National prevalence and exposure risk for mouse allergen in US households

Article Outline

• Abstract
• Methods
  • Sample collection
  • Statistical analyses
• Results
  • Distributions of allergen concentrations
  • Mouse allergen and household characteristics
  • Comparability with National Cooperative Inner-City Asthma Study results
• Discussion
• Acknowledgment
• References
• Copyright

Background

Exposure to mouse allergen is a known cause of asthma in occupational settings and exhibits high prevalence and association with allergic sensitization in inner-city home environments. It has never been characterized on a nationally representative scale.

Objective

This study was designed to characterize mouse allergen prevalence in a representative sample of US homes and to assess risk factors for increased concentrations.

Methods

Allergen, questionnaire, and observational data were analyzed from the first National Survey of Lead and Allergens in Housing, a cross-sectional survey of 831 US housing units. Allergen levels were characterized and related to demographic factors and household characteristics.

Results

Detectable levels of mouse allergen (Mus m 1) exist in 82% of US homes. Kitchen floor concentrations exceed 1.6 μg/g, a level associated with increased sensitization rates, in 22% of homes. Increased concentrations (>1.6 μg/g) were observed in high-rise apartments and mobile homes, older homes, and low-income homes. Odds of having increased concentrations were increased when rodent (odds ratio [OR], 3.38) or cockroach (OR, 1.81) problems were reported and when floor mopping (OR, 2.17) was performed instead of vacuuming.

Conclusions

Household mouse allergen is widespread in many settings at levels that might contribute to asthma morbidity. The likelihood of exposure can be assessed by consideration of demographic and household determinants.

Key words: Asthma, allergens, mouse allergen, Mus m 1

Abbrevations used: NCICAS, National Cooperative Inner-City Asthma Study, NIEHS, National Institute of Environmental Health Sciences, NSLAH I, The first National Survey of Lead and Allergens in Housing

Exposure to rodent allergens and associations with asthma or allergic diseases have been characterized with increasing clarity through focused observational studies of specific populations.¹, ², ³, ⁴, ⁵, ⁶, ⁷, ⁸ Mouse allergen in particular has been frequently studied in occupational settings to investigate exposure and response among laboratory animal handlers.⁹, ¹⁰, ¹¹, ¹², ¹³ More recent research has examined home environments, revealing potentially important relationships between household mouse allergen exposure and sensitization among children.¹⁴, ¹⁵

A major study targeting the homes of children with asthma living in several inner-city areas found a strikingly high prevalence of mouse allergen and increased mouse allergen sensitization rates.¹⁵ However, in the same study wide variation was observed in kitchen mouse allergen levels between different cities.¹⁴ In particular, about a 25-fold difference was seen between cities having the lowest and highest median concentrations. This strong geographic variation and the narrowly focused population of study are suggestive of possible limitations regarding the scope and applicability of these results on a broader scale.

Nationally representative data are needed to provide a broadly applicable characterization of household mouse allergen levels and their determinants. In this article, such data are taken from the first National Survey of Lead and Allergens in Housing (NSLAH I), which was conducted from 1998 to 1999 by the National Institute of Environmental Health Sciences (NIEHS) and the US Department of Housing and Urban Development. The objectives of this article are to provide the first nationally representative estimates of mouse allergen prevalence at multiple locations within households and to identify demographic factors and housing characteristics associated with high mouse allergen levels. Through those objectives, the larger goals are to characterize household mouse allergen exposure nationwide, to assist clinicians in assessing the likelihood of a patient's exposure, and to generate further research hypotheses for intervention studies.

Back to Article Outline

Methods 

NSLAH I was a cross-sectional survey of the US population of 96 million permanently occupied, noninstitutional housing units that permit resident children and was carried out from 1998 through 1999. A complex and multistage design was used to sample and gain participation from 831 housing units containing 2456 individuals in a total of 75 locations across the United States. At each home, a questionnaire was administered to an adult householder, environmental samples were collected, and observations were recorded. A detailed description of the survey design, methodology, and response rates can be found elsewhere.¹⁶, ¹⁷ The survey was approved by the NIEHS Institutional Review Board on June 16, 1998, and in each home, informed consent was obtained in writing from an adult household member.

Sample collection 

Dust samples used in this analysis were collected from the kitchen floor, living room floor, upholstered living room furniture, a randomly selected bedroom bed, and bedroom floor by using a Eureka Mighty-Mite 7.0-A vacuum cleaner (Eureka Co). A 19 mm × 90 mm cellulose extraction thimble (Whatman International, Ltd) was placed in the distal end of the vacuum's extension tube, sealed with a rubber o-ring, and covered with a clean crevice tool. Details of dust collection protocols are described elsewhere.¹⁶

At the laboratory, dust samples were sieved through 425-μm pore grating, weighed, and divided into 100-mg aliquots of fine dust. Dust aliquots were extracted in borate-buffered saline and clarified by means of centrifugation. Supernatants were decanted and stored at −20°C. Allergen concentrations were measured according to previously published methods.¹⁶, ¹⁸, ¹⁹ Allergen concentrations reported in this article are of Mus m 1, or mouse urinary protein, measured in micrograms of allergen per gram of sampled dust. For most samples, the lower limit of detection of the assay was 0.25 μg/g. Allergen loads are calculated as the product of concentration and dust weight measured in micrograms of allergen per square meter of sampled area. Because some dust samples were not collected and because some samples had too little dust to analyze for all allergens, there were some missing concentration values.

Statistical analyses 

Spearman rank correlation coefficients were calculated as a robust measure of association between allergen concentrations. Odds ratios (ORs) and 95% CIs were estimated by using logistic regression and Wald F test statistics. Factors were selected for modeling on the basis of hypothesized relevance gleaned from the literature or other sources. All percentages, correlations, means, percentiles, and ORs were weighted to represent the US population of permanently occupied, noninstitutional housing units that permit resident children. SEs, CIs, and P values were developed in accordance with the complex survey design by using Taylor series linearization methods. Statistical analyses were conducted in SUDAAN, Release 8.0 (Research Triangle Institute) and S-Plus (version 6, Release 2). A detailed description of the statistical weighting for the NSLAH I can be found elsewhere.¹⁶

Back to Article Outline

Results 

The weighted NSLAH population is, by design, comparable with the US population of permanently occupied, noninstitutional housing units that permit resident children: 28% in urban areas with populations of greater than 1 million, 39% with children less than 18 years of age, 80% white, 8% Hispanic, and 80% above the poverty level.

Distributions of allergen concentrations 

Detectable concentrations of mouse allergen were found in at least one sampling location of an estimated 82% of US homes. Kitchen floors exhibited the highest prevalence, with 57% exceeding the lower limit of detection and with 22% having concentrations of greater than 1.6 μg/g, a level previously found to be associated with significantly increased mouse allergen sensitization rates. Table I shows the median (50th percentile) and geometric mean of mouse allergen concentration and load in US homes.

Table I. Estimated distribution of mouse allergen concentration and load in US homes

Spearman rank correlations of mouse allergen concentrations between the sampling locations ranged from 0.17 (bedroom bed and kitchen floor) to 0.43 (living room floor and living room upholstery). All correlations among the 3 floor surfaces (kitchen, bedroom, and living room) were between 0.29 and 0.31.

Among other measured allergen concentrations, mouse was most highly correlated with Alternaria species (Alt a 1) in a range of 0.22 to 0.38 across the sampling locations and cockroach (Bla g 1) in a range of 0.14 to 0.25.

Mouse allergen and household characteristics 

To investigate associations between mouse allergen and various demographic factors, we tested the equality of the geometric mean kitchen floor concentration across levels of the factors shown in Table II. Kitchen floor concentrations were used because they were previously found to exhibit the strongest relationship to sensitization relative to a threshold of 1.60 μg/g.¹⁵ Generally higher concentrations were observed in high-rise apartments, mobile homes, and duplex-triplex residences, with the lowest concentrations in low-rise apartments. Stated in terms of risk, ORs for elevated (>1.60 μg/g) concentrations were 2.28 for high-rise apartments and 2.98 for mobile homes, each as compared with detached single-family homes. Concentrations consistently increased with increasing age of the home and with decreasing household income. Only slight differences were observed according to geographic region of the country, degree of urbanization, and presence of a child in the home.

Table II. Estimated percentage of US households with detectable kitchen floor mouse allergen concentrations, levels exceeding 1.60 μg/g, and the geometric mean concentration, according to demographic factors

Factor	No. of homes sampled	Percent detectable (SE)	Percent >1.60 μg/g (SE)	Geometric mean (SE), μg/g
Total	735	57.0 (2.1)	21.7 (2.1)	0.52 (0.04)
Type of dwelling (P = .009)∗
Detached single family	487	57.2 (2.7)	18.8 (2.6)	0.48 (0.04)
Duplex-triplex	48	67.7 (7.8)	37.4 (6.8)	0.80 (0.21)
Row house	36	50.3 (11.9)	23.7 (6.8)	0.55 (0.19)
Low-rise apartment (1-4 floors)	74	40.7 (8.1)	16.1 (4.3)	0.37 (0.07)
High-rise apartment (≥5 floors)	15	81.5 (10.3)	34.6 (15.6)	1.98 (1.44)
Mobile home	38	80.0 (7.4)	40.8 (13.3)	1.08 (0.38)
Construction year (P = .003)
1978-1998	194	50.4 (4.8)	21.2 (3.8)	0.45 (0.06)
1960-1977	227	53.3 (4.8)	18.3 (2.9)	0.43 (0.04)
1946-1959	123	55.8 (4.8)	23.2 (4.5)	0.53 (0.09)
1940-1945	42	72.7 (9.7)	21.1 (6.5)	0.71 (0.20)
1939 or earlier	149	69.0 (3.1)	26.5 (4.0)	0.73 (0.07)
Geographic region (P = .642)
Northeast	130	55.1 (4.7)	18.4 (2.7)	0.46 (0.05)
Midwest	178	56.6 (4.1)	21.5 (2.1)	0.55 (0.06)
South	256	57.1 (4.1)	23.4 (4.5)	0.48 (0.08)
West	171	59.2 (3.5)	21.7 (5.2)	0.59 (0.12)
Urbanization (P = .742)
MSA ≥1 million population	245	57.4 (3.3)	20.1 (2.2)	0.56 (0.05)
MSA <1 million population	362	53.2 (3.2)	20.9 (4.0)	0.48 (0.07)
Non-MSA	128	63.9 (4.1)	25.0 (2.1)	0.54 (0.06)
Household income (P = .008)
$0-$19,999	166	66.9 (4.0)	32.9 (4.6)	0.81 (0.15)
$20,000-$39,999	199	57.3 (4.9)	23.6 (3.6)	0.54 (0.08)
$40,000-$59,999	141	55.2 (5.6)	14.5 (3.8)	0.39 (0.04)
≥$60,000	174	47.2 (4.8)	17.0 (3.1)	0.42 (0.06)
Child resident (P = .779)
Child resident <18 y old	354	52.9 (3.8)	21.1 (2.9)	0.50 (0.05)
No child resident	378	59.6 (2.3)	22.2 (2.3)	0.52 (0.04)

MSA, Metropolitan statistical area.

Table III provides a more detailed view of the relationship between allergen level and construction year for each dwelling type. Most dwelling types reflected the overall pattern of increasing concentrations with age of the home. Exceptions were duplex-triplex and mobile homes. For this analysis, limited numbers of homes in several subcategories necessitated collapsing across construction-year ranges and defining different construction-year groupings for mobile homes.

Table III. Estimated percentage of US households with kitchen floor mouse allergen concentrations exceeding 1.60 μg/g, by construction year and type of dwelling

After accounting for demographic factors, specific household characteristics were analyzed to investigate their ability to predict higher levels of kitchen floor mouse allergen relative to 2 thresholds: 0.52 μg/g (the estimated national geometric mean) and 1.60 μg/g. Results are displayed in Table IV. Higher mouse allergen levels were observed in the presence of characteristics associated with rodent or cockroach activity. Floor mopping was also associated with higher levels compared with vacuuming.

Table IV. Adjusted^∗ ORs (95% CIs) for increased kitchen floor mouse allergen concentration, according to household characteristics

Comparability with National Cooperative Inner-City Asthma Study results 

NSLAH I data were used to define a subpopulation, restricted to households in low-income urban neighborhoods, to facilitate comparison against selected results from the National Cooperative Inner-City Asthma Study (NCICAS)¹⁴ strictly for mutual validation purposes. The subpopulations are not identical, primarily because the NSLAH I sample size prevents further reduction to only include households of children with diagnosed asthma; however, the demographic-based restriction alone was deemed sufficient to support a general comparison (Table V).

Table V. Results from a low-income urban subpopulation of NSLAH I compared with NCICAS subpopulation and to all US homes

Prevalence of detectable mouse allergen was comparable and, in some respects, identical between the 2 subpopulations. Both studies found that 95% of low-income urban homes had detectable mouse allergen in at least one room and that 83% to 87% had detectable levels in the kitchen. The prevalence of increased kitchen concentrations and the correlation of concentrations between rooms differed somewhat between the 2 studies, but these were not incongruent in view of the high variability seen across NCICAS cities.

Back to Article Outline

Discussion 

This article provides the first nationally representative estimates of household mouse allergen prevalence and finds that prevalence of mouse allergen is widespread, with detectable levels in 82% of all homes, which is less but not dramatically lower than the 95% prevalence in inner-city homes alone, as found in this and other studies.¹⁴ This study also finds that 22% of US kitchen floors exhibit elevated concentrations relative to the previously established 1.6 μg/g threshold, as related to allergic sensitization.¹⁵ These results provide an important perspective on the breadth of health effects potentially associated with exposure to mouse allergen. Although perhaps greater in low-income urban environments, the allergen is widespread, and elevated levels are not restricted to those environments.

Elevated mouse allergen levels are most prevalent in pre-1945 construction, households with incomes of less than $20,000, and high-rise apartments, mobile homes, and duplex-triplex residences. Apart from these factors, levels of mouse allergen do not vary appreciably across large geographic quadrants, urban versus rural settings, or households with and without resident children.

After accounting for the demographics, elevated exposure risk is most strongly associated with the reported or observed presence of rodents or cockroaches, as expected. ORs for these factors range between 1.58 and 3.38. Also, kitchen floor mopping, as opposed to vacuuming, carries a marginal increase in risk of exposure. This was not found in some prior research and provides added context to what is known about disturbance and activity levels increasing airborne allergen exposure.¹⁹, ²⁰ Type of flooring and presence of food debris are not associated with elevated risk for kitchen floor allergen levels; however, in other (nonkitchen) rooms, allergen levels and food debris did exhibit such associations. For example, food debris observed in the living room is associated with elevated living room upholstery mouse allergen levels (OR, 2.61; 95% CI, 1.85-3.67). Our results also suggest that working with animals does not necessarily translate into elevated mouse allergen levels in the home; however, our question on occupational exposure did not differentiate types of animal work, and a more specific question on mouse-related occupations might have illuminated a real association relative to the 1.6 μg/g threshold.

On the basis of a completely data-driven prediction model generated through consideration of all factors and backward elimination model fitting (not shown), essentially these same factors were found to constitute independent predictors of increased mouse allergen concentration: dwelling type, construction year, household income, reported problems with rodents, reported problems with cockroaches, and floor-cleaning method.

Allergen levels vary within the home but correlate significantly between rooms and between floored and upholstered surfaces within a room. This finding is consistent with research on airborne allergens in occupational settings, which suggested small-particle transportation of the allergen into rooms without mice, in some cases over substantial distances.²¹ Thus direct contact is not a necessary condition for exposure, but avoidance of areas in which mice are present should reduce risk.²², ²³, ²⁴

This study, which is demonstrably consistent with prior research while extending the scope and mitigating the inherent variability thereof, indicates widespread prevalence of mouse allergen in homes and demonstrates where the risk is greatest. These results might help clinicians to assess whether a patient is likely to be exposed and suggest measures to reduce this exposure. Our results further suggest the need for additional investigation in longitudinal studies of mouse allergen in relation to health outcomes.

Back to Article Outline

We thank Michael Muilenberg and Harriet Burge of the Harvard School of Public Health for their assistance in performing the allergen ELISAs; the field staff at Westat, Inc, who collected the data and environmental samples; and the study participants who generously provided their time and access to their homes. We also thank Drs Stephanie London and Donna Baird of the NIEHS for their helpful comments during the preparation of this manuscript.

Back to Article Outline

References 

1. Cullinan P, Lowson D, Nieuwenhuijsen MJ, et al. Work related symptoms, sensitization and estimated exposure in workers not previously exposed to laboratory rats. Occup Environ Med. 1994;51:589–592
   • View In Article
   • MEDLINE
   • CrossRef
2. Bryant DH, Boscato LM, Mboloi PN, Stuart MC. Allergy to laboratory animals among animal handlers. Med J Aust. 1995;163:415–418
   • View In Article
   • MEDLINE
3. Eggleston PA, Ansari AA, Zeimann B, Adkinson NF. Occupational challenge studies with laboratory workers allergic to rats. J Allergy Clin Immunol. 1990;86:63–72
   • View In Article
   • MEDLINE
   • CrossRef
4. Eggleston PA, Ansari AA, Adkinson NF, Wood RA. Environmental challenge studies in laboratory animal allergy. Am J Respir Crit Care Med. 1995;151:640–646
   • View In Article
   • MEDLINE
5. Bush RK, Wood RA, Eggleston PA. Laboratory animal allergy. J Allergy Clin Immunol. 1998;102:99–112
   • View In Article
   • Abstract
   • Full Text
   • Full-Text PDF (237 KB)
   • CrossRef
6. Krakowiak A, Szulc B, Gorski P. Allergy to laboratory animals in children of parents occupationally exposed to mice, rats, and hamsters. Eur Respir J. 1999;14:352–356
   • View In Article
   • MEDLINE
   • CrossRef
7. Heederik D, Venables KM, Malmberg P, et al. Exposure-response relationships for work-related sensitization in workers exposed to rat urinary allergens: results from a pooled study. J Allergy Clin Immunol. 1999;103:678–684
   • View In Article
   • Abstract
   • Full Text
   • Full-Text PDF (49 KB)
   • CrossRef
8. Lieutier-Colas F, Meyer P, Larsson P, et al. Difference in exposure to airborne major rat allergen (Rat n 1) and to endotoxin in rat quarters, according to tasks. Clin Exp Allergy. 2001;31:1449–1456
   • View In Article
   • MEDLINE
   • CrossRef
9. Phipatanakul W. Rodent allergens. Curr Allergy Asthma Rep. 2002;2:412–416
   • View In Article
   • MEDLINE
   • CrossRef
10. Sakaguchi M, Inouye S, Miyazawa H, Kamimura H, Kimura M, Yamazaki S. Evaluation of countermeasures for reduction of airborne mouse allergens. Lab Anim Sci. 1990;40:613–615
    • View In Article
    • MEDLINE
11. Jones RB, Kacergis JB, MacDonald MR, et al. The effect of relative humidity on mouse allergen levels in an environmentally-controlled mouse room. Am Ind Hyg Assn J. 1995;56:398–401
    • View In Article
12. Renstrom A, Malmberg P, Larsson K, Larsson PH, Sundblad B-M. Allergic sensitization is associated with increased bronchial responsiveness: a prospective study of allergy to laboratory animals. Eur Respir J. 1995;8:1514–1519
    • View In Article
    • MEDLINE
13. Gordon S, Kiernan LA, Nieuwenhuihsen MJ, Cook AD, Tee RD, Newman Taylor AJ. Measurement of exposure to mouse urinary proteins in an epidemiological study. Occup Environ Med. 1997;54:135–140
    • View In Article
    • MEDLINE
    • CrossRef
14. Phipatanakul W, Eggleston PA, Wright EC, Wood RA, Mouse allergen I. The prevalence of mouse allergen in inner-city homes. The National Cooperative Inner-City Asthma Study. J Allergy Clin Immunol. 2000;106:1070–1074
    • View In Article
    • Abstract
    • Full Text
    • Full-Text PDF (71 KB)
    • CrossRef
15. Phipatanakul W, Eggleston PA, Wright EC, Wood RA, Mouse allergen II. The relationship of mouse allergen exposure to mouse sensitization and asthma morbidity in inner-city children with asthma. The National Cooperative Inner-City Asthma Study. J Allergy Clin Immunol. 2000;106:1075–1080
    • View In Article
    • Abstract
    • Full Text
    • Full-Text PDF (109 KB)
    • CrossRef
16. Vojta PJ, Friedman W, Marker D, et al. The First National Survey of Lead and Allergens in Housing: survey design and methods for the allergen component. Environ Health Perspect. 2002;110:527–532
    • View In Article
    • MEDLINE
    • CrossRef
17. Jacobs DE, Clickner RP, Zhou JY, et al. The prevalence of lead-based paint hazards in U.S. Housing. Environ Health Perspect. 2002;110:A599–A606
    • View In Article
    • MEDLINE
    • CrossRef
18. Swanson MC, Agarwal MK, Reed CE. An immunochemical approach to aeroallergen quantitation with a new volumetric air sampler: studies with mite, roach, cat, mouse and guinea pig antigens. J Allergy Clin Immunol. 1985;76:724–729
    • View In Article
    • MEDLINE
    • CrossRef
19. Twiggs JT, Agarwal MK, Dahlberg MJF, Yunginger JW. Immunochemical measurement of airborne mouse allergens in a laboratory animal facility. J Allergy Clin Immunol. 1982;69:474–477
    • View In Article
    • MEDLINE
    • CrossRef
20. Eggleston PA, Newill CA, Ansari AA, et al. Task related variation in airborne concentrations of laboratory animal allergens: studies with Rat n 1. J Allergy Clin Immunol. 1989;84:347–352
    • View In Article
    • MEDLINE
    • CrossRef
21. Ohman JL, Hagberg K, MacDonald MR, Jones RR, Paigen BJ, Kacergis JB. Distribution of airborne mouse allergen in a major mouse breeding facility. J Allergy Clin Immunol. 1994;94:810–817
    • View In Article
    • Abstract
    • Full-Text PDF (784 KB)
    • CrossRef
22. Hollander A, Heederik D, Doekes G. Respiratory allergy to rats: exposure-response relationships in laboratory animal workers. Am J Respir Crit Care Med. 1997;155:562–567
    • View In Article
    • MEDLINE
23. Venables KM, Tee RD, Hawkins ER. Laboratory animal allergy in a pharmaceutical company. Br J Ind Med. 1988;45:660–666
    • View In Article
    • MEDLINE
24. Chapman MD, Wood RA. The role and remediation of animal allergens in allergic diseases. J Allergy Clin Immunol. 2001;107:414–421
    • View In Article
    • Abstract
    • Full-Text PDF (135 KB)
    • CrossRef