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1684
VOLUME 114 |NUMBER 11 |November 2006
•
Environmental Health Perspectives
Research
Insecticide use in inner-city communities in
the United States is widespread, and resultant
indoor exposures can be extensive (Fenske
et al. 1990; Gurunathan et al. 1998; Lemus
et al. 1998; Whitmore et al. 1994; Whyatt
et al. 2003). In a recent study of African-
American, Latina, and Caucasian mothers and
newborns residing in East Harlem in New
York City, 72% of subjects reported indoor
insecticide exposure during pregnancy to con-
trol cockroaches and other pests. Maternal
urine samples collected on delivery showed
that 55% of subjects had detectable levels of
3,5,6-trichloro-2-pyridinol (TCPy), a metabo-
lite of the organophosphate chlorpyrifos, and
37% had detectable levels of 3-phenoxy-
benzoic acid, a metabolite of pyrethroid insec-
ticides (Berkowitz et al. 2004). In our prior
study of pregnant African-American and Latina
women residing in northern Manhattan and
the South Bronx, 85% of subjects reported that
pest control measures were used during preg-
nancy, and 100% of participants had detectable
airborne exposures to organophosphate and
carbamate insecticides (Whyatt et al. 2003). In
addition, these same insecticides were detected
in 45–74% of blood samples collected from
mothers and newborns at delivery. Insecticide
levels in maternal and newborn blood samples
were similar and highly correlated, suggesting
that placental transfer of these compounds can
occur (Whyatt et al. 2003). Further, the infants
with the highest in utero exposure to the
organophosphate chlorpyrifos had significantly
lowered weight and length at birth and signifi-
cantly poorer mental and motor development
at 3 years of age (Rauh et al., in press; Whyatt
et al. 2004). Experimental evidence has linked
exposure to organophosphate insecticides dur-
ing gestation or the early postnatal period to
adverse neurodevelopmental sequelae in the
offspring (reviewed by both Eskenazi et al.
1999; Landrigan et al. 1999).
Although there is sufficient evidence docu-
menting that residential insecticide use is perva-
sive among African-American and Latino
populations residing in low-income urban
communities in New York City, there is a
paucity of data in the current literature describ-
ing methods to reduce residential insecticide
exposure in these environments. Attempts have
been made to determine the risk factors associ-
ated with pest infestation and resulting insecti-
cide use. A survey of pest control measures
used by residents of public housing in New
York State conducted during 2000–2001 con-
cluded that pest problems and insecticide use
were related to housing disrepair and housing
density (Surgan et al. 2002). Additional evi-
dence has shown that cockroaches and other
household pests thrive in multifamily dwellings
where excessive moisture, cracks and crevices,
and abundant food sources are present
(Brenner et al. 2003). In our prior research, the
proportion of women reporting that pests were
sighted in the home, as well as the proportion
reporting that pest control measures were used
during pregnancy, increased significantly with
the level of disrepair in the home (including
holes and cracks in the walls and ceilings, water
damage, leaky pipes, peeling or flaking paint)
(Whyatt et al. 2002). Women who reported
sighting pests in their home (primarily cock-
roaches and rodents) were significantly more
likely to use pest control measures than women
reporting no pest sightings (chi-square test,
p< 0.001) (Whyatt et al. 2003). Therefore,
effective interventions to reduce pest infestation
levels and residential insecticide exposure must
address aspects of housing quality such as unre-
paired cracks and crevices, leaky pipes, and
food sources.
Integrated pest management (IPM) is con-
sidered an environmentally sustainable pest
control strategy. It aims to reduce pest popula-
tions by identifying and understanding the
biology and behavior of the insects and
rodents; selecting and implementing a set of
environmentally safe and effective control
strategies; and monitoring the effectiveness of
the strategies (Ogg et al. 1995). Techniques
include building repairs to eliminate pest entry
points and breeding sites, cleaning to remove
pest food sources, and the use of low-toxicity,
nonaerosol insecticides including baits, gels,
and boric acid (Ogg et al. 1995). Interventions
Address correspondence to R.M. Whyatt, Department
of Environmental Health Sciences, Mailman School
of Public Health, Columbia University, 60 Haven
Ave., B-109, New York, NY 10032 USA. Telephone:
(646) 459-9609. Fax: (646) 459-9610. E-mail:
rmw5@columbia.edu
We thank the obstetrics/gynecology staffs at Harlem
and New York Presbyterian Hospitals, D. Holmes,
J. Lai, L. Qu, X. Jin, G. Weerasekera, and J. Perez.
This work was supported by the New York City
Council Speaker’s Fund for Public Health Research,
National Institute of Environmental Health Sciences
grants P50 ES09600, RO1 ES08977, and RO1
ES11158; and U.S. Environmental Protection
Agency grants R827027 and R82860901.
The authors declare they have no competing
financial interests.
Received 15 March 2006; accepted 27 July 2006.
An Intervention to Reduce Residential Insecticide Exposure during Pregnancy
among an Inner-City Cohort
Megan K. Williams,1Dana B. Barr,2David E. Camann,3Linda A. Cruz,1Elizabeth J. Carlton,1Mejico Borjas,1
Andria Reyes,1Dave Evans,1Patrick L. Kinney,1Ralph D. Whitehead Jr.,2Frederica P. Perera,1
Stephen Matsoanne,4and Robin M. Whyatt1
1Columbia Center for Children’s Environmental Health, Mailman School of Public Health, Columbia University, New York, New York, USA;
2National Center for Environmental Health, Centers for Disease Control and Prevention, Atlanta, Georgia, USA; 3Southwest Research
Institute, San Antonio, Texas, USA; 4Department of Obstetrics and Gynecology, Columbia University, New York, New York, USA
BACKGROUND:We previously reported widespread insecticide exposure during pregnancy among
inner-city women from New York City. Here we report on a pilot intervention using integrated pest
management (IPM) to reduce pest infestations and residential insecticide exposures among pregnant
New York City African-American and Latina women (25 intervention and 27 control homes).
METHODS:The IPM consisted of professional cleaning, sealing of pest entry points, application of
low-toxicity pesticides, and education. Cockroach infestation levels and 2-week integrated indoor air
samples were collected at baseline and one month postintervention. The insecticides detected in the
indoor air samples were also measured in maternal and umbilical cord blood collected at delivery.
RESULTS:Cockroach infestations decreased significantly (p = 0.016) after the intervention among
intervention cases but not control households. Among the intervention group, levels of piperonyl
butoxide (a pyrethroid synergist) were significantly lower in indoor air samples after the interven-
tion (p = 0.016). Insecticides were detected in maternal blood samples collected at delivery from
controls but not from the intervention group. The difference was significant for trans-permethrin
(p = 0.008) and of borderline significance (p = 0.1) for cis-permethrin and 2-isopropoxyphenol
(a propoxur metabolite).
CONCLUSION: To our knowledge, this is the first study to use biologic dosimeters of prenatal pesti-
cide exposure for assessing effectiveness of IPM. These pilot data suggest that IPM is an effective
strategy for reducing pest infestation levels and the internal dose of insecticides during pregnancy.
KEY WORDS:insecticides, integrated pest management, intervention, prenatal, residential. Environ
Health Perspect 114:1684–1689 (2006). doi:10.1289/ehp.9168 available via http://dx.doi.org/
[Online 27 July 2006]
that have included IPM-like practices have
been endorsed by the National Institutes of
Health (1997), and several studies have docu-
mented the ability of IPM interventions to
reduce pest populations, allergen levels, and
asthma morbidity (Arbes et al. 2003; Brenner
et al. 2003; Morgan et al. 2004; Wood et al.
2001). However, only limited data address the
effectiveness of IPM interventions at reducing
residential insecticide exposure (Campbell et al.
1999; Kass and Outwater, 2001).
The current study is the first to use bio-
markers and air monitoring to document
changes in insecticide exposure after an IPM
intervention. The IPM strategy used here was
adapted from the Columbia Intervention to
Reduce Indoor Allergens Study (Kinney et al.
2002). The aim of this study was to assess the
feasibility of reducing prenatal exposures to
pests and insecticides through an IPM inter-
vention that included professional cleaning,
building repairs, sealing pest entry points, pro-
fessional insecticide placement, and one-on-
one education.
Study Design and Methods
Subject recruitment. Intervention group.
Recruitment and enrollment efforts for the
intervention study occurred from August 2002
through April 2004. Thirty women were
recruited from obstetrics and gynecology
(OB/GYN) clinics located in New York
Presbyterian and Harlem Hospitals. Eligibility
was restricted to women 18–35 years of age
who self-identified as either African American
or Latina (Dominican or Puerto Rican) and
reported using high-toxicity insecticides (use of
exterminators, can sprays, and/or pest bombs)
during pregnancy. Further, eligible subjects
must have resided in northern Manhattan
(north of 110th Street) or the South Bronx
(south of Fordham Road) for at least 1 year
before pregnancy and must not be planning to
move from the community before delivery.
From the 30 subjects who completed the
screening and consent forms, 5 women
dropped from the study between enrollment
and monitoring (2 women gave birth before
the intervention was completed, 1 experienced
health problems restricting her participation,
and 2 moved out of the community). Samples
collected from the subjects before the interven-
tion will be referred to as preintervention, and
samples collected after the intervention will be
referred to as postintervention. From the
remaining 25 women, 25 (100%) completed
the prenatal questionnaire, 25 (100%) partici-
pated in pre- and postintervention indoor air
monitoring, and biologic samples were col-
lected from 21 (84%) subjects. Nineteen
(76%) completed pre- and postintervention
assessment of pest infestation.
Control group. The control group was
selected from participants in an ongoing
prospective cohort study designed to validate
biomarkers of prenatal insecticide exposure. As
part of this study, insecticide levels were meas-
ured in 2-week integrated indoor air samples
collected continuously over the last 2 months
of pregnancy. Blood samples were collected
from the mother and newborn at delivery.
Enrollment for this study occurred in the
OB/GYN clinics located in New York
Presbyterian Hospital and Harlem Hospital
from October 2001 through July 2004. The
recruitment strategy and eligibility criteria for
the controls were identical to those for the
cases. From the total of 110 women fully
enrolled in the biomarker validation study, 27
were selected as controls for the intervention
study. Control selection aimed to match case
subjects on year of enrollment (2002–2004)
and self-reported use of high-toxicity insecti-
cides (use of exterminators, can sprays, and/or
pest bombs) during pregnancy. Baseline and
follow-up integrated air samples were selected
to match the pre- and postintervention sam-
ples in the cases. Questionnaire data were
available for 100% of subjects. Baseline and
follow-up indoor air data were available for 24
(88%) subjects; blood samples were collected
from 17 (63%) subjects. Fourteen (52%) sub-
jects completed the initial pest infestation lev-
els. Follow-up samples were available for only
six (22%) subjects.
The institutional review board of the
Columbia Presbyterian Medical Center
approved the study, and we obtained written
informed consent from all study subjects.
Intervention. The intervention commenced
at the conclusion of the 2-week preintervention
monitoring period. This IPM consisted of three
main components: an extensive cleaning with
minor building repairs, a low-toxicity insecti-
cide application, and behavioral/health educa-
tion. The kitchen, bathroom, and living room
areas of the intervention apartments were pro-
fessionally cleaned using low-toxicity, citrus-
based cleaning products. Pest entry points were
sealed with caulking compounds and/or metal
screens. A professional insecticide placement
company injected low-toxicity insecticides,
2.15% hydramethylnon (MAXFORCE;
Maxforce Insect Control Systems, Oakland,
CA), or small amounts of boric acid directly
into the cracks and holes before sealing and
placed glue traps for cockroaches throughout
the kitchen, bathroom, and problem areas.
Hydramethylnon has low toxicity and low
vapor pressure and has been shown previously
to be effective for long-term cockroach control
(Appel 1992). Using a checklist prepared for
the Columbia Intervention to Reduce Indoor
Allergens Study, the health educator assessed
the frequency and location of pest sightings and
tailored the health education accordingly for
each participant. After the cleaning, a health
educator met with the family to discuss IPM
strategies for pest control. Training sessions
targeted as many household members as possi-
ble and strongly emphasized a team effort.
Strategies included removing garbage from the
home each day, eating meals only in the
kitchen, and cleaning up dishes and food spills
as soon as possible. In addition, the program
included education and instruction regarding
nontoxic pest control methods. Airtight con-
tainers for food and trash storage were provided
to each household. The intervention cleaning
and behavioral training took place over
approximately 2–3 days. The control group
did not receive an IPM intervention, nor did
they receive a placebo intervention. However,
all subjects in the biomarker validation study,
including those selected as controls for the cur-
rent study, received written material on the
importance of reducing insecticide use in the
home and techniques for controlling pests
without using higher toxicity insecticides.
Sample collection. Questionnaire data. A
45-minute questionnaire was administered to
the intervention and control groups in each
woman’s home by a trained bilingual inter-
viewer during the third trimester of pregnancy.
The questionnaire included information on
demographics, home characteristics including
housing disrepair and pest infestation levels,
lifetime residential history, history of active and
passive smoking, occupational history, maternal
education and income level, alcohol and drug
use during pregnancy, and history of residential
insecticide use. Information about insecticide
use included whether or not any pest control
measures were used by an exterminator or by
others (the woman herself, other household
members, or the building superintendent) dur-
ing pregnancy and, if so, what types of meas-
ures were used and at what frequency (Perera
et al. 2003; Whyatt et al. 2002, 2003).
Indoor air monitoring. Before the inter-
vention, a baseline 2-week integrated indoor
air sample was collected from the homes of
subjects in the intervention and control
groups. Monitoring commenced in each home
at the end of the second or beginning of the
third trimester of pregnancy using a BGI
pump with a 0.5-L/min flow-rate (BGI, Inc.,
Waltham, MA). The pump was attached to a
URG (University Research Group, Chapel
Hill, NC) polyurethrane foam (PUF) sampler
with a 2.5-µm inlet cut fitted with a 30-mm
quartz fiber filter and a foam cartridge backup
to capture semivolatile vapors and aerosols. The
pumps were attached to a battery and operated
continuously over the 2 weeks. The monitoring
equipment was placed in the main living area of
the apartment, with the pump in a secure box
and the sampler (located inside a protective
wire cage) placed at least 60 cm from wall sur-
faces at a height of 135 cm. The sampler height
was chosen to represent the average between the
woman’s sitting and standing heights, because
Intervention to reduce residential pesticide use
Environmental Health Perspectives
•
VOLUME 114 |NUMBER 11 |November 2006
1685
residential insecticide air concentrations have
been shown to vary with height, being greatest
near the floor (Aprea et al. 2000; Fenske et al.
1991). Study subjects were instructed on the
importance of not disturbing the equipment
and told to go about their daily activity as nor-
mal. The research staff returned after 2 weeks
to collect the equipment, perform a leak
check, and record the pump flow-rates. A
careful log was kept of elapsed time on the
pump meter and of rotometer readings and
leak check results at each visit. The monitor-
ing strategies for intervention and control
homes were identical. Prior quality control
analyses indicated that there would be no dan-
ger of insecticide breakthrough with this mon-
itoring protocol (Camann and Whyatt 2001).
Approximately 4 weeks after the interven-
tion, a follow-up 2-week integrated indoor air
sample was collected from intervention and
control homes. Protocols for the follow-up air
monitoring were identical to those for the base-
line sample. The monitoring was targeted to
occur during the 38th to 40th week of preg-
nancy; however, because of premature births or
postponements, some subject’s homes were
monitored immediately after delivery.
Cockroach infestation levels. To monitor
cockroach infestation levels, six pheromone
glue traps (Victor Roach Pheromone Traps;
Woodstream, Lititz, PA) were placed in stan-
dardized locations throughout the kitchens of
each subject during the 2-week baseline and
follow-up indoor air monitorings. After
2 weeks, traps were collected and the number
of adult and nymph cockroaches caught in
each trap was counted.
Maternal and cord blood. We used blood
collection procedures validated in our prior
research studies to ensure that blood samples
(maternal and/or umbilical cord) were collected
from women in the intervention and control
groups at delivery (Whyatt et al. 2003). A sam-
ple of infant cord blood was collected by deliv-
ery room staff immediately after the cord was
cut and the placenta delivered. Infant cord
blood was obtained by syringing the blood into
heparinized syringes at the point the cord enters
the placenta. A sample of maternal blood
(30–35 mL) was obtained within 1–2 days
postpartum by the research staff or by hospital
staff. A member of the research staff transported
the blood samples to the biomarker laboratory
located at Columbia University, New York
City, immediately after collection. Within 12
hr of blood collection, the cord and maternal
bloods were transferred to centrifuge tubes and
spun for 15 min at 1,500 rpm. Plasma samples
were collected and stored at –70°C before ship-
ment to the Centers for Disease Control and
Prevention (CDC) for insecticide analysis.
Pesticide analysis. Pesticides in air
monitoring filters. Analysis of insecticides
in the 2-week integrated indoor air samples
was conducted by Southwest Research
Institute under the direction of D. Camann.
Immediately after each 2-week collection
period, air monitoring filters were brought to
the laboratory at the Columbia Children’s
Center for Environmental Health, inventoried
and stored at 20°C. Every 4–6 weeks, air sam-
ples were shipped to Southwest Research
Institute. The entire PUF plug and filter was
placed in a Soxhlet extractor, spiked with ter-
phenyl-d
14
as a recovery surrogate, extracted
with 6% diethyl ether in hexane for 16 hr and
concentrated to 1.0 mL in 10% ether in hexa-
nes. Extracts were stored frozen below –4°C.
Insecticides are stable in the extract under these
conditions. We determined the amounts of the
target insecticides in samples using Agilent
6890/5973 gas chromatography/mass spec-
trometry (Agilent, Wilmington, DE) in selected
ion mode. Paired pre- and postintervention air
samples were available on 25 cases and 39 con-
trols. The target insecticides that were measured
in the indoor air samples were bendiocarb, car-
baryl, carbofuran, cis- and trans-permethrin,
malathion, methyl parathion and propoxur. In
addition, piperonyl butoxide, a synergist added
to natural and synthetic pyrethroid insecticides,
was measured as an indicator of pyrethroid
insecticides. Chlorpyrifos and diazinon were
not assessed because most of the women were
enrolled in the study after the federal ban on
their residential use and our prior data indicate
that the ban was effective at reducing use and
exposures to these insecticides among inner-city
women in New York City (Carlton et al. 2004;
Whyatt et al. 2003, 2004).
Pesticides in plasma samples. Analysis of
the insecticides or their metabolites in mater-
nal and cord plasma was conducted by the
CDC under the direction of D. Barr using
isotope dilution gas chromatography–high reso-
lution mass spectrometry (Barr et al. 2002).
Approximately 10–15% of all samples assayed
were positive or negative control samples. Two
concentrations of positive control samples were
Williams et al.
1686
VOLUME 114 |NUMBER 11 |November 2006
•
Environmental Health Perspectives
Table 1. Distribution of maternal sociodemographic
characteristics gathered from questionnaires
administered on recruitment (intervention group,
n
= 25; control group,
n
= 27).
Characteristic Intervention (%) Control (%)
Age [years (range)] 26.6 (19–36) 24.3 (18–36)
Education
a
< High school diploma 28.0 55.6
High school diploma or 28.0 37
equivalent
> High school diploma 44.0 7.4
Race/ethnicity
Latina 76.0 59.3
African American 20.0 37.0
Marital status
Married 12.0 22.0
Never married 72.0 66.7
Divorced/separated 16.0 11.1
Income
< $10,000 44.0 41.7
$10,000–30,000 40.0 45.8
> $30,000 12.0 12.3
Housing conditions
Holes in ceiling/walls
a
75.0 48.1
Unrepaired water damage 40.0 22.2
Leaky pipes
a
42.0 11.1
Year of delivery
2002 28.0 44.4
2003 68.0 33.3
2004 4.0 22.2
Season of delivery
January–March 20 30.8
April–June 8 23.1
July–September 40 15.4
October–December 32 30.8
Missing information for the two groups includes, for inter-
vention, race/ethnicity (1), income (1), unrepaired water
damage (1), leaky pipes (1); for control, income (3), season
of delivery (1).
a
Pearson’s chi-square test,
p
< 0.05.
Table 2. Reported pest infestation levels and pesti-
cide use assessed from prenatal questionnaires
administered on recruitment (intervention group,
n
= 25; control group,
n
= 27).
Affirmative (%)
Questionnaire Intervention Control
Reported roaches 91.7 85.2
Reported exposure to high- 100 100
toxicity pest control measures:
Spray by exterminator 47.8 40.7
Can spray 73.9 76.9
Pest bomb 31.8 15.4
Missing information for the two groups includes, for inter-
vention, reported roaches (1), spray by exterminator (2),
can spray (2), pest bomb (2); for control, can spray (1), pest
bomb (1).
Figure 1. Cockroach infestation levels. (
A
) Mean (± SE) cockroaches (adults + nymphs) in traps collected
over 2 weeks pre- (Pre) and postintervention (Post). Intervention group: preintervention (
n
= 22), post-
intervention (
n
= 19); control group: preintervention (
n
= 14), postintervention (
n
= 6). (
B
) Percent reduction
between total cockroaches in traps collected over 2 weeks pre- and postintervention. Intervention
(
n
= 19), control (
n
= 6). Comparison of differences in percent reduction in pest infestation levels between
the intervention and control groups, group
t
-test,
p
= 0.1 (
B
).
*Wilcoxon signed-rank test,
p
= 0.016.
Intervention Control
250
200
150
100
50
0Intervention Control
50
40
30
20
10
0
–10
Total cockroaches
Percent reduction in
total cockroaches
AB
*
Pre
Post
47%
–0.3%
used: one spiked at the mid-calibration range
and one at the low-calibration range. A set of
blinded positive control samples was also run,
which an independent quality assurance officer
evaluated. CDC provided results on insecticide
levels in maternal blood samples for 21 cases
and 32 controls and from umbilical cord blood
for 13 cases and 20 controls. The target insecti-
cides that were analyzed in blood were those
that corresponded to the insecticides detected
in the indoor air samples, and included the
parent compounds for cis-permethrin and
trans-permethrin as well as the metabolite of
propoxur, 2-isopropoxyphenol.
Statistical analysis. For both environmen-
tal and biologic monitoring data, we assigned
samples less than the limit of detection
(LOD) a value of 0.5 ×LOD. For hypothesis
testing, variables were treated as continuous or
categorical depending on their distributional
properties. Continuous variables were initially
log-transformed as appropriate to normalize the
distribution. However, in almost all cases, the
data could not be normally distributed after
log-transformation, so nonparametric statistics
were used. The differences in pest infestation
levels and air insecticide levels between pre- and
postintervention in both cases and controls
were normally distributed, so we used para-
metric statistics to evaluate whether these dif-
ferences varied significantly between the
intervention and control group. Analyses were
also undertaken to determine whether the inter-
vention and control groups differed in terms of
demographic characteristics or season and year
of delivery. No significant differences were seen.
For pest infestation levels, we used the
Wilcoxon signed-rank test to assess the differ-
ences between pre- and postintervention pest
infestation levels in both intervention and con-
trol groups. Because the differences in pest
infestation levels were normally distributed, we
used the independent sample t-test to deter-
mine whether the differences in pest infestation
levels between pre- and postintervention
observed in the intervention group were signifi-
cantly different from the differences in pest
infestation levels observed in the control group.
For 2-week integrated air insecticide levels,
we compared detection frequencies as well as
detection levels. We used McNemar’s test to
examine the change in detection frequency of
insecticide levels in air between pre- and
postintervention in both the intervention and
control groups. We used the Wilcoxon signed-
rank test to examine the change in insecticide
levels between pre- and postintervention for
both groups. Finally, we used the independent
sample t-tests and regression analyses control-
ling for race/ethnicity, season, and year of
delivery to compare whether the change in air
insecticide levels between pre- and postinter-
vention differed significantly between the
intervention and control groups. For insecti-
cide levels in maternal and cord blood samples,
we compared differences in detection frequen-
cies between intervention and control subjects
using chi-square analyses (Fisher’s exact test).
Results were considered significant at p< 0.05
(two-tailed).
Results
Study participants. Participants included 25
intervention cases and 27 nonintervention con-
trols. Demographic characteristics were com-
pared between cases and controls and were
generally comparable between the two groups
(Table 1). Discrepancies between the groups
were limited to education and housing condi-
tions (holes in ceilings and walls and leaky
pipes) (Pearson’s chi-square test, p= 0.008,
0.05, and 0.012, respectively). Table 2
describes reported insecticide use and pest
infestation levels in the intervention and control
groups. According to the prenatal questionnaire
and in compliance with eligibility criteria,
100% of the intervention and control subjects
reported exposure to high-toxicity insecticides
during pregnancy either through spray by an
exterminator, personal (or household) use of
spray insecticides, and/or use of a pest bomb.
Patterns of insecticide use and reported pest
infestation levels were not different between the
two groups. Most of both intervention and
control subjects reported seeing cockroaches in
their homes (91.7 and 85.2%, respectively).
More than 50% of both groups reported seeing
cockroaches in their homes on a daily basis.
Pest infestation levels. Pest traps placed in
the subjects’ homes for a 2-week collection
period before the intervention revealed that
adult cockroaches were present at baseline in
77% of the intervention group and 86% of
the control group. Figure 1A displays the total
number of cockroaches (adult and nymph)
collected in traps pre- and postintervention
from case and control households. At baseline,
the mean (± SE) adult cockroach count was
higher in the intervention than in control sub-
jects (27.6 ± 6.8 vs. 11.9 ± 3.1, respectively).
At baseline, nymph cockroaches were found in
82% of intervention homes and 93% of control
homes and nymph counts were higher in the
intervention than in the controls (148.6 ± 32.5
vs. 76.6 ± 21.1). We assessed the effectiveness
of the intervention by comparing the differ-
ences in pre- and postintervention roach counts
within and between intervention and control
subjects. Overall, there was a 47% decrease in
total cockroach infestation among intervention
households after the intervention (Wilcoxon
signed-rank test, p = 0.016) (Figure 1B). Adult
cockroaches decreased by 60% (p= 0.006)
and nymph cockroaches decreased by 44%
(p= 0.033). By contrast, control households
showed no significant reduction of adult or
nymph cockroaches between baseline and fol-
low-up (see Figure 1A). However, the differ-
ences between the preintervention compared
with postintervention total, nymph, and adult
cockroach levels were not significantly greater
in the intervention group than in the control
group (Figure 1B).
Air samples. Of the nine insecticides meas-
ured in 2-week integrated indoor air samples,
five insecticides (bendiocarb, carbaryl, carbo-
furan, malathion, and methyl parathion) were
not detected or were found in < 10% of either
intervention or control samples. Of the
remaining insecticides, propoxur was detected
in 92% of pre- and postintervention case sam-
ples and 100% of baseline and follow-up con-
trol samples; and cis- and trans-permethrin
in approximately 30% of pre- and 15% of
postintervention samples and 24 and 16% of
baseline control samples and 17 and 13% of
follow-up control samples, respectively. In
addition, piperonyl butoxide was detected in
71% of pre- and postintervention samples and
72 and 57% of baseline and follow-up control
samples, respectively. The mean levels for
these compounds in pre- and postintervention
2-week integrated indoor air samples are pre-
sented in Table 3.
Among the intervention group, only piper-
onyl butoxide decreased significantly after the
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Table 3. Pre- and postintervention levels of pesticides measured in 2-week integrated indoor air samples (ng/m3) collected from intervention group and control
group from African-American and Latina subjects residing in northern Manhattan and the South Bronx.
Intervention (
n
= 25) Control (
n
= 24)
Wilcoxon signed-rank test Wilcoxon signed-rank test
LOD Preintervention Postintervention Negative Positive Preintervention Postintervention Negative Positive
Pesticide (ng/m3) (mean ± SE) (mean ± SE) ranks
a
ranks
b
Ties
p
-Value (mean ± SE) (mean ± SE) ranks
a
ranks
b
Ties
p
-Value
Propoxur 0.2 49.3 ± 19.0 56.8 ± 24.2 11 11 0 0.592 45.6 ± 10.9 36.9 ± 8.3 14 10 0 0.081
Piperonyl butoxide 0.2 1.66 ± 0.71 0.80 ± 0.22 17 6 0 0.016 6.12 ± 3.8 3.5 ± 2.2 14 9 1 0.089
cis-
Permethrin 0.4 1.54 ± 0.85 1.25 ± 0.60 14 11 1 0.510 1.84 ± 1.48 0.99 ± 0.63 9 13 2 0.758
trans
-Permethrin 0.7 2.60 ± 1.45 1.9 ± 0.96 13 11 0 0.475 2.75 ± 2.2 1.66 ± 1.0 9 15 0 0.338
Missing information includes, for intervention, propoxur (3), piperonyl butoxide (2),
trans
-permethrin (1).
a
Levels were lower in follow-up compared with baseline.
b
Levels were higher in follow-up compared with baseline.
intervention (Table 3 and Figure 2A). The
mean level of piperonyl butoxide in interven-
tion homes decreased by 50% (Wilcoxon
signed-rank test, p= 0.016). Of the 23 inter-
vention homes with available air sampling, a
decrease in piperonyl butoxide was seen in 74%
(17/23) of homes, whereas an increase was seen
in 26% (6/23) of homes. Piperonyl butoxide
levels also decreased in control homes, but not
significantly (p= 0.08). The difference between
pre- and postintervention levels of piperonyl
butoxide in the intervention group was not
significantly different from the difference
between baseline to follow-up levels in the
controls (independent sample t-test, p= 0.3,
Figure 2B). Levels of the pyrethroid insecti-
cides cis-permethrin and trans-permethrin
decreased in follow-up compared with baseline
air samples in most intervention homes and
increased in most control homes (see negative
and positive ranks in Table 3), but these dif-
ferences were not significant. Propoxur levels
decreased nonsignificantly from baseline to
follow-up among control homes only
(Wilcoxon signed-rank test, p= 0.08).
Biologic samples. Table 4 shows the levels
of insecticides that were measured in maternal
plasma samples. These included 2-iso-
propoxyphenol (metabolite of propoxur) and
cis- and trans-permethrin (two isomers of the
pyrethroid insecticide permethrin). These
insecticides were detected in plasma samples
from the control group but not from the inter-
vention group. Specifically, 2-isopropoxy-
phenol was detected in 0% of maternal blood
samples from the intervention group and in
12% of maternal blood samples from controls
(chi-square, p = 0.1). Cis- and trans-permethrin
were detected in 0% of maternal blood samples
from intervention group and 12 and 29% of
maternal blood samples from controls, differ-
ences that were significant for trans-permethrin
(chi-square, p = 0.008) (Table 4). None of
these three pesticides were present at levels
greater than LOD in either intervention or
control cord blood samples.
Discussion
This pilot intervention study demonstrates that
IPM can have a significant effect on pest infes-
tation levels and appears to reduce residential
insecticide exposures during pregnancy. Our
findings showing significant reductions in
cockroach populations are consistent with
those of other intervention studies that focused
on reducing either pest infestations or allergen
levels related to pest infestation (Arbes et al.
2003; Brenner et al. 2003; Kass and Outwater
2001; McConnell et al. 2003; Wood et al.
2001). To our knowledge, however, no other
studies have demonstrated reductions in pesti-
cide exposure using biologic and environmen-
tal measures of insecticide exposure.
Success of IPM interventions has been
attributed to simultaneous application of mul-
tiple nonchemical approaches to pest control,
including education, repair, least-toxic exter-
minations, reinforcement, and repetition
(Brenner et al. 2003). In our study, attention
was focused on problem areas in the house
including the kitchen, bathroom, and main
living space. In addition to repairing the
cracks and holes present in the home, we per-
formed an extensive cleaning to remove food
debris, grease stains, and general clutter.
Airtight containers were provided for food
storage, and individualized education plans
were developed for each home that targeted
high-risk behaviors. We conclude that the
intervention was successful at reducing cock-
roaches based on data from pest traps placed
in the subjects’ homes for 2-week periods
immediately before and approximately
1 month after the intervention. Cockroach
infestation levels in intervention households
declined by more than one-third, whereas
cockroach levels in the control households
remained unchanged.
Despite the dual goal of IPM to reduce
cockroach and insecticide exposures, most IPM
evaluations have focused on the reduction of
pests. Data on the effectiveness of reducing
insecticide exposure are limited, and docu-
mented in only two studies. A building-wide
intervention in New York City public housing
found resident’s use of spray insecticides and
Chinese Chalk, an illegal insecticide, dropped
to zero after a building-wide IPM intervention
that included education about the safe use of
insecticides (Kass DE, Outwater T, unpub-
lished data). An IPM intervention in Canada
found decreases in both personal use of spray
insecticides and resident requests for extermi-
nators to use spray insecticides in their apart-
ment, requesting instead lower-toxicity pastes
or gels (Campbell et al. 1999). Although these
findings are encouraging, they rely on resident-
reported insecticide use after educational ses-
sions and do not include objective measures
of insecticide exposures. The current study is
the first to use indoor air monitoring and bio-
markers to document changes in insecticide
exposure after an IPM intervention.
In the present study, target insecticides in
indoor air samples included the carbamate,
propoxur, the pyrethroids cis-permethrin and
trans-permethrin, and the pyrethroid synergist
piperonyl butoxide. Selection of these insecti-
cides was based on evidence that they were
widely used for residential pest control (Whyatt
et al. 2003). Detection frequencies and mean
levels of these insecticides in the current study
were similar to those previously documented in
this population (Whyatt et al. 2003, 2004). To
assess the effectiveness of the IPM, levels of resi-
dential insecticides were measured in 2-week
integrated indoor air samples collected before
and after implementation of the IPM and com-
pared with those for a control population. The
effectiveness of the IPM on reducing indoor air
levels of residential insecticides can be discerned
from trends in piperonyl butoxide. Piperonyl
butoxide is a compound added to many
pyrethroid formulations to delay metabolic
degradation of the active ingredients and
enhance insecticidal properties. It is not used in
other products and is more volatile than the
pyrethroids themselves, so they can be reliably
measured in air samples as an indicator of
pyrethroid insecticide use. It has been suggested
that pyrethroid insecticides are being used to
replace the recently restricted organophosphates
Williams et al.
1688
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•
Environmental Health Perspectives
Table 4. Pesticide levels (pg/g) in maternal plasma samples collected at delivery in intervention group
(
n
= 21) and in control group (
n
= 17).
Pesticide LOD Intervention (% > LOD) Control (% > LOD) Chi-square
p
-value
a
2-Isopropoxyphenol 1.50 0 11.8 0.106
cis-
Permethrin 0.50 0 11.8 0.106
trans
-Permethrin 0.50 0 29.4 0.008
Missing information includes, for controls,
cis
-permethrin (1),
trans
-permethrin (1).
a
Difference in detection frequency between intervention and control groups.
Figure 2. Piperonyl butoxide in 2-week integrated air samples. (
A
) Changes in mean (± SE) piperonyl butoxide
levels in 2-week integrated indoor air samples collected over 2 weeks before and 2 weeks after the inter-
vention. Intervention (
n
= 23), control (
n
= 24). (
B
) Percent reduction in piperonyl butoxide levels between
2-week integrated indoor air samples collected over 2 weeks before and 2 weeks after the intervention.
Intervention (
n
= 23), control (
n
= 24). Comparison of differences in percent reduction in piperonyl butoxide
levels between the intervention and control groups, group
t
-test,
p
= 0.3) (
B
).
*Wilcoxon signed-rank test,
p
= 0.016.
Intervention Control
9
8
7
6
5
4
3
2
1
0Intervention Control
60
50
40
30
20
10
0
Piperonyl butoxide ng/m3
Percent reduction in
piperonyl butoxide
AB
*
Pre
Post
52%
42%
Intervention to reduce residential pesticide use
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VOLUME 114 |NUMBER 11 |November 2006
1689
chlorpyrifos and diazinon (Surgan et al. 2002).
In our study, among the intervention house-
holds, detection frequencies and levels of piper-
onyl butoxide decreased significantly after the
intervention. This decreasing trend was not sig-
nificant in the control households. Further, the
data suggest that the intervention may have
been particularly effective at reducing exposure
to the pyrethroid insecticides. Levels of the
trans-isomer of permethrin were lower in
maternal plasma samples collected from the
intervention group than in controls.
However, these findings should be inter-
preted with caution, particularly because results
for propoxur do not mirror those seen for
piperonyl butoxide. Specifically, propoxur levels
in indoor air samples decreased in follow-up
compared with baseline air samples among con-
trol households, but not among intervention
households. Propoxur is a carbamate licensed
for residential pest control and has not been
subject to regulatory restrictions, as have the
organophosphates, chlorpyrifos, and diazinon.
However, our prior data suggest that propoxur
use in inner-city communities in New York
City may be decreasing. Specifically, we found
a highly significant decrease in propoxur levels
between 1999 and 2001 in personal air sam-
ples collected from African-American and
Dominican women in New York City during
pregnancy and in the corresponding blood
samples collected from the mothers and new-
borns at delivery (Whyatt et al. 2003, 2004).
Unfortunately, no data are available comparing
frequencies of pyrethroid versus propoxur use
in these communities.
Although this pilot intervention indicated
that IPM is effective at reducing pest infestation
and the internal dose of the insecticides during
pregnancy, limitations in the study design
should be noted. The primary limitation of the
study is the small sample size and the short time
elapsed between pre- and postintervention
monitoring. Many intervention studies allow
6 months to 1 year between samplings to deter-
mine if the intervention is both successful and
sustainable. However, the current intervention
was conducted during pregnancy and was thus
limited in follow-up time. Further, the controls
were selected from an ongoing biomarker vali-
dation study that followed women only during
pregnancy. Thus we were not able to evaluate
the sustainability of the intervention over an
extended period. In addition, the optimal
design for an intervention study is to match the
intervention subjects to control subjects and
have all data collected and analyzed simultane-
ously. This was not possible here because the
controls were selected from ongoing research.
However, the intervention and control groups
were comparable in terms of years of enroll-
ment and self-reported pesticide use.
A principal goal of the pilot study was to
assess whether environmental and biologic
measures can be used in evaluating the efficacy
of IPM interventions in reducing residential
pesticide exposures. These initial results are
promising, although additional research is war-
ranted given the small sample size and inconsis-
tency in some of the findings. Environmental
measures for the targeted pesticides are not nec-
essarily associated with the biologic measures.
Therefore, a lack of meaningfully different
results in air levels of pesticides between the
intervention and control groups does not influ-
ence the expected results in maternal plasma
between the two groups. Subsequent research
could also draw on our study design to devise
an IPM intervention that can be conducted by
household members themselves and that is both
feasible and affordable. Such an intervention
could be applied to entire apartment buildings
or complexes to determine the effects of larger-
scale interventions, as opposed to individual
units. In the current study, cleaning and home
repairs were completed by a professional clean-
ing crew to allow comparability and consis-
tency. However, the supplies and techniques
are similar to those available in the community.
In conclusion, we believe that this intervention
protocol using IPM can be successfully adapted
for use by individuals within households in this
community to reduce pest infestation levels and
residential pesticide exposure.
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