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Article

Endotoxins in Household Dust in Northern China: Associations with Home Environment Factors and Childhood Asthma and Allergies

by
Yuxuan Zhao
1,
Yixin Liu
1,
Lianwang Cui
1,
Jing Hou
1,
Feng Gao
2,
Dan Norback
3 and
Yuexia Sun
1,*
1
Tianjin Key Laboratory of Indoor Air Environmental Quality Control, School of Environmental Science and Engineering, Tianjin University, Tianjin 300350, China
2
Tianjin Architecture Design Institute Co., Ltd., Tianjin 300350, China
3
Department of Medical Sciences, Uppsala University, 75105 Uppsala, Sweden
*
Author to whom correspondence should be addressed.
Atmosphere 2024, 15(7), 759; https://doi.org/10.3390/atmos15070759
Submission received: 25 May 2024 / Revised: 14 June 2024 / Accepted: 21 June 2024 / Published: 26 June 2024
(This article belongs to the Special Issue Toxicology and Health Effects of Air Pollution)

Abstract

:
The available information on endotoxin in Chinese households is limited and there is inconsistency regarding its impact on asthma and allergies in children. A case-control study was performed in 324 homes in Tianjin, China. Linear regression analysis was performed to identify the determinants of endotoxin concentrations in household dust. Logistic regression models were employed to investigate the associations of endotoxin concentrations with asthma and allergies in children. Endotoxin concentrations were determined from 284 valid dust samples, ranging from 94 to 11,625 EU/g, with a mean concentration of 3638 EU/g. We found a significant positive association between endotoxin concentrations and children’s current asthma. Old houses, ventilation systems without exhaust fans and windows opened infrequently were related to higher concentrations of endotoxins. In conclusion, endotoxin exposure in the home might be a risk factor for current asthma in children. Strategies for controlling endotoxin concentrations such as building maintenance and ventilation improvements are recommended.

1. Introduction

The prevalence of allergic diseases has increased worldwide over the past few decades. In the 1990s, the ECRHS (the European Community Respiratory Health Survey) surveyed the prevalence of asthma in 22 European countries and found that with the development of urbanization, the prevalence of asthma was increasing year by year [1]. In Chinese Taipei, Hsieh and Tsai [2] examined the prevalence of allergic diseases in school children aged 7 to 15 years and found that the prevalence of childhood asthma increased from 1.3% in 1974 to 5.1% in 1985 and 5.8% in 1991. In Guangzhou, China, a survey among school-aged children found that the prevalence of asthma has doubled over the past 15 years [3]. In the process of exploring the rising incidence of allergic diseases, indoor environmental exposure has received extensive attention. Endotoxins are ubiquitous in indoor environments and serve as important components of active ingredients in indoor dust. Endotoxins are the lipopolysaccharide components of the outer membrane of Gram-negative bacteria and have strong immunostimulatory and pro-inflammatory properties [4]. It is of great significance to explore endotoxin exposure and its health effects.
Endotoxin concentrations in household dust have been investigated in some studies and geographical variations have been observed. The International Study of Asthma and Allergy in Children (ISAAC II) reported a fivefold difference in the endotoxin concentration in house dust between Rome, Italy and Linkoping, Sweden [5]. A multi-center study conducted across 22 study centers from 10 European countries found that the median endotoxin concentration in mattress dust ranged from 772 EU/g in Reykjavik, Iceland, to 4806 EU/g in Turin, Italy [6]. In China, previous research on household endotoxins has primarily focused on southern regions such as Guangzhou and Hong Kong [7,8]. However, to our knowledge, endotoxin concentrations in household dust in northern China have not been reported previously.
Aiming to enhance the comprehension of endotoxins, numerous studies have been conducted to investigate the determinants of endotoxins in household dust. These studies have indicated various factors, including the dwelling type, dwelling location, occupant density, household cleaning frequency, use of air conditioners, environmental tobacco smoking and pet ownership [6,7,9,10,11,12,13,14,15,16]. It has been demonstrated by Giovannangelo et al. [12] that the determinants of endotoxins vary across countries. Our understanding in this area is limited in China, as only one study conducted in Hong Kong has reported the determinants of household endotoxins [7].
Exposure to endotoxins might induce an inflammatory response, leading to the development of allergy-related diseases [17]. However, previous observational studies that have examined the associations of endotoxin concentrations with asthma and allergic symptoms in children did not provide a consistent picture, with reports of a protective role of endotoxin exposure [10,18,19], a higher risk and severity of disease in those who were exposed at elevated levels [20,21,22] and no influence of exposure on disease [14,23].
Considering the limited information on endotoxins in Chinese households and inconsistent findings regarding its impact on asthma and allergies in children, the present study aims to describe the concentrations and determinants of endotoxins in household dust in northern China, as well as investigate their associations with asthma, rhinitis and eczema among children.

2. Methods

This study was part of the project “CCHH (China, Children, Health, Home)” in Tianjin region. Tianjin is located approximately 130 km away from Beijing and covers an area of 11,966.45 square kilometers with a resident population of 13.64 million [24]. The average outdoor air temperatures for spring, summer, autumn and winter are 13.4 °C, 25.7 °C, 13.6 °C and −1.7 °C in Tianjin [25]. The outdoor average relative humidities range from 52% in spring to 72% in summer [26]. The CCHH study consisted of two phases. The first phase (May 2013–December 2014) was a cross-sectional questionnaire survey, which collected information on children’s and family background, building characteristics, dampness problems, personnel activities as well as the health status of children. In the second phase (September 2013–January 2016), home inspections were conducted to collect dust samples and to measure indoor environmental parameters such as indoor temperature, relative humidity and ventilation. This paper focuses on 324 inspected homes in urban Tianjin.

2.1. Dust Collection and Endotoxin Analysis

Dust samples were collected from children’s bedroom floors using filter socks mounted on a mouthpiece connected to a household vacuum cleaner. A minimum of 100 mg dust was collected for each sample. The filter sock was then detached and wrapped in aluminum foil. The samples were transported to the laboratory and stored in a freezer at −20 °C until analysis.
For endotoxin analysis, dust was extracted in pyrogen-free water with 0.05% Tween for 40 min centrifuged and the supernatant was removed and assayed. Endotoxins were analyzed by Limulus Amebocyte Lysate (LAL) assay according to the manufacturer’s protocol (GenScript, Inc., Piscataway, NJ, USA). All endotoxin levels were within the limits of detection of the assay. The resulting endotoxin unit (EU) per mL values were converted into EU/g dust.

2.2. Building Characteristics, Environmental Parameters and Personnel Activities in Homes

Information on building characteristics, self-reported indoor environmental parameters and personnel activities were collected in the first phase through questionnaires. The questionnaire details have been previously published [27]. The measurement of indoor environmental parameters was conducted during home inspection. Portable CO2 monitors (AZ® 7798, Taiwan, China) were placed in the living room and bedrooms to continuously monitor indoor temperature, relative humidity and CO2 concentration for at least 24 h with sampling interval of one minute. We used CO2 produced by the occupants during sleep as a tracer gas to calculate ventilation rate at night. The detailed method has been described previously [28]. Absolute humidity (AH, g/m3) was calculated as a function of relative humidity (RH, %) and temperature (T, °C) using the following empirical equation [29]:
A H = 1322.7 exp ( 17.625 T / ( T + 243.04 ) ) ( R H / 100 ) T + 273.15

2.3. Asthma and Allergy of Investigated Children

Asthma and allergic symptoms among children were self-reported by parents through the questionnaire survey. These questions were identical to those used in the ISAAC study [30]. We used the diagnosis of disease and the related symptoms in the last 12 months to categorize current asthma, current rhinitis and current eczema, while children without any allergic symptoms were defined as controls, as shown below,
Current asthma: “child has been diagnosed with asthma by a doctor” and “child has had wheezing or whistling in the chest in the last 12 months”.
Current rhinitis: “child has been diagnosed with hay fever or allergic rhinitis by a doctor” and “child has had a problem with sneezing, or a runny, or a blocked nose in the last 12 months when he/she has not had a cold or the flu”.
Current eczema: “child has been diagnosed with eczema by a doctor” and “child has had eczema symptoms in the last 12 months”.
This study was approved by the research office at Tianjin University. Guardian of participants provided written informed consent to participate in this study.

2.4. Statistical Analysis

Endotoxin concentrations were normally distributed and expressed as mean and standard deviation (SD). The associations between endotoxin concentrations in household dust and determinants were investigated using linear regression analysis. The mutual effect of determinants that showed marginal significant associations (p < 0.1) with endotoxin concentrations were further explored in multivariate linear regression model. Locally weighted regression smoothing plots were used to exhibit the variation of proportion of asthma and allergies among investigated children with endotoxin concentrations. Logistic regression models were performed to estimate odds ratios (ORs) of endotoxin for health outcomes in children with adjustment for gender, age and family allergic history. Endotoxin concentration was treated as a dichotomized variable (below vs. above median). p-values less than 0.05 were accepted as significant. Statistical analysis was performed with SPSS 26.

3. Results

3.1. Endotoxin Concentrations in Household Dust

A total of 324 homes were inspected and sampled in urban Tianjin. Forty (40) samples had a deficient weight or were lost, so we finally obtained 284 effective dust samples. The endotoxin concentrations ranged from 94 to 11,625 EU/g, with a mean value of 3638 (SD = 2010) EU/g. The valid dust samples for determining endotoxin concentrations in spring, summer, autumn and winter were 62, 58, 68 and 96, respectively. The corresponding mean concentrations of endotoxins in the four seasons were 3849 (SD = 2097), 3182 (SD = 1918), 3538 (SD = 2221) and 3850 (SD = 1822) EU/g, respectively. No significant seasonal differences in the endotoxin concentrations were found by the analysis of variance.

3.2. Building Characteristics, Indoor Environmental Parameters and Personnel Activities in Inspected Homes

The building characteristics, indoor environmental parameters and personnel activities in the inspected homes are summarized in Table 1, Table 2 and Table 3.

3.3. Determinants of Endotoxin Concentrations in Chinese Homes

The associations between the building characteristics and endotoxin concentrations are shown in Table 4. The age of the house showed a positive trend with endotoxin exposure, with significantly higher concentrations observed in houses aged over 20 years than those less than 10 years. The endotoxin concentrations were significantly lower in homes with exhaust fans compared to those without exhaust fans.
Table 5 shows the associations of endotoxin concentrations with both measured and self-reported environmental parameters. The absolute humidity was found to have a significantly negative association with endotoxin concentrations (p = 0.02).
The associations between the personnel activities and endotoxin concentrations are shown in Table 6. Frequent room-cleaning was associated with a higher concentration of endotoxin. Significantly higher endotoxin concentrations were found in homes with infrequent window opening for ventilation (p = 0.03). The utilization of buckwheat pillows exhibited a positive trend with the endotoxin concentration where it was of borderline significance (p = 0.067).
The mutual effect of the variables that showed marginal significant associations (p < 0.1) with endotoxin concentrations was further explored, including the age of the house, the mode of ventilation, the temperature, absolute humidity, suspected dampness problems, frequency of cleaning the child’s room, frequency of window opening for ventilation, and usage of buckwheat pillows. These variables accounted for 7.8% of the observed variability in the endotoxin concentrations in household dust. The mutual effect model revealed that the age of the house and frequency of cleaning exhibited significant associations with the endotoxin concentrations in household dust (Table 7).

3.4. Associations between Endotoxin Concentrations and Children’s Asthma and Allergies

A total of 332 children were investigated in 324 inspected homes in Tianjin. Among them, 16 children exhibited current asthma, 58 had current rhinitis and 89 had current eczema. Eight (8) children had both current asthma and current rhinitis, 21 had both current rhinitis and current eczema, 4 had both current asthma and current eczema and 2 had all three conditions. There were 36 children who did not exhibit any allergic symptoms who were considered as controls. The demographic information of these children is shown in Table 8.
Figure 1 shows the smoothed mean proportion of asthma and allergies with variations of the endotoxin concentration in household dust. A clear positive trend was observed between the endotoxin concentrations and the proportion of childhood asthma and rhinitis.
The odds ratios of endotoxin exposure for asthma and allergies in children are shown in Table 9. We found a significant positive association between the endotoxin concentrations in household dust and children’s current asthma (AOR: 9.68, 95% CI: 1.01–92.45). The same patterns have been observed for the endotoxin concentrations with current rhinitis and current eczema in children, although these associations did not reach statistical significance.

4. Discussion

In this study, we found a positive association between endotoxin concentrations and children’s current asthma. Endotoxin concentrations in bedroom floor dust were associated with the age of the house, cleaning frequency and ventilation system.
In 324 inspected homes in urban Tianjin, we observed a wide range of endotoxin concentrations in dust samples collected from children’s bedrooms, ranging from 94 to 11,625 EU/g, with a mean concentration of 3638 EU/g. Comparing the endotoxin concentrations between our study and other Chinese studies was challenging due to limited household studies in China and variations in the units used for measuring endotoxin, with EU/m2 [8] and ng/mg dust [31] being employed while we utilized EU/g. Given the strong pro-inflammatory and immunostimulatory properties of endotoxins, further investigations employing a standardized approach are warranted to characterize endotoxins in Chinese households. The endotoxin concentrations in bedroom floor dust in our study were lower than those reported by previous studies conducted in other countries, with geometric means of 7300 EU/g in Germany [32], 35,300 EU/g in the USA [33], 9244 EU/g in New Zealand [20], 5700 EU/g in Sweden [14] and 31,100 EU/g in Denmark [13].
In this study, we found a clear positive trend between endotoxin concentrations and the proportion of current asthma in children. Additionally, we observed a significant association between high endotoxin concentrations and an increased risk of current asthma in children (AOR: 9.68, 95% CI: 1.01–92.45). Our results indicate that endotoxins in household dust may be a risk factor for current asthma in children, which is consistent with some of the previous studies [20,21,22]. One potential mechanism is that alveolar macrophages in the airways produce a wide variety of cytokines and express functional CD14 and Toll-like receptors, which recognize endotoxins and can induce inflammatory responses [34].
The determinants of endotoxin concentrations in household dust were explored to identify effective control measures. Both one-determinant regression and mutual effect models revealed a positive association between the age of the house and the endotoxin concentration, consistent with Gehring et al.’s [10] findings of higher endotoxin levels in “old” houses. One possible explanation is that endotoxins accumulate over time [10]. Another possibility could be that older houses serve as an indicator of poor housing quality, as we have previously reported a significant association between older houses and dampness indicators [35]. Dampness indicators were positively related to endotoxin exposure (See Table 5, self-reported dampness). Additionally, exhaust fans were less frequently installed in older houses (>20 years: 77.3% vs. <10 years: 47.4%). Significantly lower endotoxin concentrations were observed in those houses equipped with exhaust fans in the present study. Therefore, older houses require maintenance to control endotoxins, such as reducing dampness problems and installing exhaust fans to improve ventilation.
We found that homes equipped with exhaust fans and frequently opened windows had significantly lower concentration of endotoxins. The same patterns were also observed in the mutual effect analysis. A study conducted in Nanjing, China, found that both airborne endotoxins and endotoxins in dust were lower in the outdoor environment than those in the home environment [31]. An outdoor to indoor airflow might dilute the endotoxins in the home environment. This influence of ventilation on the indoor endotoxin concentration was also observed by Bischof et al. [9], who reported a significant negative association between ventilation and endotoxin concentrations in living room floor dust. Therefore, ventilation may serve as an effective strategy for controlling endotoxins indoors.
We observed a significant increase in endotoxin levels in bedrooms with frequent cleaning. The association between endotoxin concentrations and cleaning frequency were contradictory in previous studies. Bischof et al. [9] observed an association between elevated endotoxin concentrations and infrequent vacuum cleaning, whereas Moniruzzaman et al. [14] identified an association between frequent vacuum cleaning and higher endotoxin concentrations. These two studies primarily focused on the frequency of vacuum cleaning, while wet mopping emerged as the most predominant cleaning method employed in children’s bedroom (86%) in our study. Smedje and Norback [36] reported that the wet mopping of floors increased the airborne concentrations of viable bacteria. We speculate that frequent wet mopping facilitates bacteria growth and increases endotoxin concentrations in dust. The influence of cleaning frequency and endotoxins, considering the cleaning method, requires further investigation.
We noticed a significant inverse association between the absolute humidity and endotoxin levels. In the mutual effect model, although not statistically significant, there was still a negative trend between the absolute humidity and endotoxins. A previous study reported a significant association between a low relative humidity and high endotoxin concentrations [16]. The authors argued that measuring the relative humidity on a single day may be a poor measure of the usual indoor conditions, leading to potential misclassification. Some studies have not found an association between the air’s relative humidity and the endotoxin concentration [9,14,37]. However, a study conducted in New Zealand revealed a significant positive association between the carpet-based relative humidity and endotoxin concentrations in living room floor dust [38]. The association between endotoxins and air relative humidity as well as surface relative humidity requires further investigation through extended-duration measurements.

5. Strengths and Limitations

To our knowledge, this is the first study to report endotoxin concentrations in household dust in northern China. A comprehensive investigation was conducted to identify the determinants of endotoxin concentrations in household dust, encompassing building characteristics, environmental parameters and personnel activities. This helps to develop strategies for controlling indoor endotoxin levels.
This study was limited to the Tianjin region and further research across multiple locations within China is warranted.

6. Conclusions

Our results suggest that endotoxin in household dust may be a risk factor for current asthma in children. Strategies for controlling endotoxin concentrations such as building maintenance and ventilation improvement are recommended. The current state of knowledge on endotoxins in China necessitates further research to enhance our comprehension.

Author Contributions

Conceptualization, Y.S.; methodology, Y.Z., L.C., J.H. and Y.S.; software, Y.Z.; formal analysis, Y.Z. and Y.L.; investigation, L.C., J.H. and F.G.; data curation, L.C. and J.H.; writing—original draft preparation, Y.Z. and Y.L.; writing—review and editing, Y.S. and D.N.; visualization, Y.Z.; supervision, Y.S.; project administration, Y.S.; funding acquisition, Y.S. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Natural Science Foundation of China (grant number 21207097), the Natural Science Foundation of Tianjin City (grant number 21JCZDJC00540), the Tianjin Municipal Bureau of Science and Technology (grant number 19YFZCSN01120) and the Tianjin University Graduate Education Fund 2021 (grant number C1-2021-009).

Institutional Review Board Statement

The study was conducted in accordance with the Declaration of Helsinki, and approved by the Research Office at Tianjin University.

Informed Consent Statement

Informed consent was obtained from all subjects involved in the study.

Data Availability Statement

The data presented in this study are available on request from the corresponding author. The data are not publicly available due to privacy.

Acknowledgments

The authors thank the participating families and staff of the CCHH study.

Conflicts of Interest

Author Feng Gao was employed by the company Tianjin Architecture Design Institute Co., Ltd. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

References

  1. Burney, P.G.; Luczynska, C.; Chinn, S.; Jarvis, D. The European community respiratory health survey. Eur. Respir. J. 1994, 5, 954–960. [Google Scholar] [CrossRef]
  2. Hsieh, K.H.; Shen, J.J. Prevalence of childhood asthma in Taipei, Taiwan, and other Asian Pacific countries. J. Asthma Off. J. Assoc. Care Asthma 1988, 2, 73–82. [Google Scholar] [CrossRef] [PubMed]
  3. Li, J.; Wang, H.; Chen, Y.; Zheng, J.; Wong, G.W.K.; Zhong, N. House dust mite sensitization is the main risk factor for the increase in prevalence of wheeze in 13-to 14-year-old schoolchildren in Guangzhou city, China. Clin. Exp. Allergy 2013, 10, 1171–1179. [Google Scholar] [CrossRef] [PubMed]
  4. Douwes, J.; Pearce, N.; Heederik, D. Does environmental endotoxin exposure prevent asthma? Thorax 2002, 1, 86–90. [Google Scholar] [CrossRef]
  5. Gehring, U.; Strikwold, M.; Schram-Bijkerk, D.; Weinmayr, G.; Genuneit, J.; Nagel, G.; Wickens, K.; Siebers, R.; Crane, J.; Doekes, G.; et al. Asthma and allergic symptoms in relation to house dust endotoxin: Phase two of the international study on asthma and allergies in childhood (ISAAC II). Clin. Exp. Allergy 2008, 12, 1911–1920. [Google Scholar] [CrossRef]
  6. Chen, C.M.; Thiering, E.; Doekes, G.; Zock, J.P.; Bakolis, I.; Norbäck, D.; Sunyer, J.; Villani, S.; Verlato, G.; Täubel, M.; et al. Geographical variation and the determinants of domestic endotoxin levels in mattress dust in Europe. Indoor Air 2012, 1, 24–32. [Google Scholar] [CrossRef]
  7. Leung, T.F.; Wong, Y.S.; Chan, I.H.S.; Yung, E.; Wong, C.K.; Lam, C.W.K.; Wong, G.W.K. Indoor determinants of endotoxin and dust mite exposures in Hong Kong homes with asthmatic children. Int. Arch. Allergy Immunol. 2010, 3, 279–287. [Google Scholar] [CrossRef]
  8. Li, J.; Yang, Z.W.; Feng, M.L.; Roponen, M.; Schaub, B.; Wong, G.W.K. Associations of early life exposures and environmental factors with asthma among children in rural and urban areas of Guangdong, China. J. Allergy Clin. Immunol. 2016, 2, AB389. [Google Scholar] [CrossRef]
  9. Bischof, W.; Koch, A.; Gehring, U.; Fahlbusch, B.; Wichmann, H.E.; Heinrich, J.; Grp, I.S. Predictors of high endotoxin concentrations in the settled dust of German homes. Indoor Air 2002, 1, 2–9. [Google Scholar] [CrossRef]
  10. Gehring, U.; Bischof, W.; Borte, M.; Herbarth, O.; Wichmann, H.E.; Heinrich, J.; Grp, L.S. Levels and predictors of endotoxin in mattress dust samples from East and West German homes. Indoor Air 2004, 4, 284–292. [Google Scholar] [CrossRef]
  11. Gereda, J.E.; Klinnert, M.D.; Price, M.R.; Leung, D.Y.M.; Liu, A.H. Metropolitan home living conditions associated with indoor endotoxin levels. J. Allergy Clin. Immunol. 2001, 5, 790–796. [Google Scholar] [CrossRef] [PubMed]
  12. Giovannangelo, M.; Gehring, U.; Nordling, E.; Oldenwening, M.; Terpstra, G.; Bellander, T.; Hoek, G.; Heinrich, J.; Brunekreef, B. Determinants of house dust endotoxin in three European countries—The AIRALLERG study. Indoor Air 2007, 1, 70–79. [Google Scholar] [CrossRef] [PubMed]
  13. Holst, G.; Host, A.; Doekes, G.; Meyer, H.W.; Madsen, A.M.; Sigsgaard, T. Determinants of house dust, endotoxin, and β-(13)-d-glucan in homes of Danish children. Indoor Air 2015, 3, 245–259. [Google Scholar] [CrossRef] [PubMed]
  14. Moniruzzaman, S.; Engman, L.H.; James, P.; Sigsgaard, T.; Thorne, P.S.; Sundell, J.; Bornehag, C.G. Levels of endotoxin in 390 Swedish homes: Determinants and the risk for respiratory symptoms in children. Int. J. Environ. Health Res. 2012, 1, 22–36. [Google Scholar] [CrossRef] [PubMed]
  15. Ownby, D.R.; Peterson, E.L.; Wegienka, G.; Woodcroft, K.J.; Nicholas, C.; Zoratti, E.; Johnson, C.C. Are cats and dogs the major source of endotoxin in homes? Indoor Air 2013, 3, 219–226. [Google Scholar] [CrossRef] [PubMed]
  16. Thorne, P.S.; Cohn, R.D.; Mav, D.; Arbes, S.J.; Zeldin, D.C. Predictors of endotoxin levels in US housing. Environ. Health Perspect. 2009, 5, 763–771. [Google Scholar] [CrossRef] [PubMed]
  17. Min, K.B.; Min, J.Y. Exposure to household endotoxin and total and allergen-specific IGE in the US population. Environ. Pollut. 2015, 199, 148–154. [Google Scholar] [CrossRef] [PubMed]
  18. Irahara, M.; Yamamoto-Hanada, K.; Sato, M.; Saito-Abe, M.; Miyaji, Y.; Yang, L.M.; Nishizato, M.; Kumasaka, N.; Mezawa, H.; Ohya, Y. Endotoxin concentration and persistent eczema in early childhood. J. Dermatol. 2023, 5, 646–655. [Google Scholar] [CrossRef]
  19. Phipatanakul, W.; Celedón, J.C.; Raby, B.A.; Litonjua, A.A.; Milton, D.K.; Sredl, D.; Weiss, S.T.; Gold, D.R. Endotoxin exposure and eczema in the first year of life. Pediatrics 2004, 1, 13–18. [Google Scholar] [CrossRef]
  20. Gillespie, J.; Wickens, K.; Siebers, R.; Howden-Chapman, P.; Town, I.; Epton, M.; Fitzharris, P.; Fishwick, D.; Crane, J.; New Zealand Asthma Allergy, B. Endotoxin exposure, wheezing, and rash in infancy in a New Zealand birth cohort. J. Allergy Clin. Immunol. 2006, 6, 1265–1270. [Google Scholar] [CrossRef]
  21. Park, J.H.; Gold, D.R.; Spiegelman, D.L.; Burge, H.A.; Milton, D.K. House dust endotoxin and wheeze in the first year of life. Am. J. Respir. Crit. Care Med. 2001, 2, 322–328. [Google Scholar] [CrossRef] [PubMed]
  22. Yen, Y.C.; Yang, C.Y.; Wang, T.N.; Yen, P.C.; Ho, C.K.; Mena, K.D.; Lee, T.C.; Chen, K.S.; Lin, Y.C.; Chen, P.S. Household airborne endotoxin associated with asthma and allergy in elementary school-age children: A case-control study in Kaohsiung, Taiwan. Environ. Sci. Pollut. Res. 2020, 16, 19502–19509. [Google Scholar] [CrossRef] [PubMed]
  23. Chen, C.M.; Sausenthaler, S.; Bischof, W.; Herbarth, O.; Borte, M.; Behrendt, H.; Krämer, U.; Williams, H.C.; Wichmann, H.E.; Heinrich, J.; et al. Perinatal exposure to endotoxin and the development of eczema during the first 6 years of life. Clin. Exp. Dermatol. 2010, 3, 238–424. [Google Scholar] [CrossRef] [PubMed]
  24. Tianjin Bureau of Statistics, Statistical Bulletin of Tianjin National Economic and Social Development in 2023. 2024. Available online: https://stats.tj.gov.cn/tjsj_52032/tjgb/202403/t20240318_6563697.html (accessed on 2 May 2024).
  25. Meteorological Data Center of China Meteorological Administration, Statistics of Monthly Average Temperature. 2017. Available online: http://data.cma.cn/data/weatherBk.html (accessed on 2 May 2024).
  26. Meteorological Data Center of China Meteorological Administration, Statistics of Monthly Average Relative Humidity. 2017. Available online: http://data.cma.cn/data/weatherBk.html (accessed on 2 May 2024).
  27. Sun, Y.X.; Hou, J.; Sheng, Y.; Kong, X.R.; Weschler, L.B.; Sundell, J. Modern life makes children allergic. A cross-sectional study: Associations of home environment and lifestyles with asthma and allergy among children in Tianjin region, China. Int. Arch. Occup. Environ. Health 2019, 4, 587–598. [Google Scholar] [CrossRef] [PubMed]
  28. Hou, J.; Zhang, Y.F.; Sun, Y.X.; Wang, P.; Zhang, Q.N.; Kong, X.R.; Sundell, J. Air change rates at night in northeast Chinese homes. Build. Environ. 2018, 132, 273–281. [Google Scholar] [CrossRef]
  29. Marr, L.C.; Tang, J.W.; Van Mullekom, J.; Lakdawala, S.S. Mechanistic insights into the effect of humidity on airborne influenza virus survival, transmission and incidence. J. R. Soc. Interface 2019, 150, 20180298. [Google Scholar] [CrossRef] [PubMed]
  30. Asher, M.I.; Keil, U.; Anderson, H.R.; Beasley, R.; Crane, J.; Martinez, F.; Mitchell, E.A.; Pearce, N.; Sibbald, B.; Stewart, A.W. International study of asthma and allergies in childhood (ISAAC): Rationale and methods. Eur. Respir. J. 1995, 8, 483–491. [Google Scholar] [CrossRef] [PubMed]
  31. Yao, M.S.; Wu, Y.; Zhen, S.Q.; Mainelis, G. A comparison of airborne and dust-borne allergens and toxins collected from home, office and outdoor environments both in New Haven, United States and Nanjing, China. Aerobiologia 2009, 3, 183–192. [Google Scholar] [CrossRef]
  32. Douwes, J.; Doekes, G.; Heinrich, J.; Koch, A.; Bischof, W.; Brunekreef, B. Endotoxin and β(13)-glucan in house dust and the relation with home characteristics: A pilot study in 25 German houses. Indoor Air 1998, 4, 255–263. [Google Scholar] [CrossRef]
  33. Thorne, P.S.; Kulhánkova, K.; Yin, M.; Cohn, R.; Arbes, S.J.; Zeldin, D.C. Endotoxin exposure is a risk factor for asthma: The national survey of endotoxin in United States housing. Am. J. Respir. Crit. Care Med. 2005, 11, 1371–1377. [Google Scholar] [CrossRef]
  34. Radon, K. The two sides of the “endotoxin coin”. Occup. Environ. Med. 2006, 1, 73–78. [Google Scholar] [CrossRef]
  35. Kong, X.R.; Sun, Y.X.; Weschler, L.B.; Sundell, J. Dampness problems in Tianjin dwellings: A cross-sectional study of associations with building characteristics and lifestyles. Indoor Built Environ. 2019, 1, 132–144. [Google Scholar] [CrossRef]
  36. Smedje, G.; Norbäck, D. Irritants and allergens at school in relation to furnishings and cleaning. Indoor Air-Int. J. Indoor Air Qual. Clim. 2001, 2, 127–133. [Google Scholar] [CrossRef] [PubMed]
  37. Frankel, M.; Bekö, G.; Timm, M.; Gustavsen, S.; Hansen, E.W.; Madsen, A.M. Seasonal variations of indoor microbial exposures and their relation to temperature, relative humidity, and air exchange rate. Appl. Environ. Microbiol. 2012, 23, 8289–8297. [Google Scholar] [CrossRef] [PubMed]
  38. Wickens, K.; Douwes, J.; Siebers, R.; Fitzharris, P.; Wouters, I.; Doekes, G.; Mason, K.; Hearfield, M.; Cunningham, M.; Crane, J. Determinants of endotoxin levels in carpets in New Zealand homes. Indoor Air 2003, 2, 128–135. [Google Scholar] [CrossRef]
Figure 1. Smoothed plots of the proportion of asthma and allergies in relation to endotoxins in household dust. The blue lines show the smoothed mean proportion of asthma and allergies while dark regions indicate 95% confidence intervals. Children with both physician-diagnosed and related symptoms in the last 12 months were defined as current asthma, current rhinitis and current eczema.
Figure 1. Smoothed plots of the proportion of asthma and allergies in relation to endotoxins in household dust. The blue lines show the smoothed mean proportion of asthma and allergies while dark regions indicate 95% confidence intervals. Children with both physician-diagnosed and related symptoms in the last 12 months were defined as current asthma, current rhinitis and current eczema.
Atmosphere 15 00759 g001
Table 1. Building characteristics of 324 urban homes inspected in Tianjin.
Table 1. Building characteristics of 324 urban homes inspected in Tianjin.
n%
House size (m2)
≤608426.3
60–10014846.4
>1008727.3
House age (year)
<109228.8
10–2013843.3
≥208927.9
Outer walls insulation
No11047.4
Yes12252.6
Single-, double- or triple-glazed windows
Single-pane11939.5
Double- or triple-pane18260.5
Ventilation mode
Natural ventilation without exhaust fans9132.3
Natural ventilation with exhaust fans19167.7
Heating system in winter
Radiator27386.9
Underground heating4113.1
Cooling system in summer
Air conditioning25078.9
Opening windows or electric fans6721.1
Table 2. Environmental parameters of 324 urban homes inspected in Tianjin.
Table 2. Environmental parameters of 324 urban homes inspected in Tianjin.
Measured Parameters
Ventilation rate (L/s/person)3.29 (1.47–7.15) a
Temperature (°C)22.92 (3.90) b
Relative humidity (%)44.56 (12.77) b
Absolute humidity (g/m3)10.20 (4.28) b
Self-reported parametersn%
Visible mildew, mould or damp stains in child’s room 175.5
Suspected dampness6823.7
Flooring that is peeling or discolored in child’s room196.2
Condensation on the windowpane in child’s room11039.3
Dampness8126.8
a Ventilation rates were reported as the median with the 25th and 75th percentiles for the non-normal distribution. b Temperature, relative humidity and absolute humidity were described as mean and standard deviation owing to the approximately normal distribution.
Table 3. Personnel activities of 324 urban homes inspected in Tianjin.
Table 3. Personnel activities of 324 urban homes inspected in Tianjin.
n%
Number of people living in the home
≤424882.7
>45217.3
Pet keeping
No26785.9
Yes4414.1
Frequency of cleaning child’s room
Less than everyday15148.1
Everyday16351.9
Frequency of window opening for ventilation
Less than everyday165.1
Everyday29994.9
Frequency of sun-cure bedding
Not often23276.3
Often7223.7
Usage of humidifier
No10936.0
Yes19464.0
Usage of air cleaner
No21471.3
Yes8628.7
Usage of insecticide
No17357.3
Yes12942.7
Environmental tobacco exposure
No18157.1
Yes13642.9
Usage of buckwheat pillows
No5218.6
Yes22781.4
Table 4. Associations a between building characteristics and endotoxin concentrations, n = 284.
Table 4. Associations a between building characteristics and endotoxin concentrations, n = 284.
Regression Coefficient with 95% Confidence Intervalsp
House size (m2)
60–100 vs. ≤60 (ref.)−248.80 (−817.77, 320.16)0.39
>100 vs. ≤60 (ref.)−523.74 (−1166.43, 118.95)0.11
Age of house (year)
10–20 vs. <10 (ref.)414.54 (−143.68, 972.76)0.15
≥20 vs. <10 (ref.)717.15 (98.43, 1335.88) d0.02 d
Outer walls insulation
Yes vs. No (ref.)−399.45 (−941.65, 142.74)0.15
Glazing window in child’s room
Double- or triple-pane vs. Single-pane (ref.)−199.35 (−675.95, 277.25)0.41
Ventilation mode
Natural ventilation with exhaust fans vs. Natural ventilation without exhaust fans (ref.)−553.28 (−1079.35, −27.22) d0.04 d
Heating system in winter b
Underground heating vs. Radiator (ref.)−439.55 (−1787.48, 908.38)0.52
Cooling system in summer c
Air conditioning vs. Opening windows or fans (ref.)−89.93 (−1299.15, 1119.28)0.88
a With adjustment for measurement seasons. b Restricted to winter season. c Restricted to summer season. d p-values less than 0.05 are indicated in bold for significance.
Table 5. Associations a between environmental parameters and endotoxin concentrations, n = 284.
Table 5. Associations a between environmental parameters and endotoxin concentrations, n = 284.
Regression Coefficient with 95% Confidence Intervalsp
Measured parameters
Ventilation rate−5.03 (−23.78, 13.72)0.60
Temperature−57.01 (−122.40, 8.40)0.09
Relative humidity−16.85 (−37.30, 3.59)0.11
Absolute humidity−76.37 (−138.42, −14.33) b0.02 b
Self-reported parameters
Visible mildew, mould or damp stains: yes vs. no (ref.)52.46 (−154.89, 259.81)0.62
Suspected dampness problems: yes vs. no (ref.)479.60 (−99.37, 1058.57)0.10
Flooring that is peeling or discolored in child’s room: yes vs. no (ref.)243.25 (−737.54, 1224.05)0.63
Condensation on the windowpane in child’s room: yes vs. no (ref.)−3.79 (−519.93, 512.36)0.99
a With adjustment for measurement seasons. b p-values less than 0.05 are indicated in bold for significance.
Table 6. Associations a between personnel activities and endotoxin concentrations, n = 284.
Table 6. Associations a between personnel activities and endotoxin concentrations, n = 284.
Regression Coefficient with 95% Confidence Intervalsp
Number of people living in the home: >4 vs. ≤4 (ref.)−190.77 (−849.31, 467.77)0.60
Pet keeping: yes vs. no (ref.)58.14 (−628.90, 745.17)0.87
Frequency of cleaning child’s room: everyday vs. less than everyday (ref.)481.17 (9.24, 953.10) b0.05 b
Frequency of window opening for ventilation: everyday vs. less than everyday (ref.)−1241.04 (−2389.83, −92.25) b0.03 b
Frequency of sun-cure bedding: often vs. not often (ref.)244.68 (−306.74, 796.10)0.38
Usage of humidifier: yes vs. no (ref.)−263.12 (−770.39, 244.16)0.31
Usage of air cleaner: yes vs. no (ref.)−354.95 (−884.17, 174.27)0.19
Usage of insecticide: yes vs. no (ref.)−63.11 (−554.86, 428.64)0.80
Environmental tobacco exposure: yes vs. no (ref.)−13.08 (−488.90, 462.74)0.96
Usage of buckwheat pillows: yes vs. no (ref.)622.75 (−43.67, 1289.16)0.07
a With adjustment for measurement seasons. b p-values less than 0.05 are indicated in bold for significance.
Table 7. Mutual effect a model on associations of endotoxin concentrations with building characteristics, indoor environmental parameters and personnel activities, n = 284.
Table 7. Mutual effect a model on associations of endotoxin concentrations with building characteristics, indoor environmental parameters and personnel activities, n = 284.
Regression Coefficient with 95% Confidence Intervalsp
Age of house b (years): <10 (ref.), 10–20, ≥20477.37 (72.72, 882.03) c0.02 c
Ventilation mode: natural ventilation with exhaust fans vs. without exhaust fans (ref.)−426.18 (−1077.31, 224.94)0.20
Temperature−12.82 (−129.49, 103.85)0.83
Absolute humidity−74.16 (−180.85, 32.53)0.17
Suspected dampness problems: yes vs. no (ref.)84.09 (−578.09, 746.27)0.80
Frequency of cleaning child’s room: everyday vs. less than everyday (ref.)828.49 (244.46, 1412.52) c0.01 c
Frequency of window opening for ventilation: everyday vs. less than everyday (ref.)−1000.98 (−2374.72, 372.77)0.15
Usage of buckwheat pillows: yes vs. no (ref.)406.87 (−324.18, 1137.92)0.27
a With adjustment for measurement seasons. b Treated as an ordinal variable. c p-values less than 0.05 are indicated in bold for significance.
Table 8. Demographic information of 332 investigated children in Tianjin, China, n (%).
Table 8. Demographic information of 332 investigated children in Tianjin, China, n (%).
Total, n = 332Current Asthma a, n = 16Current rhinitis a, n = 58Current Eczema a, n = 89Controls a, n = 36
GenderMale156 (47.7)10 (62.5)23 (40.4)45 (51.1)17 (47.2)
Female171 (52.3)6 (37.5)34 (59.6)43 (48.9)19 (52.8)
Age0–2 years old47 (14.6)1 (6.3)5 (8.9)23 (26.4)3 (8.6)
3–6 years old210 (65.0)14 (87.5)45 (80.4)49 (56.3)20 (57.1)
7–8 years old66 (20.4)1 (6.3)6 (10.7)15 (17.2)12 (34.3)
Family allergic historyYes109 (34.0)9 (60.0)33 (58.9)40 (45.5)8 (22.9)
No212 (66.0)6 (40.0)23 (41.1)48 (54.5)27 (77.1)
a Children with both physician-diagnosed and related symptoms in the last 12 months were defined as current asthma, current rhinitis and current eczema, while children without any allergic symptoms were defined as controls.
Table 9. Crude and adjusted odds ratios (ORs) with 95% confidence intervals (CIs) for the associations of endotoxin concentrations with children’s asthma and allergies.
Table 9. Crude and adjusted odds ratios (ORs) with 95% confidence intervals (CIs) for the associations of endotoxin concentrations with children’s asthma and allergies.
ORs a (95% CIs)AORs b (95% CIs)
Current asthma vs. controls3.12 (0.79, 12.35)9.68 (1.01, 92.45) c
Current rhinitis vs. controls1.63 (0.66, 4.02)2.41 (0.74, 7.88)
Current eczema vs. controls1.31 (0.57, 2.99)1.96 (0.75, 5.10)
a ORs were calculated using endotoxin concentrations below the median as a reference. b AORs: adjusted odds ratio, with adjustment for child’s age, gender and family allergic history. c p-values less than 0.05 are indicated in bold for significance.
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Zhao, Y.; Liu, Y.; Cui, L.; Hou, J.; Gao, F.; Norback, D.; Sun, Y. Endotoxins in Household Dust in Northern China: Associations with Home Environment Factors and Childhood Asthma and Allergies. Atmosphere 2024, 15, 759. https://doi.org/10.3390/atmos15070759

AMA Style

Zhao Y, Liu Y, Cui L, Hou J, Gao F, Norback D, Sun Y. Endotoxins in Household Dust in Northern China: Associations with Home Environment Factors and Childhood Asthma and Allergies. Atmosphere. 2024; 15(7):759. https://doi.org/10.3390/atmos15070759

Chicago/Turabian Style

Zhao, Yuxuan, Yixin Liu, Lianwang Cui, Jing Hou, Feng Gao, Dan Norback, and Yuexia Sun. 2024. "Endotoxins in Household Dust in Northern China: Associations with Home Environment Factors and Childhood Asthma and Allergies" Atmosphere 15, no. 7: 759. https://doi.org/10.3390/atmos15070759

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