1684 VOLUME 114 | NUMBER 11 | November 2006 • Environmental Health Perspectives

Research

Insecticide use in inner-city communities inthe United States is widespread, and resultantindoor exposures can be extensive (Fenskeet al. 1990; Gurunathan et al. 1998; Lemuset al. 1998; Whitmore et al. 1994; Whyattet al. 2003). In a recent study of African-American, Latina, and Caucasian mothers andnewborns residing in East Harlem in NewYork City, 72% of subjects reported indoorinsecticide exposure during pregnancy to con-trol cockroaches and other pests. Maternalurine samples collected on delivery showedthat 55% of subjects had detectable levels of3,5,6-trichloro-2-pyridinol (TCPy), a metabo-lite of the organophosphate chlorpyrifos, and37% had detectable levels of 3-phenoxy-benzoic acid, a metabolite of pyrethroid insec-ticides (Berkowitz et al. 2004). In our priorstudy of pregnant African-American and Latinawomen residing in northern Manhattan andthe South Bronx, 85% of subjects reported thatpest control measures were used during preg-nancy, and 100% of participants had detectableairborne exposures to organophosphate andcarbamate insecticides (Whyatt et al. 2003). Inaddition, these same insecticides were detectedin 45–74% of blood samples collected frommothers and newborns at delivery. Insecticidelevels in maternal and newborn blood sampleswere similar and highly correlated, suggesting

that placental transfer of these compounds canoccur (Whyatt et al. 2003). Further, the infantswith the highest in utero exposure to theorganophosphate chlorpyrifos had significantlylowered weight and length at birth and signifi-cantly poorer mental and motor developmentat 3 years of age (Rauh et al., in press; Whyattet al. 2004). Experimental evidence has linkedexposure to organophosphate insecticides dur-ing gestation or the early postnatal period toadverse neurodevelopmental sequelae in theoffspring (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 Latinopopulations residing in low-income urbancommunities in New York City, there is apaucity of data in the current literature describ-ing methods to reduce residential insecticideexposure in these environments. Attempts havebeen made to determine the risk factors associ-ated with pest infestation and resulting insecti-cide use. A survey of pest control measuresused by residents of public housing in NewYork State conducted during 2000–2001 con-cluded that pest problems and insecticide usewere related to housing disrepair and housingdensity (Surgan et al. 2002). Additional evi-dence has shown that cockroaches and other

household pests thrive in multifamily dwellingswhere excessive moisture, cracks and crevices,and abundant food sources are present(Brenner et al. 2003). In our prior research, theproportion of women reporting that pests weresighted in the home, as well as the proportionreporting that pest control measures were usedduring pregnancy, increased significantly withthe level of disrepair in the home (includingholes and cracks in the walls and ceilings, waterdamage, leaky pipes, peeling or flaking paint)(Whyatt et al. 2002). Women who reportedsighting pests in their home (primarily cock-roaches and rodents) were significantly morelikely to use pest control measures than womenreporting no pest sightings (chi-square test,p < 0.001) (Whyatt et al. 2003). Therefore,effective interventions to reduce pest infestationlevels and residential insecticide exposure mustaddress aspects of housing quality such as unre-paired cracks and crevices, leaky pipes, andfood sources.

Integrated pest management (IPM) is con-sidered an environmentally sustainable pestcontrol strategy. It aims to reduce pest popula-tions by identifying and understanding thebiology and behavior of the insects androdents; selecting and implementing a set ofenvironmentally safe and effective controlstrategies; and monitoring the effectiveness ofthe strategies (Ogg et al. 1995). Techniquesinclude building repairs to eliminate pest entrypoints and breeding sites, cleaning to removepest 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, Departmentof Environmental Health Sciences, Mailman Schoolof Public Health, Columbia University, 60 HavenAve., 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 Harlemand 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 CityCouncil Speaker’s Fund for Public Health Research,National Institute of Environmental Health Sciencesgrants P50 ES09600, RO1 ES08977, and RO1ES11158; and U.S. Environmental ProtectionAgency grants R827027 and R82860901.

The authors declare they have no competingfinancial interests.

Received 15 March 2006; accepted 27 July 2006.

An Intervention to Reduce Residential Insecticide Exposure during Pregnancyamong an Inner-City Cohort

Megan K. Williams,1 Dana B. Barr,2 David E. Camann,3 Linda A. Cruz,1 Elizabeth J. Carlton,1 Mejico Borjas,1

Andria Reyes,1 Dave Evans,1 Patrick L. Kinney,1 Ralph D. Whitehead Jr.,2 Frederica P. Perera,1

Stephen Matsoanne,4 and 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 ResearchInstitute, 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 amonginner-city women from New York City. Here we report on a pilot intervention using integrated pestmanagement (IPM) to reduce pest infestations and residential insecticide exposures among pregnantNew 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 oflow-toxicity pesticides, and education. Cockroach infestation levels and 2-week integrated indoor airsamples were collected at baseline and one month postintervention. The insecticides detected in theindoor 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 amongintervention cases but not control households. Among the intervention group, levels of piperonylbutoxide (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 fromcontrols 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 effectivestrategy for reducing pest infestation levels and the internal dose of insecticides during pregnancy.

KEY WORDS: insecticides, integrated pest management, intervention, prenatal, residential. EnvironHealth 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 havebeen endorsed by the National Institutes ofHealth (1997), and several studies have docu-mented the ability of IPM interventions toreduce pest populations, allergen levels, andasthma morbidity (Arbes et al. 2003; Brenneret al. 2003; Morgan et al. 2004; Wood et al.2001). However, only limited data address theeffectiveness of IPM interventions at reducingresidential insecticide exposure (Campbell et al.1999; Kass and Outwater, 2001).

The current study is the first to use bio-markers and air monitoring to documentchanges in insecticide exposure after an IPMintervention. The IPM strategy used here wasadapted from the Columbia Intervention toReduce Indoor Allergens Study (Kinney et al.2002). The aim of this study was to assess thefeasibility of reducing prenatal exposures topests 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 theintervention study occurred from August 2002through April 2004. Thirty women wererecruited from obstetrics and gynecology(OB/GYN) clinics located in New YorkPresbyterian and Harlem Hospitals. Eligibilitywas restricted to women 18–35 years of agewho self-identified as either African Americanor Latina (Dominican or Puerto Rican) andreported using high-toxicity insecticides (use ofexterminators, can sprays, and/or pest bombs)during pregnancy. Further, eligible subjectsmust have resided in northern Manhattan(north of 110th Street) or the South Bronx(south of Fordham Road) for at least 1 yearbefore pregnancy and must not be planning tomove from the community before delivery.From the 30 subjects who completed thescreening and consent forms, 5 womendropped from the study between enrollmentand monitoring (2 women gave birth beforethe intervention was completed, 1 experiencedhealth problems restricting her participation,and 2 moved out of the community). Samplescollected from the subjects before the interven-tion will be referred to as preintervention, andsamples collected after the intervention will bereferred to as postintervention. From theremaining 25 women, 25 (100%) completedthe prenatal questionnaire, 25 (100%) partici-pated in pre- and postintervention indoor airmonitoring, and biologic samples were col-lected from 21 (84%) subjects. Nineteen(76%) completed pre- and postinterventionassessment of pest infestation.

Control group. The control group wasselected from participants in an ongoing

prospective cohort study designed to validatebiomarkers of prenatal insecticide exposure. Aspart of this study, insecticide levels were meas-ured in 2-week integrated indoor air samplescollected continuously over the last 2 monthsof pregnancy. Blood samples were collectedfrom the mother and newborn at delivery.Enrollment for this study occurred in theOB/GYN clinics located in New YorkPresbyterian Hospital and Harlem Hospitalfrom October 2001 through July 2004. Therecruitment strategy and eligibility criteria forthe controls were identical to those for thecases. From the total of 110 women fullyenrolled in the biomarker validation study, 27were selected as controls for the interventionstudy. Control selection aimed to match casesubjects on year of enrollment (2002–2004)and self-reported use of high-toxicity insecti-cides (use of exterminators, can sprays, and/orpest bombs) during pregnancy. Baseline andfollow-up integrated air samples were selectedto match the pre- and postintervention sam-ples in the cases. Questionnaire data wereavailable for 100% of subjects. Baseline andfollow-up indoor air data were available for 24(88%) subjects; blood samples were collectedfrom 17 (63%) subjects. Fourteen (52%) sub-jects completed the initial pest infestation lev-els. Follow-up samples were available for onlysix (22%) subjects.

The institutional review board of theColumbia Presbyterian Medical Centerapproved the study, and we obtained writteninformed consent from all study subjects.

Intervention. The intervention commencedat the conclusion of the 2-week preinterventionmonitoring period. This IPM consisted of threemain components: an extensive cleaning withminor building repairs, a low-toxicity insecti-cide application, and behavioral/health educa-tion. The kitchen, bathroom, and living roomareas of the intervention apartments were pro-fessionally cleaned using low-toxicity, citrus-based cleaning products. Pest entry points weresealed with caulking compounds and/or metalscreens. A professional insecticide placementcompany injected low-toxicity insecticides,2.15% hydramethylnon (MAXFORCE;Maxforce Insect Control Systems, Oakland,CA), or small amounts of boric acid directlyinto the cracks and holes before sealing andplaced glue traps for cockroaches throughoutthe kitchen, bathroom, and problem areas.Hydramethylnon has low toxicity and lowvapor pressure and has been shown previouslyto be effective for long-term cockroach control(Appel 1992). Using a checklist prepared forthe Columbia Intervention to Reduce IndoorAllergens Study, the health educator assessedthe frequency and location of pest sightings andtailored the health education accordingly foreach participant. After the cleaning, a healtheducator met with the family to discuss IPM

strategies for pest control. Training sessionstargeted as many household members as possi-ble and strongly emphasized a team effort.Strategies included removing garbage from thehome each day, eating meals only in thekitchen, and cleaning up dishes and food spillsas soon as possible. In addition, the programincluded education and instruction regardingnontoxic pest control methods. Airtight con-tainers for food and trash storage were providedto each household. The intervention cleaningand behavioral training took place overapproximately 2–3 days. The control groupdid not receive an IPM intervention, nor didthey 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 theimportance of reducing insecticide use in thehome and techniques for controlling pestswithout using higher toxicity insecticides.

Sample collection. Questionnaire data. A45-minute questionnaire was administered tothe intervention and control groups in eachwoman’s home by a trained bilingual inter-viewer during the third trimester of pregnancy.The questionnaire included information ondemographics, home characteristics includinghousing disrepair and pest infestation levels,lifetime residential history, history of active andpassive smoking, occupational history, maternaleducation and income level, alcohol and druguse during pregnancy, and history of residentialinsecticide use. Information about insecticideuse included whether or not any pest controlmeasures were used by an exterminator or byothers (the woman herself, other householdmembers, or the building superintendent) dur-ing pregnancy and, if so, what types of meas-ures were used and at what frequency (Pereraet al. 2003; Whyatt et al. 2002, 2003).

Indoor air monitoring. Before the inter-vention, a baseline 2-week integrated indoorair sample was collected from the homes ofsubjects in the intervention and controlgroups. Monitoring commenced in each homeat the end of the second or beginning of thethird trimester of pregnancy using a BGIpump with a 0.5-L/min flow-rate (BGI, Inc.,Waltham, MA). The pump was attached to aURG (University Research Group, ChapelHill, NC) polyurethrane foam (PUF) samplerwith a 2.5-µm inlet cut fitted with a 30-mmquartz fiber filter and a foam cartridge backupto capture semivolatile vapors and aerosols. Thepumps were attached to a battery and operatedcontinuously over the 2 weeks. The monitoringequipment was placed in the main living area ofthe apartment, with the pump in a secure boxand the sampler (located inside a protectivewire cage) placed at least 60 cm from wall sur-faces at a height of 135 cm. The sampler heightwas chosen to represent the average between thewoman’s sitting and standing heights, because

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residential insecticide air concentrations havebeen shown to vary with height, being greatestnear the floor (Aprea et al. 2000; Fenske et al.1991). Study subjects were instructed on theimportance of not disturbing the equipmentand told to go about their daily activity as nor-mal. The research staff returned after 2 weeksto collect the equipment, perform a leakcheck, and record the pump flow-rates. Acareful log was kept of elapsed time on thepump meter and of rotometer readings andleak check results at each visit. The monitor-ing strategies for intervention and control

homes were identical. Prior quality controlanalyses 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 airsample was collected from intervention andcontrol homes. Protocols for the follow-up airmonitoring were identical to those for the base-line sample. The monitoring was targeted tooccur during the 38th to 40th week of preg-nancy; however, because of premature births orpostponements, some subject’s homes weremonitored immediately after delivery.

Cockroach infestation levels. To monitorcockroach infestation levels, six pheromoneglue traps (Victor Roach Pheromone Traps;Woodstream, Lititz, PA) were placed in stan-dardized locations throughout the kitchens ofeach subject during the 2-week baseline andfollow-up indoor air monitorings. After2 weeks, traps were collected and the numberof adult and nymph cockroaches caught ineach trap was counted.

Maternal and cord blood. We used bloodcollection procedures validated in our priorresearch studies to ensure that blood samples(maternal and/or umbilical cord) were collectedfrom women in the intervention and controlgroups at delivery (Whyatt et al. 2003). A sam-ple of infant cord blood was collected by deliv-ery room staff immediately after the cord wascut and the placenta delivered. Infant cordblood was obtained by syringing the blood intoheparinized syringes at the point the cord entersthe placenta. A sample of maternal blood(30–35 mL) was obtained within 1–2 dayspostpartum by the research staff or by hospitalstaff. A member of the research staff transportedthe blood samples to the biomarker laboratorylocated at Columbia University, New YorkCity, immediately after collection. Within 12hr of blood collection, the cord and maternalbloods were transferred to centrifuge tubes andspun for 15 min at 1,500 rpm. Plasma sampleswere collected and stored at –70°C before ship-ment to the Centers for Disease Control andPrevention (CDC) for insecticide analysis.

Pesticide analysis. Pesticides in airmonitoring filters. Analysis of insecticidesin the 2-week integrated indoor air samples was conducted by Southwest ResearchInstitute under the direction of D. Camann.Immediately after each 2-week collectionperiod, air monitoring filters were brought tothe laboratory at the Columbia Children’sCenter for Environmental Health, inventoriedand stored at 20°C. Every 4–6 weeks, air sam-ples were shipped to Southwest ResearchInstitute. The entire PUF plug and filter wasplaced in a Soxhlet extractor, spiked with ter-phenyl-d14 as a recovery surrogate, extractedwith 6% diethyl ether in hexane for 16 hr andconcentrated to 1.0 mL in 10% ether in hexa-nes. Extracts were stored frozen below –4°C.Insecticides are stable in the extract under theseconditions. We determined the amounts of thetarget insecticides in samples using Agilent6890/5973 gas chromatography/mass spec-trometry (Agilent, Wilmington, DE) in selectedion mode. Paired pre- and postintervention airsamples were available on 25 cases and 39 con-trols. The target insecticides that were measuredin the indoor air samples were bendiocarb, car-baryl, carbofuran, cis- and trans-permethrin,malathion, methyl parathion and propoxur. Inaddition, piperonyl butoxide, a synergist addedto natural and synthetic pyrethroid insecticides,was measured as an indicator of pyrethroidinsecticides. Chlorpyrifos and diazinon werenot assessed because most of the women wereenrolled in the study after the federal ban ontheir residential use and our prior data indicatethat the ban was effective at reducing use andexposures to these insecticides among inner-citywomen in New York City (Carlton et al. 2004;Whyatt et al. 2003, 2004).

Pesticides in plasma samples. Analysis ofthe insecticides or their metabolites in mater-nal and cord plasma was conducted by theCDC under the direction of D. Barr usingisotope dilution gas chromatography–high reso-lution mass spectrometry (Barr et al. 2002).Approximately 10–15% of all samples assayedwere positive or negative control samples. Twoconcentrations of positive control samples were

Williams et al.

1686 VOLUME 114 | NUMBER 11 | November 2006 • Environmental Health Perspectives

Table 1. Distribution of maternal sociodemographiccharacteristics gathered from questionnairesadministered on recruitment (intervention group,n = 25; control group, n = 27).

Characteristic Intervention (%) Control (%)

Age [years (range)] 26.6 (19–36) 24.3 (18–36)Educationa

< High school diploma 28.0 55.6High school diploma or 28.0 37

equivalent> High school diploma 44.0 7.4

Race/ethnicityLatina 76.0 59.3African American 20.0 37.0

Marital statusMarried 12.0 22.0Never married 72.0 66.7Divorced/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 conditionsHoles in ceiling/wallsa 75.0 48.1Unrepaired water damage 40.0 22.2Leaky pipesa 42.0 11.1

Year of delivery2002 28.0 44.42003 68.0 33.32004 4.0 22.2

Season of deliveryJanuary–March 20 30.8April–June 8 23.1July–September 40 15.4October–December 32 30.8

Missing information for the two groups includes, for inter-vention, race/ethnicity (1), income (1), unrepaired waterdamage (1), leaky pipes (1); for control, income (3), seasonof delivery (1).aPearson’s chi-square test, p < 0.05.

Table 2. Reported pest infestation levels and pesti-cide use assessed from prenatal questionnairesadministered on recruitment (intervention group,n = 25; control group, n = 27).

Affirmative (%)Questionnaire Intervention Control

Reported roaches 91.7 85.2Reported exposure to high- 100 100

toxicity pest control measures:Spray by exterminator 47.8 40.7Can spray 73.9 76.9Pest 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), pestbomb (1).

Figure 1. Cockroach infestation levels. (A) Mean (± SE) cockroaches (adults + nymphs) in traps collectedover 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 reductionbetween 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 betweenthe intervention and control groups, group t-test, p = 0.1 (B).*Wilcoxon signed-rank test, p = 0.016.

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used: one spiked at the mid-calibration rangeand one at the low-calibration range. A set ofblinded positive control samples was also run,which an independent quality assurance officerevaluated. CDC provided results on insecticidelevels in maternal blood samples for 21 casesand 32 controls and from umbilical cord bloodfor 13 cases and 20 controls. The target insecti-cides that were analyzed in blood were thosethat corresponded to the insecticides detectedin the indoor air samples, and included theparent compounds for cis-permethrin andtrans-permethrin as well as the metabolite ofpropoxur, 2-isopropoxyphenol.

Statistical analysis. For both environmen-tal and biologic monitoring data, we assignedsamples less than the limit of detection(LOD) a value of 0.5 × LOD. For hypothesistesting, variables were treated as continuous orcategorical depending on their distributionalproperties. Continuous variables were initiallylog-transformed as appropriate to normalize thedistribution. However, in almost all cases, thedata could not be normally distributed afterlog-transformation, so nonparametric statisticswere used. The differences in pest infestationlevels and air insecticide levels between pre- andpostintervention in both cases and controlswere normally distributed, so we used para-metric statistics to evaluate whether these dif-ferences varied significantly between theintervention and control group. Analyses werealso undertaken to determine whether the inter-vention and control groups differed in terms ofdemographic characteristics or season and yearof delivery. No significant differences were seen.

For pest infestation levels, we used theWilcoxon signed-rank test to assess the differ-ences between pre- and postintervention pestinfestation levels in both intervention and con-trol groups. Because the differences in pestinfestation levels were normally distributed, weused the independent sample t-test to deter-mine whether the differences in pest infestationlevels between pre- and postinterventionobserved in the intervention group were signifi-cantly different from the differences in pestinfestation levels observed in the control group.

For 2-week integrated air insecticide levels,we compared detection frequencies as well asdetection levels. We used McNemar’s test toexamine the change in detection frequency of

insecticide levels in air between pre- andpostintervention in both the intervention andcontrol groups. We used the Wilcoxon signed-rank test to examine the change in insecticidelevels between pre- and postintervention forboth groups. Finally, we used the independentsample t-tests and regression analyses control-ling for race/ethnicity, season, and year ofdelivery to compare whether the change in airinsecticide levels between pre- and postinter-vention differed significantly between theintervention and control groups. For insecti-cide levels in maternal and cord blood samples,we compared differences in detection frequen-cies between intervention and control subjectsusing chi-square analyses (Fisher’s exact test).Results were considered significant at p < 0.05(two-tailed).

Results

Study participants. Participants included 25intervention cases and 27 nonintervention con-trols. Demographic characteristics were com-pared between cases and controls and weregenerally comparable between the two groups(Table 1). Discrepancies between the groupswere limited to education and housing condi-tions (holes in ceilings and walls and leakypipes) (Pearson’s chi-square test, p = 0.008,0.05, and 0.012, respectively). Table 2describes reported insecticide use and pestinfestation levels in the intervention and controlgroups. According to the prenatal questionnaireand in compliance with eligibility criteria,100% of the intervention and control subjectsreported exposure to high-toxicity insecticidesduring pregnancy either through spray by anexterminator, personal (or household) use ofspray insecticides, and/or use of a pest bomb.Patterns of insecticide use and reported pestinfestation levels were not different between thetwo groups. Most of both intervention andcontrol subjects reported seeing cockroaches intheir homes (91.7 and 85.2%, respectively).More than 50% of both groups reported seeingcockroaches in their homes on a daily basis.

Pest infestation levels. Pest traps placed inthe subjects’ homes for a 2-week collectionperiod before the intervention revealed thatadult cockroaches were present at baseline in77% of the intervention group and 86% ofthe control group. Figure 1A displays the total

number of cockroaches (adult and nymph)collected in traps pre- and postinterventionfrom case and control households. At baseline,the mean (± SE) adult cockroach count washigher in the intervention than in control sub-jects (27.6 ± 6.8 vs. 11.9 ± 3.1, respectively).At baseline, nymph cockroaches were found in82% of intervention homes and 93% of controlhomes and nymph counts were higher in theintervention than in the controls (148.6 ± 32.5vs. 76.6 ± 21.1). We assessed the effectivenessof the intervention by comparing the differ-ences in pre- and postintervention roach countswithin and between intervention and controlsubjects. Overall, there was a 47% decrease intotal cockroach infestation among interventionhouseholds after the intervention (Wilcoxonsigned-rank test, p = 0.016) (Figure 1B). Adultcockroaches decreased by 60% (p = 0.006)and nymph cockroaches decreased by 44%(p = 0.033). By contrast, control householdsshowed no significant reduction of adult ornymph cockroaches between baseline and fol-low-up (see Figure 1A). However, the differ-ences between the preintervention comparedwith postintervention total, nymph, and adultcockroach levels were not significantly greaterin the intervention group than in the controlgroup (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) werenot detected or were found in < 10% of eitherintervention or control samples. Of theremaining insecticides, propoxur was detectedin 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% ofpostintervention samples and 24 and 16% ofbaseline control samples and 17 and 13% offollow-up control samples, respectively. Inaddition, piperonyl butoxide was detected in71% of pre- and postintervention samples and72 and 57% of baseline and follow-up controlsamples, respectively. The mean levels forthese compounds in pre- and postintervention2-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 controlgroup 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 PositivePesticide (ng/m3) (mean ± SE) (mean ± SE) ranksa ranksb Ties p-Value (mean ± SE) (mean ± SE) ranksa ranksb Ties p-ValuePropoxur 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 0.081Piperonyl 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 0.089cis-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 0.758trans-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 0.338Missing information includes, for intervention, propoxur (3), piperonyl butoxide (2), trans-permethrin (1). aLevels were lower in follow-up compared with baseline. bLevels were higher in follow-up compared with baseline.

intervention (Table 3 and Figure 2A). Themean level of piperonyl butoxide in interven-tion homes decreased by 50% (Wilcoxonsigned-rank test, p = 0.016). Of the 23 inter-vention homes with available air sampling, adecrease in piperonyl butoxide was seen in 74%(17/23) of homes, whereas an increase was seenin 26% (6/23) of homes. Piperonyl butoxidelevels also decreased in control homes, but notsignificantly (p = 0.08). The difference betweenpre- and postintervention levels of piperonylbutoxide in the intervention group was notsignificantly different from the differencebetween baseline to follow-up levels in thecontrols (independent sample t-test, p = 0.3,Figure 2B). Levels of the pyrethroid insecti-cides cis-permethrin and trans-permethrindecreased in follow-up compared with baselineair samples in most intervention homes andincreased in most control homes (see negativeand positive ranks in Table 3), but these dif-ferences were not significant. Propoxur levelsdecreased nonsignificantly from baseline tofollow-up among control homes only(Wilcoxon signed-rank test, p = 0.08).

Biologic samples. Table 4 shows the levelsof insecticides that were measured in maternalplasma samples. These included 2-iso-propoxyphenol (metabolite of propoxur) andcis- and trans-permethrin (two isomers of thepyrethroid insecticide permethrin). Theseinsecticides were detected in plasma samplesfrom the control group but not from the inter-vention group. Specifically, 2-isopropoxy-phenol was detected in 0% of maternal bloodsamples from the intervention group and in12% of maternal blood samples from controls(chi-square, p = 0.1). Cis- and trans-permethrinwere detected in 0% of maternal blood samples

from intervention group and 12 and 29% ofmaternal blood samples from controls, differ-ences that were significant for trans-permethrin(chi-square, p = 0.008) (Table 4). None ofthese three pesticides were present at levelsgreater than LOD in either intervention orcontrol cord blood samples.

Discussion

This pilot intervention study demonstrates thatIPM can have a significant effect on pest infes-tation levels and appears to reduce residentialinsecticide exposures during pregnancy. Ourfindings showing significant reductions incockroach populations are consistent withthose of other intervention studies that focusedon reducing either pest infestations or allergenlevels related to pest infestation (Arbes et al.2003; Brenner et al. 2003; Kass and Outwater2001; McConnell et al. 2003; Wood et al.2001). To our knowledge, however, no otherstudies have demonstrated reductions in pesti-cide exposure using biologic and environmen-tal measures of insecticide exposure.

Success of IPM interventions has beenattributed 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, attentionwas focused on problem areas in the houseincluding the kitchen, bathroom, and mainliving space. In addition to repairing thecracks and holes present in the home, we per-formed an extensive cleaning to remove fooddebris, grease stains, and general clutter.Airtight containers were provided for foodstorage, and individualized education planswere developed for each home that targeted

high-risk behaviors. We conclude that theintervention was successful at reducing cock-roaches based on data from pest traps placedin the subjects’ homes for 2-week periodsimmediately before and approximately1 month after the intervention. Cockroachinfestation levels in intervention householdsdeclined by more than one-third, whereascockroach levels in the control householdsremained unchanged.

Despite the dual goal of IPM to reducecockroach and insecticide exposures, most IPMevaluations have focused on the reduction ofpests. Data on the effectiveness of reducinginsecticide exposure are limited, and docu-mented in only two studies. A building-wideintervention in New York City public housingfound resident’s use of spray insecticides andChinese Chalk, an illegal insecticide, droppedto zero after a building-wide IPM interventionthat included education about the safe use ofinsecticides (Kass DE, Outwater T, unpub-lished data). An IPM intervention in Canadafound decreases in both personal use of sprayinsecticides and resident requests for extermi-nators to use spray insecticides in their apart-ment, requesting instead lower-toxicity pastesor gels (Campbell et al. 1999). Although thesefindings are encouraging, they rely on resident-reported insecticide use after educational ses-sions and do not include objective measuresof insecticide exposures. The current study isthe first to use indoor air monitoring and bio-markers to document changes in insecticideexposure after an IPM intervention.

In the present study, target insecticides inindoor air samples included the carbamate,propoxur, the pyrethroids cis-permethrin andtrans-permethrin, and the pyrethroid synergistpiperonyl butoxide. Selection of these insecti-cides was based on evidence that they werewidely used for residential pest control (Whyattet al. 2003). Detection frequencies and meanlevels of these insecticides in the current studywere similar to those previously documented inthis population (Whyatt et al. 2003, 2004). Toassess the effectiveness of the IPM, levels of resi-dential insecticides were measured in 2-weekintegrated indoor air samples collected beforeand after implementation of the IPM and com-pared with those for a control population. Theeffectiveness of the IPM on reducing indoor airlevels of residential insecticides can be discernedfrom trends in piperonyl butoxide. Piperonylbutoxide is a compound added to manypyrethroid formulations to delay metabolicdegradation of the active ingredients andenhance insecticidal properties. It is not used inother products and is more volatile than thepyrethroids themselves, so they can be reliablymeasured in air samples as an indicator ofpyrethroid insecticide use. It has been suggestedthat pyrethroid insecticides are being used toreplace the recently restricted organophosphates

Williams et al.

1688 VOLUME 114 | NUMBER 11 | November 2006 • 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-valuea

2-Isopropoxyphenol 1.50 0 11.8 0.106cis-Permethrin 0.50 0 11.8 0.106trans-Permethrin 0.50 0 29.4 0.008

Missing information includes, for controls, cis-permethrin (1), trans-permethrin (1).aDifference in detection frequency between intervention and control groups.

Figure 2. Piperonyl butoxide in 2-week integrated air samples. (A) Changes in mean (± SE) piperonyl butoxidelevels 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 between2-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 butoxidelevels between the intervention and control groups, group t-test, p = 0.3) (B).*Wilcoxon signed-rank test, p = 0.016.

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Intervention to reduce residential pesticide use

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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 theintervention. This decreasing trend was not sig-nificant in the control households. Further, thedata suggest that the intervention may havebeen particularly effective at reducing exposureto the pyrethroid insecticides. Levels of thetrans-isomer of permethrin were lower inmaternal plasma samples collected from theintervention group than in controls.

However, these findings should be inter-preted with caution, particularly because resultsfor propoxur do not mirror those seen forpiperonyl butoxide. Specifically, propoxur levelsin indoor air samples decreased in follow-upcompared with baseline air samples among con-trol households, but not among interventionhouseholds. Propoxur is a carbamate licensedfor residential pest control and has not beensubject to regulatory restrictions, as have theorganophosphates, chlorpyrifos, and diazinon.However, our prior data suggest that propoxuruse in inner-city communities in New YorkCity may be decreasing. Specifically, we founda highly significant decrease in propoxur levelsbetween 1999 and 2001 in personal air sam-ples collected from African-American andDominican women in New York City duringpregnancy and in the corresponding bloodsamples collected from the mothers and new-borns at delivery (Whyatt et al. 2003, 2004).Unfortunately, no data are available comparingfrequencies of pyrethroid versus propoxur usein these communities.

Although this pilot intervention indicatedthat IPM is effective at reducing pest infestationand the internal dose of the insecticides duringpregnancy, limitations in the study designshould be noted. The primary limitation of thestudy is the small sample size and the short timeelapsed between pre- and postinterventionmonitoring. Many intervention studies allow6 months to 1 year between samplings to deter-mine if the intervention is both successful andsustainable. However, the current interventionwas conducted during pregnancy and was thuslimited in follow-up time. Further, the controlswere selected from an ongoing biomarker vali-dation study that followed women only duringpregnancy. Thus we were not able to evaluatethe sustainability of the intervention over anextended period. In addition, the optimaldesign for an intervention study is to match theintervention subjects to control subjects andhave all data collected and analyzed simultane-ously. This was not possible here because thecontrols were selected from ongoing research.

However, the intervention and control groupswere comparable in terms of years of enroll-ment and self-reported pesticide use.

A principal goal of the pilot study was toassess whether environmental and biologicmeasures can be used in evaluating the efficacyof IPM interventions in reducing residentialpesticide exposures. These initial results arepromising, although additional research is war-ranted given the small sample size and inconsis-tency in some of the findings. Environmentalmeasures for the targeted pesticides are not nec-essarily associated with the biologic measures.Therefore, a lack of meaningfully differentresults in air levels of pesticides between theintervention and control groups does not influ-ence the expected results in maternal plasmabetween the two groups. Subsequent researchcould also draw on our study design to devisean IPM intervention that can be conducted byhousehold members themselves and that is bothfeasible and affordable. Such an interventioncould be applied to entire apartment buildingsor complexes to determine the effects of larger-scale interventions, as opposed to individualunits. In the current study, cleaning and homerepairs were completed by a professional clean-ing crew to allow comparability and consis-tency. However, the supplies and techniquesare similar to those available in the community.In conclusion, we believe that this interventionprotocol using IPM can be successfully adaptedfor use by individuals within households in thiscommunity to reduce pest infestation levels andresidential pesticide exposure.

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