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. 2019 Aug 11;17(2):789–795. doi: 10.1007/s40201-019-00395-6

Endotoxin and Der p1 allergen levels in indoor air and settled dust in day-care centers in Tehran, Iran

Elahe Shahhosseini 1, Kazem Naddafi 1,2, Ramin Nabizadeh 1,2, Mansour Shamsipour 3, Zahra Namvar 4, Behnoosh Tayebi 5, Raheleh Shokouhi Shoormasti 5, Mohammad Sadegh Hassanvand 2,✉, Masud Yunesian 1,2,✉
PMCID: PMC6985405  PMID: 32030152

Abstract

Background

Allergens like endotoxin and mite allergen Der p 1 are associated with early wheezing and asthma morbidity. Day-care centers can be an important source of exposure to allergens. The aim of this study was to evaluate children’s exposure to endotoxin and mite allergen (Der p 1) associated with total suspended particulate matter (TSP) and settled dust in day-care centers in two phases in years of 2015 and 2016 in Tehran city, Iran.

Methods

Endotoxin and mite allergen Der p 1 in TSP and settled dust were measured in 23 day-care centers in Tehran. After collecting dust samples and weighting them, and then their extraction, Endotoxin and Der p 1 allergen were determined using QCL-1000 Endpoint chromogenic LAL Assay and ELISA, respectively.

Results

The mean concentrations of endotoxin and mite allergen Der p 1 in settled dust were 0.3 EU/mg and 0.2 ng/mg, respectively. The mean concentration of endotoxin and mite allergen Der p 1 in indoor air TSP were 0.8 EU/m3 and 0.4 ng/m3, respectively. A significant negative correlation was found between endotoxin both in settled dust and in TSP with measured relative humidity in winter. Also, moderate correlation was observed between Der p 1 in settled dust and relative humidity in winter; however, the correlation between allergen in TSP and relative humidity was not significant.

Conclusion

Day-care centers can be an important source of endotoxin and Der p 1 allergen, so, implementation of proper interventions in these places can reduce exposure to them.

Keywords: Indoor air, Endotoxin, Der p 1, Mite allergen, Day-care centers, Tehran

Introduction

People spend most of their time in indoor environments; therefore, the existence of indoor pollutants may have considerable adverse health effects, in part because of long exposure times [1, 2]. Poor indoor air quality is one of the risk factors affecting human health and can cause or exacerbate respiratory diseases [3]. Endotoxin is a lipopolysaccharide-protein component of the outer membrane of Gram-negative bacteria that is present everywhere [1, 4–8]. This component induces the immune system and exposure in childhood is thought to have a protective effect against atopic conditions and asthma [1, 6–11]. On the other hand, high levels of endotoxin have been associated with increased wheezing and reduced lung function [1, 4, 7, 11, 12]. Dust mites are an important source of allergens in indoor environments [13]. Exposure to high levels of dust mite allergens can exacerbate asthma and lead to other related diseases such as sinusitis, allergic rhinitis and atopic dermatitis [14, 15]. Several studies have reported endotoxin and Der p 1 allergen levels in indoor environments such as home, school and day-care centers [3, 7, 11, 16–19]. In some of these studies, endotoxin and Der p 1 allergen concentrations were measured in settled dust samples [12, 18–20] and there are few studies on endotoxin and Der p 1 in indoor air and settled dust [7, 21]. The results show that in addition to homes, day-care centers can be an important source of exposure to these environmental risk factors, in part because children spend a considerable portion of their time in these places [9, 14, 16, 17, 20, 22]. The levels of endotoxin and Der p 1 allergen in day-care centers have not been examined in Iran; previously. According to endotoxin and allergens role in the development of allergic diseases [23] and that so far there is no data in this field in Iran, our goal was to evaluate endotoxin and Der p 1 allergen exposures in indoor air total suspended particulate matter (TSP), together with dust fall, in different seasons in day-care centers, in Tehran megacity, the capital of Iran. We also aimed to explore seasonal effects of temperature and humidity on endotoxin and Der p 1 allergen levels.

Materials and methods

Sampling sites and schedule

This is a cross-sectional study that was performed in two phases, April to June 2015, and November 2015 to February 2016, in day-care centers of Tehran. Initially, the list of Tehran day-care centers was taken from the Department of Welfare. Thirty day-care centers were randomly selected from them. The Department of Welfare of Tehran has granted official permissions. Finally twenty-three day-care centers agreed to cooperate (Fig. 1). Simultaneous indoor air TSP and settled dust sampling was performed once during each of the above mentioned phases. Overall, for indoor air TSP and settled dust, 46 samples were collected in the 23 sampling sites. It should be noted that children were not directly involved in this study.

Fig. 1.

Fig. 1

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Map of sampling sites in Tehran

Indoor air TSP sampling

Eight-hour TSP samplers were collected on fiberglass filters (37 mm dia., 1.0 μm pore size, from Whatman) placed in 37 mm closed face cassettes using low-volume air sampling pumps (Flite, SKC) operating at a flow rate of 10 L/min. All TSP filters were conditioned in a desiccator for about 24 to 48 h before and after indoor air sampling. They were then weighed three times using a microbalance (Mettler-Toledo; weight sensitivity of ±2 μg) and the mean weight was considered. Additionally, flow rate of the pumps was monitored at the beginning and end of each sampling period by means of an air rotameter. Samples were collected around 8 am to 4 pm and in presence of children. Indoor air TSP samplers were placed at a height of approximately 120 cm above the ground in the middle of the rooms at least one meter away from the walls, doors, windows, and ventilation inlets. Indoor air TSP samples were packed in aluminum foil and stored at −20 °C until extraction and analysis [7].

Quality assurance and quality control

For quality assurance and quality control (QA/QC), field and laboratory blank filters were used. All samples were analyzed in duplicate to ensure reproducibility.

Indoor settled dust sampling

Settled dust sample were collected using a small vacuum cleaner (Bosch) equipped with a filter holder. Floor dust was collected from an area of 1 m2 of floor of the sampled room. To remove particles greater than 425 μm, collected settled dust from the floor passed through a metal sieve of size 40 mesh. Then the collected dust was weighed three times using the microbalance and the mean weight was recorded. Finally, the settled dust samples were packed in aluminum foil and stored at −20 °C until the extraction and analysis for endotoxin and Der p 1 allergen [7]. Indoor temperature and relative humidity were measured using meteorological sensors.

Measurement of endotoxin and Der p 1 allergen

Indoor air TSP and settled dust samples were divided into two equal fractions. One half of each sample was used for endotoxin and the remaining half was used for Der p 1 allergen analysis.

For endotoxin extraction, indoor air TSP and settled dust samples and blank filters were extracted using a vortex shaker for 1 h in 5 ml of pyrogen-free water plus 0.05% Tween 20 [7, 20, 24]. After being centrifuged for 10 min at 1000 g, the supernatant was used to determine the amount of endotoxin. Endotoxin measurements were performed using the Limulus amoebocyte lysate assay (QCL-1000 Endpint chromogenic LAL Assays) (Lonza) according to the manufacturer’s instructions. The instrument was used for reading endotoxin ELISA reader (BIO TEK) was used for reading endotoxin. The wavelength was 405–410 nm. For Der p 1 allergen extraction, 1 ml PBS (Sigma Poland) plus 0.05% Tween 20 was added to samples and precipitated for 60 min at room temperature. Then, supernatants were analyzed using the ELISA method (Indoor Biotechnologies) [20, 24]. For TSP and for settled dust, considering both endotoxin and Der p 1, limits of detection (LOD) were calculated as 3 times the standard deviation of the blank levels. The mean of blank levels was subtracted from all values above the LOD limits.

Statistical analysis

Descriptive statistics (geometric mean, median, geometric standard deviation and percentiles) were used to characterize the data. The Mann-Whitney test was used to compare endotoxin and Der p 1 allergen concentrations in dust fall and TSP between day-care centers, Correlation between allergen and temperature, relative humidity, building age and area were assessed with Pearson correlation coefficient. A p value of less than 0.05 was considered statistically significant.

Results

Characteristics of sampling sites

In the present work, 63% of day-care centers were villa and single-use. The mean of building area was 270 m2. The number of individuals in kindergartens was in range of 30–117 persons. Age of selected day-care centers was more than 20 years. Ventilation of the buildings occurred both naturally and mechanically. The most common type of cover for floors are hard surfaces and foam, and only rooms for infants were covered with carpet. Typical maintenance practices included cleaned the floor with vacuum cleaner once a day and wiping the desks and chairs once a week. There was no sign of moisture in buildings.

Endotoxin and Der p 1 allergen concentrations in floor dust

Summary statistics for the indoor temperature, relative humidity, settled dust, endotoxin and Der p 1 allergen concentrations in the sampling sites are given in Table 1. In floor dust samples, endotoxin and Der p 1 were detected in 7% and 83% of samples, respectively.

Table 1.

Descriptive statistics for indoor temperature, relative humidity, dust on floor, settled dust endotoxin and Der p 1 allergen levels

Variable GM GSD P25 P50 P75 P95 Min Max

Temperature

(°C)

 24.9 1.09 23.6 24.9 26.2 28.5 20.5 30.5

Relative Humidity

(%)

 31.3 1.32 26.9 30.5 36.0 50.6 17.2 53.2

Dust on floor

(mg/m2)

 5.5 3.34 2.8 5.45 9.1 77.2 0.5 138.0
Endotoxin in floor dust (EU/mg) 0.3 2.86 0.1 0.2 0.9 0.9 0.1 0.9
Endotoxin in floor dust (EU/m2) 5.4 1.67 3.3 5.1 9.2 9.2 3.3 9.2
Der p 1 in floor dust (ng/mg) 0.2 4.27 0.1 0.2 0.6 2.3 0.01 3.8
Der p 1 in floor dust (ng/m2) 1.2 1.18 0.6 1.2 2.8 5.4 0.1 5.9
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GM: geometric mean; GSD: geometric standard deviation; P25, P50, P75, P95: percentiles 25th, 50th, 75th, 95th

The geometric mean concentration of settled dust per m2 of kindergarten floor was 5.5 mg and concentration ranges of endotoxin and Der p 1 allergen per mg of settled dust were 0.1–0.9 EU and 0.01–3.8 ng, respectively (Table 1). The corresponding median concentrations of endotoxin and Der p 1 allergen were 0.2 EU/mg and 0.2 ng/mg (Table 1).

Endotoxin and Der p 1 allergen concentrations in indoor air TSP

The concentrations of indoor TSP and endotoxin and Der p 1 allergen in TSP are summarized in Table 2. In the present study, the proportions of TSP samples exhibiting detected endotoxin and Der p 1 values were 21% and 82%, respectively. The geometric mean concentration of indoor TSP was 205 μg/m3 and concentration ranges of endotoxin and Der p 1 allergen were 0.3–2.8 EU/m3 and 0.03–3.5 ng/m3 of TSP; respectively. The median concentrations of endotoxin and Der p 1 allergen were 0.8 EU/m3 and 0.4 ng/m3 (Table 2).

Table 2.

Descriptive statistics for indoor TSP, endotoxin and der p 1 allergen in TSP

Variable GM GSD P25 P50 P75 P95 Min Max
TSP (μg/m3) 205 2.3 100 200 333 800 67 1497
Endotoxin in TSP (EU/mg) 4.4 2.9 1.7 3.3 9.1 41.6 1.2 41.6
Airborne endotoxin (EU/m3) 0.8 2.1 0.4 0.8 1.8 2.8 0.3 2.8
Der p 1 in TSP (ng/mg) 1.9 2.9 0.9 1.8 3.8 17.1 0.3 17.3
Airborne Der p 1 (ng/m3) 0.4 3.1 0.2 0.4 0.8 2.1 0.03 3.5
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TSP: total suspended particulate matter; GM: geometric mean; GSD: geometric standard deviation; P25, P50, P75, P95: percentiles 25th, 50th, 75th, 95th

Associations between allergens and characteristic of day-care centers

Table 3 displays associations between day-care center characteristics and (i) concentrations of TSP and (ii) Der p 1 allergen concentrations in dust fall and in TSP. There were significant associations between Der p 1 concentrations with type of kitchen (p value = 0.03) and construction in the vicinity of day-care centers (p value = 0.03).

Table 3.

Association of day-care centers characteristics with Der p 1 allergen and TSP levels

Independent variable Dependent variable
Der p 1 in dust fall Der p 1 in TSP TSP
GM (ng/mg) p value GM (ng/m3) p value GM (μg/m3) p value
Type of kitchen
  Open 0.03 0.03 2.7 0.48 232 0.73
  Batch 0.3 2.3 224
Type of child̕̕ room
  With bed 0.1 0.14 1.8 0.14 284 0.14
  Without bed 0.3 2.9 193
Type of humidifier
  Cold 0.4 0.55 2.9 0.16 280 1.00
  warm 0.3 1.6 261
Construction in vicinity of day-care centers
  Yes 0.2 0.78 3.6 0.03 229 0.89
  No 0.2 1.5 221
Cooling system
  Yes 0.3 0.12 3 0.08 231 0.83
  No 0.1 1.4 214
Type of window frame
  Aluminum – – 1.7 0.14 155 0.30
  Iron – – 2.5 236
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TSP: total suspended particulate matter; GM: geometric mean

Correlation between allergen and endotoxin concentrations, temperature, relative humidity, building age and area

Table 4 shows correlation between allergen and endotoxin concentrations, temperature and relative humidity (in seasons of sampling), building age and area. Significant negative correlations were found between endotoxin levels in settled dust and in TSP with measured relative humidity in fall-winter. Also, Der p 1 allergen level in dust fall was moderately correlated with measured relative humidity in fall-winter, building age and area. Correlation between allergen in TSP and relative humidity in any of sampling seasons, age and area of building was not significant. No correlation was observed between Der p 1 allergen and endotoxin concentrations. The correlation between concentrations of allergen in air and in dust samples was low: r = −0.08 for endotoxin and r = − 0.027 for Der p 1.

Table 4.

Correlation between allergen and endotoxin concentrations, temperature and relative humidity in seasons of sampling, building age and area

Dependent variable Independent variable
Temperature Relative humidity Age of building Area of building
Spring-summer Fall-winter Spring-summer Fall-winter
Der p 1 in dust fall

R* = −0.2

p value = 0.29

R = 0.09

p value = 0.65

R = 0.12

p value = 0.52

R = 0.54

p value = 0.004

R = 0.57

p value = 0.001

R = 0.42

p value = 0.02
Der p 1 in TSP

R = −0.03

p value = 0.84

R = −0.05

p value = 0.79

R = −0.2

p value = 0.32

R = 0.27

p value = 0.17

R = 0.21

p value = 0.28

R = 0.32

p value = 0.09
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R* = Pearson correlation coefficient

Discussion

In 82% and 16% of samples taken from day-care centers, Der p 1 allergen and endotoxin were detected, respectively. The geometric mean concentrations for endotoxin in the samples obtained from settled dust and TSP were 0.3 EU/mg (5.4 EU/m2) and 0.8 EU/m3 respectively. These are lower than the results reported by Lai et al. (14.3 EU/mg for dust endotoxin levels and 24.7 EU/m3 for air endotoxin levels) [25]. For Der p 1 concentration in settled dust and TSP (0.2 ng/mg (1.2 ng/m2) and 0.4 ng/m3, respectively). Fromme et al. carried out a study in Germany. The obtained results of geometric mean airborne Der p 1 was 0.14 ng/m3 that is lower than our findings [26]. In other research, geometric mean of Der p 1 levels in settled dust was (0.2 ng/mg) that is accordance with our study [16]. Although endotoxin may have a protective effect in childhood, it can cause exacerbation of asthma and chronic lung obstruction due to induction of inflammatory reactions in individuals [7, 27]. There are no criteria for evaluating endotoxin exposure with respect to allowable concentrations [28] . Exposure to low levels of endotoxin may cause local inflammatory reactions and symptoms such as coughing and phlegm [7, 27]. Der p 1 concentrations only in 4 of samples were higher than the sensitization threshold levels (2 μg/g) [29, 30]. Exposure to lower concentrations of allergens increases time for development of allergic reactions, while allergens are still a potential risk for sensitive children [20, 31, 32]. Continuous exposure to low levels of allergen in individuals with sensitization that have mild asthma, exacerbates symptoms and bronchial hyper responsiveness [33]. Therefore its reduction seems be necessary. The results showed that type of kitchen can affect the concentration of allergen in dust fall. In the open kitchen, the concentration of Der p 1 in dust fall was significantly lower than that of in batch kitchen. Another finding of this study is that construction in the vicinity of day-care centers can be an influencing factor for Der p 1 concentration in TSP. During the construction process, particulate matter is produced which may penetrate nearby day-care centers. Der p 1 is bound to relatively larger particles [3, 26]. Because physical activities of children, such particles may be resuspended after deposition. Significant association and high correlation (r = −0.89 and r = −0. 73) was found between relative humidity of indoor air and endotoxin levels in dust fall and TSP. Although it is assumed that more wet weather would relate to higher levels of endotoxin, higher humidity in the absence of wet areas does not create the water activity to support the growth of bacteria. This finding is similar to results obtained in some studies [7]. Some studies have found no relation between humidity and endotoxin [6]. Unlike endotoxin, significant association with a moderate correlation between the concentration of Der p 1 allergen in settled dust and humidity was observed as in some other studies [34]. The reason could be that high humidity has a considerable influence on the proliferation of dust mite allergens. It was also observed that with increasing building age, allergen concentration also increased (r = 0.57). Zuraimi et al. reported a similar result [30]. New buildings may have smaller amounts of allergens because they are warmer and drier and have more efficient heating and insulation systems [35]. Other factors including type of ventilation and presence of cooling system were analyzed in this study, but no significant associations were observed.

There were some limitations during this study. The most important limitation was that some of day care centers authorities did not cooperate, so we could not sample.

Conclusion

The results show that day-care centers can be important sources of exposure to indoor pollutants especially dust mite allergens. So, teaching about reducing exposure to them to staff and authorities of day care centers is recommended. Given the role of these factors in the development of many allergic and respiratory diseases, it is suggested that such a study be carried out in other parts of the country.

Acknowledgments

The authors acknowledge the Institute for Environmental Research (IER) of Tehran University of Medical Sciences for technically and financially supporting this research (grant number 93-03-46-27166). The authors also thank to the administrations of day-care centers for their cooperation.

Funding

This study was funded by Institute for Environmental Research (IER) of Tehran University of Medical Sciences (grant number 93–03–46-27166).

Compliance with ethical standards

Competing interests

There is no actual or potential conflict of interest among authors.

Footnotes

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Contributor Information

Mohammad Sadegh Hassanvand, Email: hassanvand@tums.ac.ir.

Masud Yunesian, Email: yunesian@tums.ac.ir.

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