House dust mite allergen levels in households and correlation with allergic rhinitis symptoms Yanjun Wang, M.D.,1,2 Liyan Xiong, M.B.B.S.,1 Xiaoyan Yin, M.D.,3 Jinghui Wang, M.D.,4 Quanming Zhang, M.D.,5 Zizhong Yu, M.D.,1 Guoqing Gong, M.D.,1 Yiwu Zheng, Ph.D.,6 Jianjun Chen, M.D.,1 and Weijia Kong, M.D.1,2

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ABSTRACT

Background: House dust mite (HDM) allergen is a risk factor for the development of allergic rhinitis (AR). Objectives: To determine the levels of indoor allergens in the households of patients with AR in Wuhan city, identify the environmental risk factors for high allergen exposure, and investigate the correlations between allergen exposure and specific immunoglobulin E levels and symptoms. Methods: The study examined 50 patients with AR. Two dust samples were collected from the bedding of each patient, one in summer and one in winter. Major allergens Der p 1 and Der f 1, from Dermatophagoides pteronyssinus and Dermatophagoides farinae, were measured with an enzyme-linked immunosorbent assay. Participants completed a standardized questionnaire about their living environments, and their rhinitis symptom scores were calculated. Specific immunoglobulin E levels against Der p and Der f were measured. Results: The percentage of bedding samples with high HDM allergen (Der f 1 ⫹ Der p 1) levels (⬎10 ␮g/g) was 44% in summer and 46% in winter. There was no significant difference between the level of mite allergens in summer and winter; however, the level of Der f 1 was higher than that of Der p 1 (p ⬍ 0.05). The age of the mattress and pillow was significantly correlated with allergen concentration. Indoor HDM allergen level affected the severity of nasal itching. Conclusions: HDMs are important indoor allergens in Wuhan. Mattresses and pillows that have been used for a long time contain high levels of allergens. High levels of exposure to HDM allergens correlates with the severity of nasal itching. (Am J Rhinol Allergy 28, e193–e196, 2014; doi: 10.2500/ajra.2014.28.4095)

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ouse dust mites (HDMs) are the most important source of indoor allergens in the world.1–4 Clinical reports5–8 from China have shown that HDM allergens are the main cause of sensitization in patients with perennial allergic rhinitis (AR). Li et al.9 demonstrated that HDM sensitization in the skin-prick test is approximately 60% in allergy patients in mainland China. A study in Guangzhou showed that more than 88% of households live with high levels of HDM allergens.10 However, indoor allergen levels in Chinese households have not been determined. The influence of HDM allergen levels on patient symptoms has not been fully investigated in China. This study was conducted to determine HDM allergen levels in the households of AR patients in central China, to investigate the risk factors in their living environments, and to explore the correlations between the exposure levels and specific immunoglobulin E (sIgE) levels and clinical symptoms.

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Department of Otorhinolaryngology and 2Institute of Otorhinolaryngology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China, 3Department of Otorhinolaryngology, The Second Hospital of Hebei Medical University, China, 4Department of Otorhinolaryngology, The First Hospital of Handan, Hebei, China, 5Departments of Otorhinolaryngology, Shenzhen Nanshan Hospital, Shenzhen, China, and 6Research and Development, ALK, Asia Pacific This work was supported by grants from the Research and National Promotion of Early Detection, Standardized Diagnosis and Treatment, and Preventive Strategy for Major Otology and Rhinologic Diseases (201202005), Wu Jieping Medical Foundation (LC1345), Foundation of Hubei Province Key Laboratory of Molecular Imaging (02.03.2013– 64), the National Natural Science Foundation of China (30901659), and the National Key Technology R&D Program from the Ministry of Science and Technology of China (2007BAI18B15) Yanjun Wang and Liyan Xiong contributed equally to this work The authors have no conflicts of interest to declare pertaining to this article Address correspondence to Weijia Kong, M.D., Department of Otorhinolaryngology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, 1277 Jiefang Avenue, Wuhan 430022, China E-mail address: [email protected] Copyright © 2014, OceanSide Publications, Inc., U.S.A.

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MATERIALS AND METHODS Subjects

Fifty AR patients who visited the Department of Otorhinolaryngology, Union Hospital of Tongji Medical College were recruited for this study. The patients (who had never used nasal medications) had at least two of the following symptoms: nasal obstruction, nasal itching, running nose, or sneezing. These symptoms were not caused by a cold or the flu. Each subject’s sensitization to HDM was detected with a skin-prick test. All of the subjects or their guardians signed a written informed consent before the study, which was approved by the medical ethics committee of Huazhong University of Science and Technology.

Dust sample collection and extraction Two dust samples were collected from each subject’s living environment, one in summer (July to August 2011) and one in winter (January to February 2012). All of the subjects had been living in their homes for at least one year before dust collection and were asked not to replace their bedding for two weeks before dust collection. Dust was sampled by a trained technician using a hand-held vacuum cleaner equipped with a filter trap (ALK, Hørsholm, Denmark); the aim was to get more than 1.0 gram per sample. Dust samples were collected from the sheets, pillowcases, pillows, quilts, and mattresses. Samples were stored at ⫺18°C before the dust was extracted from them as large particles using 0.125M NH4(HCO3) for 2 hours at room temperature and gentle shaking. The extracted solution was then filtered through a 0.22-␮m filter and stored at ⫺18°C until it was analyzed.

Allergen level measurement Allergen detection in the extracted dust samples was performed by sandwich enzyme-linked immunosorbent assay with monoclonal antibodies against Der p 1 and Der f 1, from Dermatophagoides pteronyssinus and Dermatophagoides farinae. All of the antibodies and allergens were from ALK. The sample results are reported as micrograms of Der p 1/Der f 1 per gram of dust. To allow comparison, HDM

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allergen levels of Der p 1 and Der f 1 were calibrated against commercial allergen standards (INDOOR Biotechnologies, Charlottesville, VA). The lower limit of enzyme-linked immunosorbent assay measurement is 0.0060 ␮g/g for Der p 1 and 0.0054 ␮g/g for Der f 1.

Table 1. Concentration of allergen in winter and summer (␮g/g)

Questionnaire about living environment

Der p 1 Der f 1 Der p 1 ⫹ Der f 1

A standardized questionnaire was administered by a trained technician on the day of the dust sample collection. The questionnaire included 19 items: years of living in this environment; age of building; house/flat size; which floor lived on; number of floors in building; pets or not; what kind of pets; pets in the bedroom; use of air conditioning (heating installation) or not; materials of pillow, quilt, sheet, and mattress; the ages of pillow, quilt, sheet, and mattress; frequency of changing the bedding; and time since last bedding change.

The severity of nasal symptoms (nasal blockage, itching, rhinorrhea, and sneezing) was recorded on the day the first dust sample was collected. A four-point scale was used to evaluate each symptom: 0 ⫽ no symptom; 1 ⫽ mild; 2 ⫽ moderate; and 3 ⫽ serious. Total scores were calculated to measure the overall severity of the symptoms.

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Risk factors of indoor allergens The 19 environmental factors in the questionnaire were analyzed using multivariate linear regression analysis and stepwise method selection. The retained risk factors for indoor allergens were age of pillow and age of mattress (Table 2).

Correlation of HDM allergen concentrations and serum sIgE or nasal symptoms The correlations between indoor allergen concentrations and serum sIgE or nasal symptoms are shown in Table 3. No significant relation-

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Our data suggest that HDM is an important allergen source in central China. In both summer and winter, HDM allergen levels are high in households. In this study, the mean Der p 1 ⫹ Der f 1 levels in summer and winter were 11.48 and 12.12 ␮g/g, respectively. The percentage of samples with high levels (⬎10 ␮g/g) of Der p 1 ⫹ Der f 1 was 44% in summer and 46% in winter; only 10% of the samples were under 2 ␮g/g. This is consistent with the premise that HDM allergen levels above 10 ␮g/g are likely to be associated with allergy symptoms.11 Previous studies12–14 reported variable levels of Der p 1 and Der f 1 in the United States and Europe, but HDM allergen exposure was generally lower than in our investigation. Der f 1 levels were higher than Der p 1 (p ⬍ 0.01) in this study. There is no obvious explanation for this observation, but it may be due to differences in the two biologic species.2 Our results demonstrated that there was no significant difference between HDM allergen levels in winter and summer, which is consistent with the report by Li et al.,9 which showed that there were no robust changes in sensitization to Der p and Der f in a 12-month period in four regions of China. It has been shown that the temperature in homes is controlled by residents, regardless of the season.15 An integrated measurement for one heating season can thus predict the indoor climate for other heating seasons. In addition, the popular use of air conditioners and heating systems makes for constant indoor temperatures and humidity levels in this study. However, Feng et al.16 found a seasonal distribution of HDMs in regions in central China, including Wuhan.17 HDMs reached a peak in summer and a trough in winter (see Fig. 1). Our results indicate that there was a significant correlation between HDM allergen level and the age of pillows and mattresses. Previous studies18,19 suggested that the age of a mattress was associated with bedding dust mites. Frequent replacement of mattresses can reduce the concentration of dust mites. Other factors such as age and size of the building, pets, material of pillows and mattresses, cleaning frequency, etc. had no influence on indoor dust mites in this study. In our study, the adjusted R2 for the multiple regression analyses were 0.450 and 0.389. This means that 45% of the variation was explained by factors considered in this study. Our data suggest that allergic patients should be advised to use newer pillows and mattresses to lower HDM allergen levels. The concentrations of Der p 1 ⫹ Der f 1 were positively related to nasal itching symptoms. Allergic sensitization to HDM and asthma has been shown to be related to HDM allergens at an early age in children.20 However, few published data show the correlation between nasal itching symptoms and HDM allergens. Moon and Choi21 found that nasal symptoms were alleviated after environment control of mite exposure in AR patients, whereas Rijssenbeek-Nouwens et al.22 found no change of rhinitis symptoms with environment control. In our study, patients were only sensitized to HDM, which reduced

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Statistical analysis

Fifty patients were recruited in the study, including 24 males and 26 females. The average age was 21.4 ⫾ 13.9 years old. A hundred dust samples (two samples, one in summer and one in winter, for each patient) were collected. The indoor allergen concentrations are shown in Table 1. The mean Der f 1 levels in summer and winter were 7.27 and 7.26 ␮g/g, respectively. Compared with the levels of Der f 1 in summer and winter, Der p 1 was lower (4.21 and 4.86 ␮g/g, respectively); however, there was no significant difference between HDM allergens in winter and summer (p ⬎ 0.05).

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DISCUSSION

Rhinitis symptom scores

Allergen levels

p 0.642 0.995 0.766

ship was found between the exposure level of indoor HDM allergens and sIgE in serum (r ⫽ ⫺0.249, r ⫽ ⫺0.313; p ⬎ 0.05) (data not shown). There was a weak positive significant correlation between nasal itching symptom scores and concentrations of HDM allergen (r ⫽ 0.302, p ⫽ 0.039).

Serum samples were obtained and stored at ⫺18°C until the sIgE tests. The UniCAP100 automatic diagnostic system was used for sIgE determination of Der p and Der f.

RESULTS

Winter 4.86 ⫾ 8.58 7.26 ⫾ 9.46 12.12 ⫾ 12.64

Plus-minus values are means ⫾ standard deviation. Data for allergens are the means of within-person medians.

sIgE detection

Excel 2007 was used for data sorting and SPSS 17.0 was used for statistical analyses. HDM allergens from the winter and summer beddings were compared using the ␹2 test. The results were expressed as means ⫾ standard deviation with 95% confidence intervals. Multivariate regression analysis was used to analyze the risk factors for allergen content in the living environment. A Pearson correlation coefficient was used to measure the correlation between variables. Linear regression was used to analyze the rhinitis symptom scores total score, and the correlation of nasal symptoms was assessed using the stepwise screening method. A p value of less than 0.05 was considered significant.

Summer 4.21 ⫾ 4.87 7.27 ⫾ 6.13 11.48 ⫾ 8.34

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Table 2. Correlation between HDM allergen (Der p 1 ⴙ Der f 1) and age of pillow and mattress Model

Not Standardized Parameters B regression coefficient Standard error

Constants in winter Age of pillow Age of mattress Constants in summer Age of mattress

48.268 4.129 4.565 37.978 13.295

Standardized Coefficients

t

p

— 0.384 0.345 — 0.644

1.054 2.388 2.142 1.226 5.458

0.298 0.022 0.038 0.227 0.049

37.848 1.729 2.131 24.665 2.436

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The HDM concentrations (Der p 1 ⫹ Der f 1) were calculated with multivariate linear regression. F ⫽ 16.786; R2 ⫽ 0.450 Winter: Der p 1 ⫹ Der f 1 ⫽ 48.268 ⫹ 4.129 * age of pillow ⫹ 4.565 * age of mattress F ⫽ 26.701 R2 ⫽ 0.389 Summer: Der p 1 ⫹ Der f 1 ⫽ 37.978 ⫹ 13.295 * age of mattress. Table 3. Spearman correlation between exposure level to allergen and nasal symptoms Nose Blockage r p Der p 1 Der f 1 Der p 1 ⫹ Der f 1

0.019 ⫺0.076 ⫺0.107

Itching

0.901 0.624 0.472

r

p

0.119 0.239 0.302

0.427 0.118 0.039

Rhinorrhea r p 0.056 0.039 0.034

RSS ⫽ rhinitis symptom scores.

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0.707 0.801 0.819

Sneezing

r

p

0.088 ⫺0.227 ⫺0.203

0.558 0.138 0.172

RSS

r

p

0.014 ⫺0.222 ⫺0.251

0.927 0.148 0.088

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Figure 1. Distribution of allergen levels of HDM. Percentage of dust samples with HDM allergen concentrations less than 2 ␮g/g, 2–10 ␮g/g, and more than 10 ␮g/g of dust. High levels (⬎10 ␮g/g) of Der f 1 were 26% and 22% in summer and winter, respectively. Der p 1 allergen concentrations were 16% and 14%, respectively. The percentage of samples with high levels (⬎10 ␮g/g) of Der p 1 ⫹ Der f 1 was 44% in summer and 46% in winter.

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the interference from other allergens. Patients living in multistory buildings in the urban area of Wuhan city also had low environmental variety. The symptoms of rhinitis were investigated only in summer, avoiding interference from the stimulation of nasal symptoms by cold air in winter; this allowed us to better evaluate the correlation between concentrations of dust mites and nasal symptoms. Our study provided novel evidence that there was no significant correlation between HDM allergen concentrations and levels of sIgE in serum of AR patients. Similarly, no significant correlation was found between the exposure levels of Der p 1/Der f 1 and the sIgE level in the Inner Mongolia region of China.23 Furthermore, a recent study24 reported that no effect was seen in high mite allergens and asthmatic patients with high levels of mite-sIgE. It was also reported that sIgE could vary between different genotypes in the same environment. Kurowski et al.25 showed that in patients with the CD14/ ⫺1359 GG and CD14/⫺159CC genotypes, there was a positive correlation between Der p 1 sIgE and the levels of dust mites in bedding, whereas there was no such correlation in patients with other genotypes. This suggested that specific sensitization and allergies might be

associated with polymorphisms of innate immune response genes and modified by allergen exposure in the environment. In conclusion, our findings provide evidence that HDM allergens are abundant in the urban areas of Wuhan. The allergen concentrations are highly associated with the age of mattresses and pillows. The level of exposure to dust mites is implicated in nasal itching symptoms.

REFERENCES 1.

2. 3.

4.

Voorhorst R, Spieksma-Boezeman MI, and Spieksma FT. Is a mite (Dermatophagoides sp.) the producer of the house-dust allergen? Allergy Asthma (Leipz) 10:329–334, 1964. Arlian LG, Morgan MS, and Neal JS. Dust mite allergens: Ecology and distribution. Curr Allergy Asthma Rep 2:401–411, 2002. McHugh BM, and MacGinnitie AJ. Indoor allergen sensitization and the risk of asthma and eczema in children in Pittsburgh. Allergy Asthma Proc 32(5):372–376, 2011. Sa´nchez-Borges M, Ferna´ndez-Caldas E, Capriles-Hulett A, et al. Mite-induced inflammation: More than allergy. Allergy Rhinol (Providence) 3(1):e25–e29, 2012.

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5.

6.

7.

8. 9.

10. 11.

12.

13.

14.

15.

Hong H, Yang Q, Zuo K, et al; Nasal Health Group, China. A hospital-based survey on the prevalence of bronchial asthma in patients with allergic rhinitis in southern China. Am J Rhinol Allergy 27(6):502–505, 2013. Ding J, Zhang J, Xu F, et al. Analyzing of the inhaled allergens profiles of 890 allergic rhinitis patients. Lin Chung Er Bi Yan Hou Tou Jing Wai Ke Za Zhi 26:164–166, 2012. Chen J, Kong W, Xiang J, et al. Age features of the allergens in allergic rhinitis patients of different age in Hubei area. Lin Chung Er Bi Yan Hou Tou Jing Wai Ke Za Zhi 22:683–685, 694, 2013. Leung R, and Jenkins M. Asthma, allergy and atopy in southern Chinese school students. Clin Exp Allergy 24:353–358, 1994. Li J, Sun B, Huang Y, et al. A multicentre study assessing the prevalence of sensitizations in patients with asthma and/or rhinitis in China. Allergy 64:1083–1092, 2009. Zhang C, Gjesing B, Lai X, et al. Indoor allergen levels in Guangzhou city, southern China. Allergy 66:186–191, 2011. Platts-Mills TA, Thomas WR, Aalberse RC, et al. Dust mite allergens and asthma: Report of a second international workshop. J Allergy Clin Immunol 89:1046–1060, 1992. Huss K, Adkinson NF Jr, Eggleston PA, et al. House dust mite and cockroach exposure are strong risk factors for positive skin test responses in the Childhood Asthma Management Program. J Allergy Clin Immunol 107:48–54, 2001. Chew GL, Burge HA, Dockery DW, et al. Limitations of a home characteristics questionnaire as a predictor of indoor allergen levels. Am J Respir Crit Care Med 157:1536–1541, 1998. Macan J, Kanceljak B, Plavec D, et al. Differences in mite fauna between the continental and Mediterranean climates of Croatia: Microscopy and DustscreenTM test findings. Allergy 58:780–73, 2003. Chew GL, Douwes J, Doekes G, et al. Fungal extracellular polysaccharides, beta (1-⬎3)-glucans and culturable fungi in repeated sampling of house dust. Indoor Air 11:171–178, 2001.

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16. 17.

18.

19.

20.

21.

22.

23.

24.

25.

Feng M, Sun W, and Cheng X. Seasonal dynamics and distribution of house dust mites in China. Biosci Trends 3:210–215, 2009. Zhong LH, Zhou YR, Li MZ, et al. Study on the breeding situations and its allergy of dust mites in Wuhan city. China Public Health 15:757, 1999. Van Strien RT, Verhoeff AP, Brunekreef B, et al. Mite antigen in house dust: Relationship with different housing characteristics in The Netherlands. Clin Exp Allergy 24:843–853, 1994. Kuehr J, Frischer T, Karmaus W, et al. Natural variation in mite antigen density in house dust and relationship to residential factors. Clin Exp Allergy 24:229–237, 1994. Sporik R, Holgate ST, Platts-Mills TA, et al. Exposure to house-dust mite allergen (Der p 1) and the development of asthma in childhood. N Engl J Med 323:502–507, 1990. Moon JS, and Choi SO. Environmental controls in reducing house dust mites and nasal symptoms in patients with allergic rhinitis. Yonsei Med J 40:238–243, 1999. Rijssenbeek-Nouwens LH, Oosting AJ, de Bruin-Weller MS, et al. Clinical evaluation of the effect of anti-allergic mattress covers in patients with moderate to severe asthma and house dust mite allergy: A randomised double blind placebo controlled study. Thorax 57:784– 790, 2002. Wang YL, Zhao X, Li FH, et al. Evaluation of exposure and sensitization to house dust mites among rhinitis patients in the steppe environment of Inner Mongolia. Zhonghua Er Bi Yan Hou Tou Jing Wai Ke Za Zhi 47:19–25, 2012. Woodcock A, Forster L, Matthews E, et al. Control of exposure to mite allergen and allergen-impermeable bed covers for adults with asthma. N Engl J Med 349:225–236, 2003. Kurowski M, Majkowska-Wojciechowska B, Wardzynska A, et al. Associations of allergic sensitization and clinical phenotypes with innate immune response genes polymorphisms are modified by house dust mite allergen exposure. Arch Med Sci 7:1029–1036, 2011. e

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House dust mite allergen levels in households and correlation with allergic rhinitis symptoms.

House dust mite (HDM) allergen is a risk factor for the development of allergic rhinitis (AR)...
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