (Baker were unable to show any area-wide effects of perimeter
and Bellamy, 2006). The registered termiticides provided treatments of fipronil.
between 2.85 and 5.4 years’ activity. In field studies in Fipronil is a phenylpyrazole insecticide that is extremely
Australia, soils treated with bifenthrin and chlorfenapyr toxic to subterranean termites, with LD50 values ranging
were the most persistent, losing  50% over 12 months from 0.2 to 2 ng/termite (Ibrahim et al., 2003; Saran and
(Horwood, 2007). Chlorpyrifos, fipronil, and imidaclo- Rust, 2007; Yamaoka and Tsunoda, 2007). It is slow-acting
prid were least persistent, losing 99, 67–96, and 50–95%, and nonrepellent with the maximal effects occurring 3–5
respectively. In simulated field studies, imidacloprid levels days after exposure (Remmen and Su, 2005a,b; Saran and
declined from 84.5 to 7.5 ppm in 6 months and the insec- Rust, 2007). Exposure to fipronil-treated deposits resulted
ticidal activity of deposits down to 15 cm decreased dra- in delayed toxicity (Hu, 2005; Saran and Rust, 2007).
matically after 9 months (Peterson, 2007). Preconstruction Horizontal transfer occurs only when donors are exposed
treatment rates of bifenthrin, chlorpyrifos, and imidaclo- to deposits with concentrations 5 ppm (Bagnères et al.,
prid applied at two locations in Mississippi were tested for 2009; Saran and Rust, 2007; Tsunoda, 2006), maximum
longevity and activity (Mulrooney et al., 2006). Bifenthrin transfer occurs within first 24 h (Saran and Rust, 2007),
and chlorpyrifos maintained their insecticidal activity and contact and grooming are the primary mechanisms
for at least 48 months, whereas the imidacloprid signifi- for transfer (Bagnères et al., 2009; Saran and Rust, 2007).
cantly declined within 12 months. Their study showed that Concentrations 100 ppm were needed to transfer fipronil
most of the insecticide and contact with termites occurred among the Formosan subterranean termite, Coptotermes
within the top 2.5 cm of the surface. Richman et al. (2006) formosansus Shiraki (Shelton and Grace, 2003). In a labo-
found that elevating soil pH with Portland cement affected ratory study, the maximum mortality occurred within 1.5 m
residual activity of insecticides as follows: imidacloprid of the treated zone and the maximum effects 2.5 m from
 fipronil  chlorpyrifos  bifenthrin  permethrin  the treated zone (Saran and Rust, 2007). Su (2005) reported
cypermethrin. As soil organic matter increased, the bio- lethal transfer effects 5 m.
availability of fipronil decreased (Mulrooney and Gerard, The neonicotinoid imidacloprid is highly toxic to ter-
2007). Saran and Kamble (2008) found that the half-lives mite workers, with as little as 10.6 ng/termite providing 50%
of bifenthrin, fipronil, and imidacloprid increased as the kill in 7 days (Rust and Saran, 2008). In addition to toxic-
concentration applied to the soil increased and there was ity, sublethal effects have been reported with imidacloprid
an inverse relationship between concentration applied and inhibiting feeding of workers of the eastern subterranean
the time required to kill 50 and 90% of the termites. The termite, Recticulitermes flavipes (Kollar), after exposure
Chapter | 5 The Changing Role of Insecticides in Structural Pest Control 265

(Ramakrishnan et al., 2000). Sublethal exposures to imi- A consequence of this research was the development of
dacloprid also decreased tunneling activity in R. virgini- cockroach baits that changed the paradigm of German
cus (Thorne and Breisch, 2001) and locomotion (Haagsma cockroach control (Reierson, 1995; Rust, 2001).
and Rust, 2007). The deposits are nonrepellent and ter- Behavioral resistance or bait aversion was first
mites readily contact lethal treatments (Haagsma and described by Silverman and Bieman (1993) in a field-
Rust, 2007). Shelton and Grace (2003) found that expo- collected strain of German cockroach. The cockroaches
sures on 100 ppm deposits were necessary for transference. avoided ingesting toxicant/diet mixtures containing
Imidacloprid is transferred between termites primarily d-glucose and this aversion was an autosomal incompletely
by contact (Haagsma and Rust, 2007). Exposures to imi- dominant trait. Another field-collected strain showed
dacloprid decreased locomotion within hours, probably avoidance to fructose, glucose, maltose, and sucrose and
minimizing the importance of horizontal transfer. This sup- moderate levels of physiological resistance to abamectin
ported the finding of Osbrink et al. (2005) that there was and fipronil (Wang et al., 2004). Behavioral resistance to
no measurable horizontal transfer under field conditions. baits was weakly sex-linked, with females inheriting to a
Chlorfenapyr is a slow-acting insecticide that is horizon- greater degree (Wang et al., 2006). These studies suggest
tally transferred by termites (Rust and Saran, 2006; Shelton that behavioral and physiological resistance will quickly
et al., 2006) by mutual grooming and contact (Rust and develop to baits, especially if they are intensively used to
Saran, 2006). Deposits ranging from 100 to 300 ppm were not control German cockroaches. Consequently, better IPM
repellent and as low as 10 ppm prevented tunneling (Rust and strategies that include improved bait bases and rotational
Saran, 2006). Termite movement was greatly hampered within schemes for toxicants will be necessary in the future.
4 h after exposure to 50 ppm chlorfenapyr deposits, limiting Secondary and tertiary mortality of cockroaches
the distance that termites might travel back to the nest. has been reported with baits containing indoxacarb
The neonicotinoid acetamiprid is extremely toxic to ter- (Buczkowski et al., 2008). Factors affecting the trans-
mites with as little as 0.02 and 0.04 ng/termite killing 50% fer included the freshness of excretions from donors, the
of the western subterranean termite, Reticulitermes hes- presence of alternative food, and the length of time of con-
perus Banks, and R. flaviceps (Oshima), respectively (Mo tact between donors and recipients. Behavioral studies of
et al., 2005; Rust and Saran, 2008). Barriers with as little as German cockroaches and baits containing microencapsu-
1–8 ppm prevented termite tunneling. Contrary to the notion lated chlorpyrifos indicated that the amount consumed was
that all slow-acting neonicotinoids are nonrepellent, acet- affected by insect age and food nutrititional content (Jones
amiprid was repellent at all concentrations and acted more and Raubenheimer, 2002). The toxicant affected the aver-
like a pyrethroid treatment in soil (Rust and Saran, 2008). age meal duration and frequency in interaction with age
With the advent of new chemistries such as the neo- and food nutrient effects. Nymphs that survived the initial
nicotinoids, phenylpyrazoles, and pyrroles, changes in the exposure to bait were less likely to ingest lethal doses at
ways that we pretreat and remedially treat structures for a later time. The chitin synthesis inhibitor noviflumu-
subterranean termites have occurred and more are likely ron was active against nymphal B. germanica producing
in the future. With shorter residuals in the soil than pro- 99% kill of laboratory populations at 7 weeks (Wang and
vided by organochlorine, organophosphate, and pyrethroid Bennett, 2006a). In simulated kitchens, mixed populations
insecticides, it may be necessary to re-treat structures more of B. germanica were reduced 96% by week 8. Indoxacarb
often as part of a contractual service. Since some of the baits were toxic and relatively nonrepellent, significantly
newer termiticides are nonrepellent and actively kill forag- reducing field populations of German cockroaches (Appel,
ers, the amount of termiticide applied and the extent of the 2003). In field studies, building-wide IPM programs
coverage may be reduced. By targeting active infestations including baiting were comparable to stand-alone baiting
with repeated treatments, the industry may begin to move for 29 weeks (Wang and Bennett, 2006b).
away from the concept of merely applying long-term pro- Baits and baiting technology are currently being mar-
tective barriers. keted to control subterranean termites (Rust, 2001). The
ideal bait toxicant for subterranean termites (1) must be
slow acting, (2) must act as a nondeterrent, and (3) must
5.6 Baits and baiting not cause adverse effects when ingested at sublethal doses.
Furthermore, its lethal time must be dose independent
Baits have been used to control structural insect pests for (Su and Scheffrahn, 1998). The uptake of hexaflumu-
over 100 years. Typically, they have incorporated fast- ron on worker R. hesperus peaked at about 280 ng at day
acting toxicants such as organochlorines, organophos- 12 (Haagsma and Rust, 2005). Dead termites contained
phates, and carbamates (Rust, 1986, 2001). With the advent 113 ng of hexaflumuron suggesting that this is the mini-
of slower-acting insecticides developed as baits for red mal lethal dose required to kill workers. Hexaflumuron
imported fire ant control in the early 1980s (Klotz et al., was quickly excreted by workers and the half-lives ranged
2008), bait development underwent a major revolution. from 2.1 to 4.7 days, but it was readily dispersed through
266 Hayes’ Handbook of Pesticide Toxicology

the termite colony by trophallaxis. The uptake of the ben- recommend that IPM be conducted (Jones et al., 2007).
zolphenylurea IGR noviflumuron by R. flavipes was simi- This will certainly increase in the future. Insecticides will
lar to hexaflumuron, but the half-life in the termites was continue to play an extremely important role in urban pest
about 29 days compared with 8–9 days with hexaflumuron management, but there will be increased emphasis on those
(Karr et al., 2004). The toxic dose of noviflumuron was that possess a real or perceived threat to urban waterways
two- to threefold less than hexaflumuron. Therefore, the and indoor and outdoor environments. The types of insecti-
faster activity of noviflumuron is in part explained by the cides applied and their use pattern will dramatically change
longer retention in termite workers and its greater intrinsic over the next 10 years and more restrictions on the use of
activity. Another benzolphenylurea compound, bistrifluron pyrethroids around structures are likely. The broadcast use
(5000 ppm), provided slower toxicity to C. formosanus at of insecticides indoors and outdoors and barrier sprays out-
8 weeks (Kubota et al., 2006). Higher concentrations of doors will be phased out for more prescription treatments
bistrifluron caused some feeding repellency. A gel for- such as baits, crack and crevice applications, and traps.
mulation of 2.15% hydramethylnon was tested against the The popularity of baits will continue, stimulating new ave-
western drywood termite, Incisitermes minor (Hagen), in nues of research dealing with the behavior and ecology of
small block tests (Indrayani et al., 2008). It was unclear structural insect pests. Natural products and other chemi-
whether termites had been killed by contact or ingestion of cals such as essential and fragrance oils and detergents
bait, but the results are interesting and warrant additional will also continue to be of interest. It remains to be seen
investigation. if these products can be effectively incorporated into via-
The development and requirements of a toxicant for an ble IPM programs. The consumer and public will demand
ant bait differ from those of termite baits because of the more environmentally safer and effective treatments that
increased amount of trophallaxis and complete metamor- use less insecticides and this will be the direction of urban
phosis in ant colonies. Stringer et al. (1964) concluded that pest management for the next decade.
ant bait toxicants must exhibit delayed toxicity over at least
10- to 100-fold dosage range, not be repellent when added
to bait, be readily transferred between ants, and kill the Conclusion
recipient. In addition, the delayed toxicity of the toxicant
must not inhibit or prevent trophallaxis. Reemerging pests and environmental challenges are chang-
Even though several toxicants such as hydramethylnon, ing the face of urban pest management. The reemergence of
sulfluramid, abamectin, and fipronil meet all the criteria, the bedbugs and invasive pest species such as the red imported
development of acceptable bait bases for the various spe- fire ant and Argentine ant pose special problems and chal-
cies of pest ants has been problematic. No single bait base lenges to the PMP. There is an increasing database and
is attractive to all pest species of ants. Consequently, special public awareness of the medical importance and role of
bait bases will be needed for different groups of ants. IGRs cockroaches and other arthropods in inducing asthma and
such as fenoxycarb, methoprene, and pyriproxyfen have been related health issues. Environmental monitoring suggests
successfully used to control S. invicta, but little information is that outdoor perimeter treatments used to control ants may
available on other pestiferous species such as Argentine ants, be an important source of insecticides in urban waterways.
odorous house ants, and carpenter ants as reviewed by Klotz This development will likely result in major regulatory
et al. (2008). Baits containing toxicants such as hydrameth- changes and use patterns of insecticides around urban struc-
ylnon provided delayed toxicity (15% mortality at 24 h; tures and present challenges to the PMP and homeowner.
Stringer et al., 1964) of S. invicta workers. However, indoxa- Increasing awareness and environmental concerns of the
carb provided 15, 55, and 100% kill at 9, 24, and 48 h, respec- public have resulted in a movement toward so-called green
tively (Oi and Oi, 2006). Indoxacarb did not provide delayed pest control. As a result, the use of botanicals, fragrance oils,
toxicity and the results clearly suggest that our criteria for ant and inorganic compounds has increased dramatically. Other
baits (based on Stringer et al., 1964) may need to be modified new chemistries such as the neonicotinoids, phenylpyr-
for pro-insecticides like indoxacarb. azoles, and pyrroles have largely replaced the organophos-
phate and some traditional uses of pyrethroid insecticides.
In the future, there will be a continued emphasis on low
environmental impact strategies that incorporate the use of
5.7 Future directions reduced-risk insecticides.
The implementation of IPM programs for the control of
structural pests and regulatory changes will increase in
response to the public’s concerns over insecticide use, the
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