Journal of Asthma, 44:455–460, 2007Copyright C© 2007 Informa HealthcareISSN: 0277-0903 print / 1532-4303 onlineDOI: 10.1080/02770900701421971

ORIGINAL ARTICLE

Efficacy of Integrated Pest Management in Reducing Cockroach Allergen

Concentrations in Urban Public Housing

JUNENETTE L. PETERS, SC.D.,1,∗ JONATHAN I. LEVY, SC.D.,2 MICHAEL L. MUILENBERG, M.S.,2BRENT A. COULL, PH.D.,3 AND JOHN D. SPENGLER, PH.D.2

1Department of Environmental Health, Environmental and Occupational Medicine and Epidemiology Program,Harvard School of Public Health, Boston, Massachusetts

2Department of Environmental Health, Exposure, Epidemiology and Risk Program,Harvard School of Public Health, Boston, Massachusetts

3Department of Biostatistics, Harvard School of Public Health, Boston, Massachsetts, U.S.A.

The efficacy of residential interventions to reduce cockroach allergens in public housing developments was evaluated over months of follow-up. Repeated measurements were collected from 39 apartments, with longitudinal analyses used to evaluate changes over time. Bla g 1 kitchenconcentrations were reduced 71% and bed concentrations 53% (86% and 70% for Bla g 2, respectively) by 6 months post-intervention, after whichconcentrations began to increase. Apartments with higher concentrations were usually in poorer condition and benefited most from pest managementefforts. Intensive interventions can significantly reduce the allergen burden in public housing apartments, but intervention efforts must be sustained.

Keywords asthma, cockroach allergen, community-based participatory research, low-income, intervention

INTRODUCTION

Low-income, urban dwellers tend to be at greater risk ofcockroach allergen sensitivity and elevated household cock-roach allergen concentrations. This tendency has been sug-gested as a contributor to the relatively high incidence ofasthma-related morbidity among inner-city children (1–4).Among urban populations in the northeastern United States,cockroach allergen sensitivity and exposure predominate, andin general, appear to have a greater effect on asthma morbiditythan dust mite or pet allergens (5).

Public housing developments are designated as housingfor low-to very-low–income households. In the northeasternUnited States, they are often located in low-income, minorityneighborhoods and typically have persistent cockroach infes-tation. Public housing authorities have the capacity to imple-ment comprehensive system-wide interventions. However,given the financial limitations faced by authorities, elucidat-ing the optimal intensity, frequency, and timing for successfulintervention and the areas of maximum benefit is critical.

Although allergen avoidance has been recommended aspart of an asthma management plan (6–9), cockroach allergenreduction efforts using a variety of intervention measureshave met with mixed results. Gergen et al. (10) focused on48 homes that were part of the National Cooperative Inner-City Asthma Study (NCICAS), finding a significant reductiononly in kitchen Bla g 1 concentrations and only at 2 monthsafter intervention. Concentrations increased to baseline levelsor higher by month 12. Williams et al. (11) looked at eight

∗Corresponding author: Junenette L. Peters, Department of Environmen-tal Health, Harvard School of Public Health, P.O. Box 15697, LandmarkCenter East/ Room 3-111-23, 401 Park Drive, Boston, MA 02215; E-mail:jpeters@hsph.harvard.edu

single-family dwellings and found a statistically significantreduction from baseline to month 6 for Bla g 1, but not forBla g 2. These two studies primarily used pest control asthe intervention method. Arbes et al. (12, 13) used a morecomprehensive suite of interventions and found reductionsover 6 months that could be sustained up to 12 months withadditional pesticide treatment.

The current study is part of the Boston Healthy Pub-lic Housing Initiative (HPHI), a community-based par-ticipatory research project including collaborators fromthree universities, Boston city housing and health agencies,and associations representing tenants (see http://www.hsph.harvard.edu/hphi/). Our focus on the linkage between indoorallergens and asthma in public housing was motivated by anearlier survey of two of the developments that are part ofthis study that reported a prevalence of asthma more thandouble the Massachusetts average of 6.5% (14–17). In addi-tion, allergy testing of asthmatic children in our study foundthat 59% of the children were allergic to cockroaches (18).A pilot study in nine apartments in one of our public housingdevelopments found that intensive cleaning alone resulted intransient reductions in allergen concentrations (19), indicat-ing the viability of this approach and the need for a morecomprehensive assessment.

This study evaluates the effectiveness of a combination ofabatement measures for reducing allergen concentrations andthe factors affecting efficacy over months of follow-up.

METHODS

PopulationWe recruited families from three public housing develop-

ments in Boston, MA: Franklin Hill, Washington Beech, andWest Broadway. To participate, a family had to include a child

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456 J. L. PETERS ET AL.

between 4 and 17 years of age who had self-reported doctor-diagnosed asthma. Asthma status was also evaluated by astudy nurse and pediatric pulmonologist (18). Households re-ceived baseline environmental sampling between July 2002and May 2003, with subsequent interventions aimed primar-ily at reducing pest-related allergen concentrations in apart-ment units. Post-intervention sampling took place betweenOctober 2002 and February 2004 at intervals immediatelyafter and approximately 3, 6, 9, and 12 months after interven-tions. The time span reflects a two-phased recruitment pro-cess. Community Health Advocates from the developmentsor surrounding neighborhoods were trained and included aspart of the study recruitment and data collection team. Thestudy was approved by Boston University, Harvard Schoolof Public Health and Tufts University institutional reviewboards. The required written, informed consent was obtainedfrom all study participants.

InterventionsIntervention activities included industrial cleaning, inte-

grated pest management (IPM), and mattress replacementand are described in detail elsewhere (20). Briefly, indus-trial cleaning by contracted services involved the removalof cockroaches and mice and their feces and secretions andthe removal of grease and debris. IPM included (1) layingmousetraps; (2) professional strategic placement of pest con-trol treatments based on thorough inspection and sightings incockroach traps; (3) sealing cracks and small holes that couldbe repaired using caulking and spray foam; (4) resident ed-ucation on how to make the home inhospitable to pests; and(5) providing plastic food storage containers and trash bins.Residents were also encouraged to use the existing work-order system for requesting apartment maintenance servicesfor more extensive repairs.

Allergen Analysis of Dust SamplesTwo separate vacuum dust samples were collected from

each apartment—one from the child’s bed and the other fromthe kitchen floor. The protocol for dust sample collection wasbased on the method outlined by Levy et al. (20) and Chewet al. (21). In brief, for bed samples, all layers of the bedding,including the mattress and pillows, were vacuumed for a totalof five minutes. For kitchen samples, the cupboard under thekitchen sink and the kitchen floor, focusing on the baseboardsand around the refrigerator and stove, were vacuumed for atotal of five minutes.

For immunoassay analysis, 100 mg of sieved dust was ex-tracted using 2 mL of borate buffered saline. Samples wereanalyzed for Bla g 1 and Bla g 2 cockroach allergens using amonoclonal sandwich enzyme-linked immunosorbent assay(ELISA) (Indoor Biotechnologies, Charlottesville, VA) (22).Concentrations are reported in U/g. The lower limits of de-tection (LLOD) were 0.20 U/g for Bla g 1 and 0.40 U/g forBla g 2.

StatisticsValues below the LLOD were assigned random numbers

between zero and the LLOD according to an assumed uniformdistribution. This gives less biased estimates than using fill-in methods such as LLOD or 1/2 LLOD (23). Days after

intervention were counted from the date of the last day ofthe multiple interventions, and then divided into months foranalyses.

The efficacy and sustainability of interventions were as-sessed using three methods: (1) comparison of the differencebetween baseline and the minimum post-intervention concen-tration and of the difference between baseline and the finalpost-intervention concentration (Wilcoxon rank-sum test);(2) modeled trend in cockroach allergen concentrations overtime (mixed model); and (3) odds of being below exacerba-tion levels over time (generalized estimating equations).

Mixed model longitudinal analysis was used on log-transformed continuous data to evaluate changes over timeand the effect of household characteristics on these changes.Longitudinal analysis enabled us to account for the correla-tion among repeated measurements on the same household.This allowed for a more efficient use of the repeated mea-surements and provided information about time trends thatwould not be available through other summary statistics (i.e.,paired t test). The mixed model is able to handle unbalanceddata (missing data and variations in the timing of follow-upamong participants) (24). We assumed that the correlationbetween repeated measures was best captured by compoundsymmetry, which assumes the same correlation between eachof the measures in time, but tested other likely correlationstructures. We allowed the baseline concentrations to varyby household (random intercept) instead of assuming that allhouseholds began at the group mean concentration. Time af-ter intervention followed a quadratic form and was thereforemodeled as month and month squared.

Concentrations were divided into categories based on thecut-point hypothesized to be associated with asthma exacer-bation (8 U/g) (1, 25). The generalized estimating equations(GEE) method was used to assess the odds of being below thiscritical exacerbation level over the months post-intervention.This longitudinal method was used because the outcome wasbinary instead of continuous.

We considered housekeeping and presence of holes in thewall and ceiling as potential modifiers of the efficacy of inter-ventions, based on a previous analysis that found both of thesefactors to be significant determinants of baseline cockroachallergen concentrations (26). Both variables were assessedduring visual inspection of the apartments before interven-tions. Housekeeping was given a rating of one through fiveon the basis of cleanliness and clutter. For analysis, the fivecategories were reduced to two: below average housekeep-ing versus average to above average. Holes in the walls andceilings were from a variety of sources including electricalinstallations and plumbing repairs. Season at sample collec-tion was controlled for and was divided into cold months(October-April) and hot (May-September), roughly corre-sponding to the designated heating/non-heating seasons. pvalues less than 0.05 were considered significant, and lessthan 0.1 as marginally significant. All tests were performedusing SAS software (version 9.1).

RESULTS

Only data up to 10 months post-intervention were usedin analyses because there were few measurements after thattime. Of the 45 apartment units receiving interventions, 39

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COCKROACH ALLERGEN INTERVENTION EFFICACY 457

had at least one post-intervention measurement, 33 had 2, 26had 3, and 17 had 4. Seventy-six percent of the 39 apartmentswith at least one post-intervention measurement had holes inthe walls/ceiling. Thirteen percent had below average house-keeping practices (clutter and lack of cleanliness).

Effect of Intervention over TimeDifference between baseline and minimum and between

baseline and final post-intervention measures. For kitchenallergen concentrations, there was a significant difference be-tween a household’s baseline value and minimum concentra-tion after intervention, for both Bla g 1 and Bla g 2 (p < 0.01)(Figure 1A; all figures show data for Bla g 1 only). The me-dian difference was 23 U/g for Bla g 1 and 41 U/g for Bla g2. Comparing the baseline concentrations with the final post-intervention measurement, the median differences were notas large (Bla g 1: 13 U/g; Bla g 2: 13 U/g), but the differencesremained statistically significant (Bla g 1: p = 0.03; Bla g 2:p = 0.04).

Similarly, bed concentrations also decreased significantlybetween pre-intervention and minimum concentrations af-ter intervention (p < 0.01). The median reduction was 0.16U/g for Bla g 1 and 1.3 U/g for Bla g 2 (Figure 1b). Atthe final post-intervention measurement, the difference forBla g 1 was statistically significant (p = 0.01), with a me-dian reduction from baseline of 0.09 U/g. The difference for

FIGURE 1.—Distribution of Bla g 1 cockroach allergen measurements at baseline,at minimum post-intervention levels, and at the final post-intervention measure-ment for (A) kitchen and (B) bed.

Bla g 2 was only marginally significant (p = 0.05), althoughthe median reduction from baseline (0.87 U/g) did representa reduction of greater than 50%. As above, the minimumconcentrations after intervention were lower than at the fi-nal post-intervention measurement, indicating the potentialfor a U-shaped relationship between concentrations and timepost-intervention.

Trend of cockroach allergen concentrationspost-intervention (mixed model). Modeled geometricmean concentrations of Bla g 1 in the kitchen declined 71%from baseline to 6 months after the intervention (Figure 2a).At the lowest point, geometric mean concentrations werestill above the asthma exacerbation cut-point of 8 U/g (at9.6 U/g). Between month 6 and 10, the modeled geometric

FIGURE 2.—Longitudinal mixed model (with random intercept) estimation ofgeometric mean and confidence intervals of (A) kitchen and (B) bed Bla g 1concentrations with time after intervention. Month 0 represents baseline (pre-intervention).

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mean concentrations started to increase so that, by month10, concentrations were only 38% below baseline concen-trations. Similarly, geometric mean Bla g 2 concentrations inthe kitchen were reduced by 86% from baseline to 6 monthsafter interventions, but concentrations then increased to43% below baseline concentrations by month 10. Geometricmean concentrations of Bla g 2 also never fell below 8 U/g(at 17 U/g at the lowest point).

Similar trends were seen the bed, albeit with significantlylower concentrations (Figure 2b). Geometric mean concen-trations of Bla g 1 in the bed were reduced 70% from baselineto 6 months post-intervention, but increased to 44% of base-line by month 10. Geometric mean Bla g 2 concentrations inthe bed were reduced 53% by month 6, but increased to 16%below baseline by month 10.

Odds of being below critical exacerbation level. Themixed model analyses provide significant insight aboutchanges in geometric mean concentrations, but the distribu-tion of benefits is of equal importance, as it provides insightregarding the households where interventions were most ef-fective and where health benefits might be anticipated. In par-ticular, given the proposed critical asthma exacerbation levelof 8 U/g, it is important to know whether the odds of beingbelow this level changed over the post-intervention period.Despite the U-shaped relationship for geometric mean con-centrations in mixed models, a quadratic term was not a statis-tically significant predictor of the odds of being below 8 U/g.Therefore, the odds ratios represent monthly changes in theodds of being below the exacerbation threshold throughoutthe study period. The odds ratio of being below the exacer-bation cut-point by month after intervention was 1.17 (95%CI: 1.05–1.30) for Bla g 1 in the kitchen and 1.20 (95%CI: 1.08–1.34) for Bla g 2 in the kitchen. For bed concen-trations, the odds ratio over time after intervention was notsignificant for Bla g 1 (0.99, 95% CI: 0.85–1.14), but wasmarginally significant (1.07, 95% CI: 0.99-1.16) for Bla g2. Given the lower concentrations of cockroach allergensin the bed relative to the proposed exacerbation level of 8U/g (especially for Bla g 1), the lack of significance is notsurprising.

Effect of Household Characteristics on Changesin Cockroach Allergen Concentrations over Time

We examined whether there was a difference in changein allergen concentrations over time by housekeeping prac-tices or holes in the walls and ceiling, controlling for season.In separate analyses, kitchen Bla g 1 had marginally greaterreductions over time for those with below average housekeep-ing (p = 0.08) and for those with holes in the walls/ceilings(p = 0.08) at the start of the study. While the significancecalculations are greatly affected by our unbalanced data setand lack of statistical power, all time trends indicated greaterimprovement among those apartments in poorer condition.

DISCUSSION

This study focused on the efficacy and sustainability ofcockroach allergen reduction efforts applied in the publichousing setting and the degree to which improvements de-pended on household conditions. We found that the combinedenvironmental interventions of intensive cleaning and inte-

grated pest management, as well as new mattresses, wereeffective in reducing cockroach allergen concentrations inpublic housing. This is consistent with what has been doc-umented from a review of cockroach allergen avoidance ef-forts (27). Apartments with higher allergen concentrationsat baseline were usually in poorer condition with respectto housekeeping and holes in the wall/ceiling, and theseapartments appeared to benefit most from the interventionefforts.

Both the traditional statistical method of comparison andlongitudinal analysis gave us similar results. Both methodsshowed that allergen levels were reduced for a period of timeafter interventions but subsequently increased. However, thelongitudinal analysis had four advantages over the Wilcoxonrank-sum test: (1) it allowed us to define the time horizonover which the allergen reduction and subsequent increasetook place; (2) it let us use information from householdseven when they lacked measurements at each time point; (3)it avoided issues of multiple comparisons; and (4) it allowedus to formally consider variable responses across apartments.Longitudinal analysis showed that geometric mean allergenlevels declined steadily for the first 6 months after interven-tion, after which point geometric mean concentrations beganto increase. This information is of great interest to publichousing authorities or other landlords attempting to addresspest-related issues, as it indicates the frequency of pest man-agement efforts needed.

Even with marked reductions in cockroach allergen con-centrations, some apartments remained above concentrationsthat have the potential for exacerbating existing asthma. Otherstudies have reported similar findings, where concentrationswere reduced significantly but remained above the hypoth-esized threshold (10, 12, 13, 28, 29). This may reflect thedifficulty of eliminating the allergen reservoirs due to cock-roach behavior patterns (7, 27). Nonetheless, as a result ofour interventions, there were greater odds that an apartmentwould be below the proposed exacerbation cut-point for eachmonth after intervention, despite increases in the geometricmean concentrations after 6 months post-intervention. Thisobservation of an increase in geometric means after 6 monthsversus the linear decrease in odds of being below the cut-pointmay reflect improvements in a growing number of homes,while a few homes may have reverted to high concentrationsthus driving up the mean.

While this analysis reports on reductions relative to anexacerbation cut-point, it should be noted that the effect ofallergen concentrations on asthma exacerbation occurs alonga continuum rather than at a sharply defined threshold (30).This suggests that even modest reductions in concentrationsmay benefit especially sensitive asthmatics. In addition, re-ductions of concentrations already below proposed thresh-olds could improve allergen-related symptoms. Morgan et al.(31) reported geometric mean bed concentrations below criti-cal sensitization and exacerbation levels, similar to what wasobserved in our study for Bla g 1. They found that a re-duction in these relatively low cockroach allergen concen-trations significantly correlated with a decrease in asthma-related morbidity. In another analysis of our cohort, reductionin cockroach allergen concentrations was moderately associ-ated with improvements in some respiratory outcomes (20)as well as quality of life (32).

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COCKROACH ALLERGEN INTERVENTION EFFICACY 459

Because of our small sample size, we may not have had thepower to detect differential effects by housekeeping practicesor presence of holes in the wall. However, the directions ofthe effects were consistent with expectations given our com-bination of interventions. We were unable to repair majorholes in the walls in this study; however, our pest manage-ment activities included integrated pest management tech-niques addressing sources of food, water, and shelter for cock-roaches, which may have limited entry of roaches from otherunits.

We conclude that cockroach allergen can be reduced in in-dividual public housing units through intensive cleaning andintegrated pest management and that the reductions can besustained up to 6 months with no further external interven-tion. However, since cockroach populations can most likelybe controlled, not eliminated, strategic placement of pest con-trol treatment based on visual inspection and cockroach trapsshould be instituted as part of the work orders for regularlyscheduled extermination visits in the developments. Theseefforts should preferably be done on a building-wide basisto minimize the likelihood of reinfestation and should followintegrated pest management principles to minimize residen-tial pesticide exposures. Coupled with an educational cam-paign, this might provide long-term, sustainable cockroachallergen reductions. Given the high prevalence of asthma andfrequency of cockroach allergen sensitivities among asthmat-ics in this population, intervention efforts may play a key rolein reducing asthma-related morbidity.

ACKNOWLEDGMENT

The authors wish to thank the community health advo-cates and those who worked with them in data collection andoutreach. In addition, they thank Jose Vallarino, ResearchSpecialist at the Harvard School of Public Health, for his in-valuable contributions to data collection efforts. They alsothank the Simmons Inc. for the allergy-free mattresses. Mostimportantly, the authors thank the families from the threepublic housing developments who participated in the study.

HPHI partners included Boston Housing Authority, BostonPublic Health Commission, Boston University School ofPublic Health, Committee for Boston Public Housing,Franklin Hill Tenant Task Force, Inc., Harvard UniversitySchool of Public Health, Peregrine Energy Group, Tufts Uni-versity School of Medicine, Urban Habitat Initiatives, andWest Broadway Tenant Task Force, Inc.

Funding for this study was received from the U.S. Depart-ment of Housing and Urban Development’s Office of HealthyHomes and Lead Hazard Control (Grant MALHH0077-00),W. K. Kellogg Foundation, Jessie B. Cox Family Trust, andThe Boston Foundation. J.L.P. was funded in part by theNIEHS Training Grant 2T32HL07118-29 and Center GrantP30 ES00002.

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