Next Article in Journal
Nutshells as Efficient Biosorbents to Remove Cadmium, Lead, and Mercury from Contaminated Solutions
Next Article in Special Issue
Pulmonary Function Testing in Work-Related Asthma: An Overview from Spirometry to Specific Inhalation Challenge
Previous Article in Journal
Diet and Health Benefits Associated with In-Home Eating and Sharing Meals at Home: A Systematic Review
Previous Article in Special Issue
The Impact of Tobacco Smoking on Adult Asthma Outcomes
 
 
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Pulmonary Health Effects of Indoor Volatile Organic Compounds—A Meta-Analysis

1
Department of Public Health Sciences, University of Miami, Miami, FL 33136, USA
2
Department of Public Health Sciences, Division of Environmental Health, Miller School of Medicine, University of Miami, Miami, FL 33136, USA
*
Author to whom correspondence should be addressed.
Int. J. Environ. Res. Public Health 2021, 18(4), 1578; https://doi.org/10.3390/ijerph18041578
Submission received: 4 January 2021 / Revised: 1 February 2021 / Accepted: 2 February 2021 / Published: 7 February 2021
(This article belongs to the Special Issue Occupational and Environmental Asthma)

Abstract

:
Volatile organic compounds (VOCs) are commonly found in consumer products, including furniture, sealants and paints. Thus, indoor VOCs have become a public health concern, especially in high-income countries (HICs), where people spend most of their time indoors, and indoor and outdoor air exchange is minimal due to a lack of ventilation. VOCs produce high levels of reaction with the airway epithelium and mucosa membrane and is linked with pulmonary diseases. This paper takes a stock of the literature to assess the strength of association (measured by effect size) between VOCs and pulmonary diseases with the focus on asthma and its related symptoms by conducting a meta-analysis. The literature was searched using the PubMed database. A total of 49 studies that measured VOCs or VOC types and pulmonary health outcomes were included in the analysis. The results of these studies were tabulated, and standard effect size of each study was computed. Most studies were conducted in high-income countries, including France (n = 7), Japan (n = 7) and the United States (n = 6). Our analysis suggests that VOCs have a medium-sized effect on pulmonary diseases, including the onset of asthma (effect size (or Cohen’s d) ~0.37; 95% confidence interval (CI) = 0.25–0.49; n = 23) and wheezing (effective size ~0.26; 95% CI = 0.10–0.42; n = 10). The effect size also varied by country, age and disease type. Multiple stakeholders must be engaged in strategies to mitigate and manage VOC exposure and its associated pulmonary disease burden.

1. Introduction

Chronic pulmonary diseases, including the onset and persistence of asthma and chronic obstructive pulmonary diseases (COPD), and their associated morbidity and healthcare costs are on the rise. Moreover, these diseases are associated with reduced productivity and mortality worldwide [1]. In 2019 alone, 339 million new cases of asthma were reported worldwide, of which 417,918 resulted in death [1]. Common symptoms associated with asthma are coughing (with or without phlegm), bronchial inflammation and shortness of breath, and the symptom severity varies from person to person [2]. There are multiple social and economic consequences of asthma morbidity, such as adverse effects on educational performance by preventing school attendance and negative economic productivity due to loss of work [3]. Studies show that asthmatic children miss anywhere between 2.1 and 14.8 days of school depending on the severity of symptoms and socioeconomic status. This is because affluent asthmatic children are less likely to miss school than their less affluent counterparts [3]. There are other costs associated with asthma, including healthcare costs. There was an average cost of USD 1502 (95% CI: USD 1493–1511) for an asthma-related emergency room (ER) visit in 2008, and the total national expenditure on asthma-related ER visits was USD 1.59 billion in 2009 [4].
The extant literature suggests that both genetic and environmental factors play roles in the onset, progression, persistence and severity of asthma [5]. Several studies show that indoor air pollution (IAP), including particulate matter of varying sizes, volatile organic compounds (VOCs), smoke, and allergens (mold spores and endotoxins), are associated with the persistence and severity of asthma morbidity [1,2,5]. Low-income countries (LICs) have different risk factors than high-income countries (HICs), as sources and types of IAP vary across these countries [6]. For the purposes of this study, HICs are defined as countries within the highest twenty nominal GDPs, and LICs are defined as countries within the lowest twenty nominal GDPs [7]. The distinction between HICs and LICs is imperative, as HICs spend more on household furnishings [8,9]. These furnishings can include, but are not limited to, paints, glues, resins and floor polishes. All of these activities and products emit harmful VOCs [10]. HIC households are also typically sealed and rely on central air conditioning (AC), which circulates the same air indoors [11]. Thus, the concentration of indoor pollutants can build up in the absence of effective ventilation and/or filtration if new sources of VOCs are introduced, such as the addition or installation of new furniture, painting, carpeting etc. [11] A study shows that people in HICs spend only 2% of their time outdoors, which can result in their chronic exposure to indoor air pollutants, including VOCs slowly being released from common consumer products and furniture [12].
The inhalation of VOCs is associated with different adverse health effects. VOCs, such as propylene glycol and glycol ethers (PG), benzene and formaldehyde, have high levels of reactivity with the epithelial lining of the respiratory tract and mucous membrane [10]. The mucous membrane is composed of mucin, a polymer of glycoproteins, which are rich in amine groups [10,13]. These amine-rich regions are nucleophilic sites which react with the C–O polar bonds that are commonly found in VOCs [13]. A continued series of intramolecular reactions result in a double-bonded C–N group, which cross-links with other similar mucin compounds [13]. This chemical reaction results is an antigen substance detected by IgE antibodies, which, in turn, triggers an inflammatory response—the root cause of airway inflammation [13]. Mucin compounds are commonly found in the eyes and esophageal lining, both common locations for irritation and dry skin incidence.
Respiratory health effects of (indoor) VOCs have been the subject of research scrutiny. Several review articles and meta-analyses have already been published [14,15,16]. However, there remains limitations to these studies. First, the relative inconsistency in the conclusion of these studies. In a review by Daisey et al., published in 2003, several of the relevant studies included found positive correlations between asthma and VOCs, which prompted them to conclude that schools should take measures to improve ventilation to reduce VOC concentrations in classrooms [17]. This is in contrast to a meta-analysis conducted by Canova et al., published in 2013. They concluded that there was inadequate evidence of the association between asthma and VOCs [14]. A review by Paciênciaa et al. concluded that high concentrations of VOCs are found indoors, but they did not observe any association between VOCs and asthma. Another review by Nurmatov et al., published in 2015, concluded inadequate evidence of the association between VOCs and asthma [15,16]. Second, most of these reviews or meta-analyses included a limited number of studies and lacked empirical data in their conclusions. Third, most of these studies were published before 2016. A few studies have also been published in recent years focusing on the association between VOCs and asthma. In Rufo et al., Daisey et al., Canova et al. and Paciênciaa et al. the number of studies incorporated in their meta-analyses were six, four, 25 and 40, respectively, and a review by Nurmatov et al. incorporated 50+ studies [14,15,16,17,18]. Finally, none of the mentioned meta-analyses or reviews found solid evidence to infer that there was an association between indoor air pollutants and asthma [14,15,16,17] due to tremendous inconsistency in the results of the studies included in these meta-analyses.
Leveraging the most recent literature (up to 2020) and methods of standardization of the effects size, this meta-analysis aims to address the above research gaps. Specifically, this meta-analysis increases the sample size to 49 relevant studies, which includes empirical data published since 2011 included in Paciênciaa et al.’s review [16], which was published in 2016. Thus, this meta-analysis offers an up-to-date account of the association between indoor VOCs and asthma. This includes all studies which were relevant to our meta-analysis. The remainder of this paper includes materials and methods used in this study, results of the meta-analysis, and a discussion on the findings of our paper vis-à-vis the available literature.

2. Materials and Methods

This study conducted an extensive literature review using the PubMed research database through EndNote software published in English. We searched PubMed, a central database for articles, with the following key words in the abstract or title: (“volatile organic compound” OR “VOC”) AND (“building material” OR “indoor air quality” OR “sick building syndrome”). We used the following criteria to select studies that were included in the meta-analysis: studies which investigated the role of airborne exposure to VOCs in indoor environments in asthma morbidity and/or related pulmonary diseases; studies that included empirical data and results in the form of coefficients, including odds ratios, relative risk and correlation.
Review articles and/or meta-analyses, and articles that reported inconclusive results or that did not measure the levels of VOC directly were excluded. Articles that reported the use of VOCs as a biomarker or as exhaled biomarkers were also excluded, as the exhalation of VOCs causing asthma development was not a focus of this study. After preliminary screening, a total of 246 articles were evaluated for inclusion. However, after reviewing these articles, only 49 studies met the inclusion criteria and were included in the meta-analysis. Only some variables were also noted, including types and concentration of causal (or exposure) variables, sample size, country where the study was conducted, age and gender composition of the sample. This is because these variables are shown to modify and/or mediate the effects of VOCs exposure. For example, the sample size affects the Type 2 error. Likewise, the effect of environmental pollutants, including VOCs, varies by age, gender and region. Moreover, these variables were comparable and available for most studies included in the analysis. Other socio-demographic variables, such as income and occupation, were not included. Even though these variables can confound the effects of VOCs on respiratory diseases, such variables were either not available or not comparable across studies.
Empirical results were found in each study, such as odds ratios (OR) and correlation coefficients (CC). There were variations in different methods of analyzing data and reporting, such as logistic regression, linear regression and correlation. Thus, we standardized these results by computing the standardized effect size using the methodology presented in Borenstein et al. [19]. The effect size that indicates the strength of association between two variables is grouped under three categories: small = 0.1 to 0.3, medium = 0.3 to 0.5 and large = 0.5 to 1. All analyses were conducted in STATA 14.2 (STATA, College Station, TX, USA) [20].

3. Results

A total of 49 studies were included in the meta-analysis. The study characteristics, including VOC types and health outcome(s), of these studies are summarized in Table 1. 37 (87.7%) of the 49 studies were epidemiological, and the remaining 12 were clinical and cross-sectional studies. 15 studies included smokers, and the average number of smokers in these studies was 16.3%. 46 of 49 studies reported ORs, and three of them reported a coefficient of correlations between VOC and pulmonary diseases. 42 of the 49 studies provided sample composition by gender and 49.3% of the sample represented male population (95% confidence interval (CI) 44.8% to 53.9%). Out of the 49 studies, adult subjects without any criteria for a given disease were most frequently included in these studies (n = 23 studies).
A total of 13 air pollutants were included across these studies which were further grouped into four groups: total VOCs (TVOC), multiple VOCs (MVOC), specific VOCs (such as formaldehyde, benzene and toluene), criteria pollutants (such as CO, PM2.5) and paint exposure. 19 (or 38.7%) of the 49 studies assessed TVOCs and 18 (36.7%) of the 49 included specific VOCs. Different health outcomes were grouped into four categories: asthma (23/49), wheezing (10/49), throat irritation (8/49) and others (8/49). About half of these studies focused on the pediatric population and the remaining studies included all age groups or the 18+ population, as summarized in Table 2.
The study specific effect sizes of the association of VOCs and selected diseases or symptoms are presented in Figure 1. The average effects size, irrespective of air pollution and health outcome types, across 49 studies was 0.37, a medium effect size (95% confidence interval (CI) = 0.29–0.44). This effect size varied across countries (Table 3). The highest effects of VOCs on any of the four outcomes was observed in Iran, followed by Korea, Germany, Sweden, The Netherlands and France. The lowest effect of VOCs was observed in Argentina, followed by Australia, South Africa and Canada. The effect size in the US was 0.36, which is close to the average effect size of all studies.
The effect size also varied by disease/symptom (Figure 2A) and VOC types (Figure 2B) as well as by age (Table 4). It is interesting to note that the effects of VOCs was more than two times higher than the effects of criteria pollutants (Figure 2B). Specific VOCs, such as formaldehyde and benzene, had the highest effect size. Although a limited number of studies have examined the association between indoor VOCs and respiratory health in the elderly population, the highest effect size was observed in the elderly population. It is interesting to note that the effect of VOCs in the adult population was 1.6 times higher than in the pediatric population (effect size 0.3 in the pediatric population versus 0.5 in the adult population).

4. Discussion

The results of this study show that VOC exposure has a medium-level association with pulmonary diseases, suggesting that indoor VOC exposure is a moderate risk factor for the onset of pulmonary diseases, including asthma and its associated symptoms, such as wheezing and throat irritation. The effect size varied by country, age and disease/symptom type. Among the confounding factors, we did not find a correlation between smoking and the development of asthma, as the findings of the studies included in the meta-analysis were inconsistent: studies with no smokers had higher effect sizes vis-à-vis those with smokers. Similarly, no correlation between ambient air pollution and the development of respiratory diseases was found. Despite The Netherlands ( x ¯ = 12.1 µg/m3; 95% CI = 11.5–12.6 µg/m3), Germany ( x ¯ = 11.7 µg/m3; 95% CI = 11.7–12.2 µg/m3) and Sweden ( x ¯ = 5.9 µg/m3; 95% CI = 5.8–6.5 µg/m3) having low mean air pollution concentrations of PM2.5, studies from these countries exhibited higher effect sizes for asthma development or exacerbation [70]. The studies from China ( x ¯ = 49.2 µg/m3; 95% CI = 49.7–53.8 µg/m3) with high mean air pollution concentration, showed a small effect. Despite these unexpected anomalies, the findings of this study have public health implications.
VOCs are commonly found in many consumer products and ubiquitously found indoors in HICs [10]. According to the United States Environmental Protection Agency (USEPA), in the United States, the concentration of VOCs is 2 to 5 times higher inside homes than outside [10]. Until recently, our major focus has been on airborne particulate matter (PM). However, the biological mechanisms and management strategies of mitigating exposure to PM are different from that of VOCs. While PM exposure induces oxidative stress [71], VOC exposure induces high chemical reactivity with the amine-rich epithelium lining and mucosa membrane through C–O polar bonding mechanism and subsequent inflammation [13]. Thus, VOC mitigation strategies need to factor in the chemical composition of VOCs. For example, high efficiency air purifiers with an activated carbon filter can reduce VOC concentration [72]. However, it will not eliminate VOC sources, as consumer products continually emit VOCs for months to years. Thus, such filters need to be operational continuously to reduce VOCs. Additional strategies are warranted to target VOC sources by engaging multiple stakeholders in bringing awareness about the danger of VOC exposure, publicly accessible information on consumer products that have VOCs and stringent regulations of consumer products that have VOCs.
The findings of this study must be interpreted in the context of its limitations. First, a limited number of studies were included in the analysis because many studies in the searched literature did not include empirical data on VOCs and respiratory health outcomes. Second, most of these studies were conducted in HICs, with the exception of a few studies in middle-income countries (MICs). Thus, the findings of this study may not be generalizable to the populations of low-income countries (LICs) and MICs, because of striking differences in the levels and types of indoor air pollution in LICs and MICs in comparison to those found in HICs. Moreover, the building design and duration of time people spend indoors also varies across HICs and LICs. Buildings in HICs are sealed for energy conservation and there is less exchange between indoor and outdoor air; consequently, the indoor air pollution concentration builds up over time. However, in LICs there is more indoor and outdoor air exchange because people leave their windows and doors open for ventilation. While it can reduce indoor VOCs from the consumer products, it may increase other air pollutants from outdoor sources if they are found in high concentration outdoors, such as ambient PM found in China and India [73]. Moreover, people spend more time indoors in HICs, and hence are more prone to chronic exposure from indoor air pollution rather than outdoor air pollution. Therefore, people in HICs may bear a relatively higher burden of pulmonary diseases associated with indoor VOCs and other pollutants in comparison to those in LICs and MICs. This was also observed in our study, as the effect size of the association between VOCs and pulmonary health was lower in China with relatively high levels of ambient PM2.5 as compared to HICs with relatively low levels of ambient PM2.5. Third, the sample of studies included from some of the countries was small. For example, only one study each from Argentina and South Africa met the inclusion criteria to be included in the analysis. These countries reported the lowest effects of VOCs on pulmonary diseases. Low exposure to other air pollutants found in these countries can result in downward bias in the effects of VOCs. Moreover, study setting (rural versus urban), sample demographics (age and gender), consumer product choices, local legislations for controlling indoor and outdoor air pollutants and preexisting comorbidities also varied by studies included in our analyses. Therefore, the country-specific effect sizes of VOCs must be interpreted with caution and these factors must be taken into consideration while interpreting the findings reported in this paper. Finally, we have a limited number of studies on all pulmonary diseases and diseases associated with long-term VOC exposure. There were only two studies that examined lung cancer and VOC exposure. Likewise, there was only one study that focused on sleep breathing disorder (SBD), which is shown to mediate the effect of indoor air pollution in pulmonary diseases. Although we found convincing evidence of a medium-sized association between VOCs and pulmonary diseases, further research is warranted to address the above limitations.

5. Conclusions

Based on up to date literature, this paper documents a medium-sized association between VOCs and pulmonary diseases. However, the strength of this association varies by country, age and disease/symptom type. The findings of this paper must be interpreted with caution because most studies included in the meta-analysis were conducted in HICs, and all potential pulmonary diseases were not included. Nonetheless, VOC exposure was associated with asthma and related symptoms, including wheezing and throat irritation. Given VOCs are ubiquitously found indoors, proactive strategies are needed to address this emerging indoor air pollutant to mitigate and manage its associated disease burden.

Author Contributions

Data curation, K.L.A.; methodology and original draft preparation, K.L.A.; conceptualization, N.K.; data curation and analysis, N.K.; writing, N.K.; review and editing, N.K.; visualization, N.K.; supervision, N.K.; project administration and funding acquisition, N.K. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Institute of Environmental Health Sciences (R21ES029765).

Institutional Review Board Statement

Ethical review and approval were waived for this study, because all data used in the paper are publically available and de-identified.

Informed Consent Statement

Not applicable.

Data Availability Statement

All data used in the paper are publically available. We may supply the complied data that we gathered from public sources upon a reasonable request to the corresponding author.

Acknowledgments

The partial financial support for this research was provided by the Department of Public Health Sciences, University of Miami, and National Institute of Health (R21ES029765).

Conflicts of Interest

The authors declare no conflict of interest, and the funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.

References

  1. Vos, T.; Abajobir, A.A.; Abate, K.H.; Abbafati, C.; Abbas, K.M.; Abd-Allah, F.; Abdulkader, R.S.; Abdulle, A.M.; Abebo, T.A.; Abera, S.F.; et al. Global, regional, and national incidence, prevalence, and years lived with disability for 328 diseases and injuries for 195 countries, 1990–2016: A systematic analysis for the Global Burden of Disease Study 2016. Lancet 2017, 390, 1211–1259. [Google Scholar] [CrossRef] [Green Version]
  2. Global Health Estimates. Disease Burden by Cause, Age, Sex, by Country and by Region, 2000–2016; World Health Organization: Geneva, Switzerland, 2018. [Google Scholar]
  3. Milton, B.; Whitehead, M.; Holland, P.; Hamilton, V. The social and economic consequences of childhood asthma across the lifecourse: A systematic review. Child. Care Health Dev. 2004, 30, 711–728. [Google Scholar] [CrossRef]
  4. Perry, R.; Braileanu, G.; Palmer, P.; Stevens, P. The Economic Burden of Pediatric Asthma in the United States: Literature Review of Current Evidence. Pharmacoeconomics 2019, 37, 155–167. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  5. Fitzpatrick, A.M.; Teague, W.G.; Meyers, D.A.; Peters, S.P.; Li, X.; Li, H.; Wenzel, S.E.; Aujla, S.; Castro, M.; Bacharier, L.B.; et al. Heterogeneity of severe asthma in childhood: Confirmation by cluster analysis of children in the National Institutes of Health/National Heart, Lung, and Blood Institute Severe Asthma Research Program. J. Allergy Clin. Immunol. 2011, 127, 382–389. [Google Scholar] [CrossRef] [Green Version]
  6. Simkovich, S.M.; Goodman, D.; Roa, C.; Crocker, M.E.; Gianella, G.E.; Kirenga, B.J.; Wise, R.A.; Checkley, W. The health and social implications of household air pollution and respiratory diseases. NPJ Prim. Care Respir. Med. 2019, 29, 1–17. [Google Scholar] [CrossRef]
  7. The World Bank. GDP (Current US$). 2019. Available online: https://data.worldbank.org/indicator/NY.GDP.MKTP.CD (accessed on 20 August 2020).
  8. Bank, T.W. Global Consumption Database. 2010. Available online: http://datatopics.worldbank.org/consumption/product/ (accessed on 20 August 2020).
  9. FRED. Advance Retail Sales: Furniture and Home Furnishings Stores (RSFHFS). 2020. Available online: https://fred.stlouisfed.org/series/RSFHFS (accessed on 10 August 2020).
  10. EPA. Volatile Organic Compounds’ Impact on Indoor Air Quality. 2020. Available online: https://www.epa.gov/indoor-air-quality-iaq/volatile-organic-compounds-impact-indoor-air-quality (accessed on 10 June 2020).
  11. Lapillonne, B. Cooling Degree Days (CDD): “EnerDemand”. AC Ownership: Internal Data Base from National Sources. GDP per Capita: “Global Energy & CO2 Data” Based on World Bank. 2019. Available online: https://www.enerdata.net/publications/executive-briefing/the-future-air-conditioning-global-demand.html (accessed on 20 August 2020).
  12. Klepeis, N.E.; Nelson, W.C.; Ott, W.R.; Robinson, J.P.; Tsang, A.M.; Switzer, P.; Behar, J.V.; Hern, S.C.; Engelmann, W.H. The National Human Activity Pattern Survey (NHAPS): A resource for assessing exposure to environmental pollutants. J. Expo. Anal. Environ. Epidemiol. 2001, 11, 231–252. [Google Scholar] [CrossRef] [Green Version]
  13. Yun, B.H.; Guo, J.; Turesky, R.J. Formalin-Fixed Paraffin-Embedded Tissues—An Untapped Biospecimen for Biomonitoring DNA Adducts by Mass Spectrometry. Toxics 2018, 6, 30. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  14. Canova, C.; Jarvis, D.; Walker, S.; Cullinan, P. Systematic review of the effects of domestic paints on asthma related symptoms in people with or without asthma. J. Asthma 2013, 50, 1020–1030. [Google Scholar] [CrossRef] [PubMed]
  15. Nurmatov, U.B.; Tagiyeva, N.; Semple, S.; Devereux, G.; Sheikh, A. Volatile organic compounds and risk of asthma and allergy: A systematic review. Eur. Respir. Rev. 2015, 24, 92–101. [Google Scholar] [CrossRef]
  16. Paciencia, I.; Madureira, J.; Rufo, J.; Moreira, A.; Ede, O.F. A systematic review of evidence and implications of spatial and seasonal variations of volatile organic compounds (VOC) in indoor human environments. J. Toxicol. Environ. Health B Crit. Rev. 2016, 19, 47–64. [Google Scholar] [CrossRef]
  17. Daisey, J.M.; Angell, W.J.; Apte, M.G. Indoor air quality, ventilation and health symptoms in schools: An analysis of existing information. Indoor Air 2003, 13, 53–64. [Google Scholar] [CrossRef] [PubMed]
  18. Rufo, J.C.; Madureira, J.; Fernandes, E.O.; Moreira, A. Volatile organic compounds in asthma diagnosis: A systematic review and meta-analysis. Allergy 2016, 71, 175–188. [Google Scholar] [CrossRef] [Green Version]
  19. Borenstein, M.; Hedges, L.V.; Higgins, J.P.T.; Rothstein, H.R. Introduction to Meta-Analysis; John Wiley & Sons, Ltd.: Hoboken, NJ, USA, 2009. [Google Scholar]
  20. Stata. Stata/Mp 14.2—Data Analysis and Statistical Software; Stata Corp. LP: College Station, TX, USA, 2017. [Google Scholar]
  21. Billionnet, C.; Gay, E.; Kirchner, S.; Leynaert, B.; Maesano, I.A. Quantitative assessments of indoor air pollution and respiratory health in a population-based sample of French dwellings. Environ. Res. 2011, 111, 425–434. [Google Scholar] [CrossRef]
  22. Maesano, C.N.; Caillaud, D.; Youssouf, H.; Banerjee, S.; Homme, J.P.; Audi, C.; Horo, K.; Toloba, Y.; Ramousse, O.; Maesano, A.I. Indoor exposure to particulate matter and volatile organic compounds in dwellings and workplaces and respiratory health in French farmers. Multidiscip. Respir. Med. 2019, 14, 33. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  23. Rumchev, K.B.; Spickett, J.T.; Bulsara, M.K.; Phillips, M.R.; Stick, S.M. Domestic exposure to formaldehyde significantly increases the risk of asthma in young children. Eur. Respir. J. 2002, 20, 403–408. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  24. Rumchev, K.; Spickett, J.; Bulsara, M.; Phillips, M.; Stick, S. Association of domestic exposure to volatile organic compounds with asthma in young children. Thorax 2004, 59, 746–751. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  25. Garrett, M.H.; Hooper, M.A.; Hooper, B.M.; Rayment, P.R.; Abramson, M.J. Increased risk of allergy in children due to formaldehyde exposure in homes. Allergy 1999, 54, 330–337. [Google Scholar] [CrossRef] [Green Version]
  26. Flamant-Hulin, M.; Annesi-Maesano, I.; Caillaud, D. Relationships between molds and asthma suggesting non-allergic mechanisms. A rural-urban comparison. Pediatr. Allergy Immunol. 2013, 24, 345–351. [Google Scholar] [CrossRef]
  27. Hulin, M.; Caillaud, D.; Annesi-Maesano, I. Indoor air pollution and childhood asthma: Variations between urban and rural areas. Indoor Air 2010, 20, 502–514. [Google Scholar] [CrossRef]
  28. Choi, H.; Schmidbauer, S.J.; Hasselgren, M.; Spengler, J.; Bornehag, C.G.N. Common household chemicals and the allergy risks in pre-school age children. PLoS ONE 2010, 5, e13423. [Google Scholar] [CrossRef]
  29. Annesi-Maesano, I.; Hulin, M.; Lavaud, F.; Raherison, C.; Kopferschmitt, C.; Blay, F.B.; Charpin, D.A.; Denis, C. Poor air quality in classrooms related to asthma and rhinitis in primary schoolchildren of the French 6 Cities Study. Thorax 2012, 67, 682–688. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  30. Hulin, M.; Moularat, S.; Kirchner, S.; Robine, E.; Mandin, C.; Maesano, I.A. Positive associations between respiratory outcomes and fungal index in rural inhabitants of a representative sample of French dwellings. Int. J. Hyg. Environ. Health 2013, 216, 155–162. [Google Scholar] [CrossRef] [PubMed]
  31. Arif, A.A.; Shah, S.M. Association between personal exposure to volatile organic compounds and asthma among US adult population. Int. Arch. Occup. Environ. Health 2007, 80, 711–719. [Google Scholar] [CrossRef] [PubMed]
  32. Zhai, L.; Zhao, J.; Xu, B.; Deng, Y.; Xu, Z. Influence of indoor formaldehyde pollution on respiratory system health in the urban area of Shenyang, China. Afr. Health Sci. 2013, 13, 137–143. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  33. Villbert, K.; Rauhamaa, H.M.; Haahtela, T.; Saarela, K. Prevalence of Plastic Additives in Indoor Air related to Newly Diagnosed Asthma. Indoor Built Environ. 2008, 17, 455–459. [Google Scholar] [CrossRef]
  34. Gordian, M.E.; Stewart, A.W.; Morris, S.S. Evaporative gasoline emissions and asthma symptoms. Int. J. Environ. Res. Public Health 2010, 7, 3051–3062. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  35. Zhou, C.; Baiz, N.; Banerjee, S.; Charpin, D.A.; Caillaud, D.; Blay, F.D.; Raherison, C.; Lavaud, F.; Maesano, I.A. The relationships between ambient air pollutants and childhood asthma and eczema are modified by emotion and conduct problems. Ann. Epidemiol. 2013, 23, 778–783. [Google Scholar] [CrossRef]
  36. Saijo, Y.; Kishi, R.; Sata, F.; Katakura, Y.; Urashima, Y.; Hatakeyama, A.; Kobayashi, S.; Jin, K.; Kurahashi, N.; Kondo, T.; et al. Symptoms in relation to chemicals and dampness in newly built dwellings. Int. Arch. Occup. Environ. Health 2004, 77, 461–470. [Google Scholar] [CrossRef]
  37. Delfino, R.J.; Gong, H.; Linn, W.S.; Hu, Y.; Pellizzari, E.D. Respiratory symptoms and peak expiratory flow in children with asthma in relation to volatile organic compounds in exhaled breath and ambient air. J. Expo. Anal. Environ. Epidemiol. 2003, 13, 348–363. [Google Scholar] [CrossRef] [Green Version]
  38. Wichmann, F.A.; Muller, A.; Busi, L.E.; Cianni, N.; Massolo, L.; Schlink, U.; Porta, A.; Sly, P.D. Increased asthma and respiratory symptoms in children exposed to petrochemical pollution. J. Allergy Clin. Immunol. 2009, 123, 632–638. [Google Scholar] [CrossRef] [PubMed]
  39. Awano, S.; Takata, Y.; Soh, I.; Yoshida, A.; Hamasaki, Y.; Sonoki, K.; Ohsumi, T.; Nishihara, T.; Ansai, T. Correlations between health status and OralChroma-determined volatile sulfide levels in mouth air of the elderly. J. Breath Res. 2011, 5, 046007. [Google Scholar] [CrossRef] [PubMed]
  40. Kim, J.L.; Elfman, L.; Mi, Y.; Wieslander, G.; Smedje, G.; Norback, D. Indoor molds, bacteria, microbial volatile organic compounds and plasticizers in schools—Associations with asthma and respiratory symptoms in pupils. Indoor Air 2007, 17, 153–163. [Google Scholar] [CrossRef] [PubMed]
  41. Baloch, R.M.; Maesano, C.N.; Christoffersen, J.; Banerjee, S.; Gabriel, M.; Csobod, E.; Oliveira, E.; Annesi-Maesano, I.; SINPHONIE Study Group. Indoor air pollution, physical and comfort parameters related to schoolchildren’s health: Data from the European SINPHONIE study. Sci. Total Environ. 2020, 739, 139870. [Google Scholar] [CrossRef]
  42. Yang, Y.; Luo, H.; Liu, R.; Li, G.; Yu, Y.; An, T. The exposure risk of typical VOCs to the human beings via inhalation based on the respiratory deposition rates by proton transfer reaction-time of flight-mass spectrometer. Ecotoxicol. Environ. Saf. 2020, 197, 110615. [Google Scholar] [CrossRef]
  43. Brinkman, P.; Pol, M.A.V.D.; Gerritsen, M.G.; Bos, L.D.; Dekker, T.; Smids, B.S.; Sinha, A.; Majoor, C.J.; Sneeboer, M.M.; Knobel, H.H.; et al. Exhaled breath profiles in the monitoring of loss of control and clinical recovery in asthma. Clin. Exp. Allergy 2017, 47, 1159–1169. [Google Scholar] [CrossRef] [PubMed]
  44. Trevillian, L.F.; Ponsonby, A.L.; Dwyer, T.; Kemp, A.; Cochrane, J.; Lim, L.L.; Carmichael, A. Infant sleeping environment and asthma at 7 years: A prospective cohort study. Am. J. Public Health 2005, 95, 2238–2245. [Google Scholar] [CrossRef]
  45. Dales, R.E.; Cakmak, S. Is residential ambient air limonene associated with asthma? Findings from the Canadian Health Measures Survey. Environ. Pollut. 2019, 244, 966–970. [Google Scholar] [CrossRef] [PubMed]
  46. Henderson, J.; Sherriff, A.; Farrow, A.; Ayres, J.G. Household chemicals, persistent wheezing and lung function: Effect modification by atopy? Eur. Respir. J. 2008, 31, 547–554. [Google Scholar] [CrossRef] [Green Version]
  47. Tavernier, G.; Fletcher, G.; Gee, I.; Watson, A.; Blacklock, G.; Francis, H.; Fletcher, A.; Frank, T.; Frank, P.C.A. Ipeadam study: Indoor endotoxin exposure, family status, and some housing characteristics in English children. J. Allergy Clin. Immunol. 2006, 117, 656–662. [Google Scholar] [CrossRef]
  48. Zhao, Z.; Zhang, A.; Wang, Z.; Ferm, M.; Liang, Y.; Norback, D. Asthmatic symptoms among pupils in relation to winter indoor and outdoor air pollution in schools in Taiyuan, China. Environ. Health Perspect. 2008, 116, 90–97. [Google Scholar] [CrossRef]
  49. Yeatts, K.B.; Sadig, M.E.; Leith, D.; Kalsbeek, W.; Maskari, F.A.; Couper, D.; Funk, W.E.; Zoubeidi, T.; Chan, R.L.; Trent, C.B. Indoor air pollutants and health in the United Arab Emirates. Environ. Health Perspect. 2012, 120, 687–694. [Google Scholar] [CrossRef]
  50. Veysi, R.; Heibati, B.; Jahangiri, M.; Kumar, P.; Latif, M.T. Indoor air quality-induced respiratory symptoms of a hospital staff in Iran. Environ. Monit. Assess. 2019, 191, 50. [Google Scholar] [CrossRef]
  51. Vanker, A.; Barnett, W.; Workman, L.; Nduru, P.M.; Sly, P.D.; Gie, R.P.; Zar, H.J. Early-life exposure to indoor air pollution or tobacco smoke and lower respiratory tract illness and wheezing in African infants: A longitudinal birth cohort study. Lancet Planet. Health 2017, 1, e328–e336. [Google Scholar] [CrossRef]
  52. Franck, U.; Weller, A.; Roder, S.W.; Herberth, G.; Junge, K.M.; Kohajda, Y.; Bergen, M.V.; Kampczyk, U.R.; Diez, U.; Borte, M. Prenatal VOC exposure and redecoration are related to wheezing in early infancy. Environ. Int. 2014, 73, 393–401. [Google Scholar] [CrossRef]
  53. Fraga, S.; Ramos, E.; Martins, A.; Samudio, M.J.; Silva, G.; Guedes, J.; Fernandes, E.O.; Barros, H. Indoor air quality and respiratory symptoms in Porto schools. Rev. Port. Pneumol. 2008, 14, 487–507. [Google Scholar] [CrossRef] [Green Version]
  54. Norback, D.; Hashim, J.H.; Hashim, Z.; Ali, F. Volatile organic compounds (VOC), formaldehyde and nitrogen dioxide (NO2) in schools in Johor Bahru, Malaysia: Associations with rhinitis, ocular, throat and dermal symptoms, headache and fatigue. Sci. Total Environ. 2017, 592, 153–160. [Google Scholar] [CrossRef] [Green Version]
  55. Araki, A.; Kawai, T.; Eitaki, Y.; Kanazawa, A.; Morimoto, K.; Nakayama, K.; Shibata, E.; Tanaka, M.; Takigawa, T.; Yoshimura, T.; et al. Relationship between selected indoor volatile organic compounds, so-called microbial VOC, and the prevalence of mucous membrane symptoms in single family homes. Sci. Total Environ. 2010, 408, 2208–2215. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  56. Lu, C.Y.; Lin, J.M.; Chen, Y.Y.; Chen, Y.C. Building-Related Symptoms among Office Employees Associated with Indoor Carbon Dioxide and Total Volatile Organic Compounds. Int. J. Environ. Res. Public Health 2015, 12, 5833–5845. [Google Scholar] [CrossRef]
  57. Park, S.A.; Gwak, S.; Choi, S. Assessment of occupational symptoms and chemical exposures for nail salon technicians in Daegu City, Korea. J. Prev. Med. Public Health 2014, 47, 169–176. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  58. Yorifuji, T.; Noguchi, M.; Tsuda, T.; Suzuki, E.; Takao, S.; Kashima, S.; Yanagisawa, Y. Does open-air exposure to volatile organic compounds near a plastic recycling factory cause health effects? J. Occup. Health 2012, 54, 79–87. [Google Scholar] [CrossRef] [Green Version]
  59. Takeda, M.; Saijo, Y.; Yuasa, M.; Kanazawa, A.; Araki, A.; Kishi, R. Relationship between sick building syndrome and indoor environmental factors in newly built Japanese dwellings. Int. Arch. Occup. Environ. Health 2009, 82, 583–593. [Google Scholar] [CrossRef]
  60. Azuma, K.; Ikeda, K.; Kagi, N.; Yanagi, U.; Osawa, H. Physicochemical risk factors for building-related symptoms in air-conditioned office buildings: Ambient particles and combined exposure to indoor air pollutants. Sci. Total Environ. 2018, 616–617, 1649–1655. [Google Scholar] [CrossRef] [PubMed]
  61. Muller, W.J.; Black, M.S. Sensory irritation in mice exposed to emissions from indoor products. Am. Ind. Hyg. Assoc. J. 1995, 56, 794–803. [Google Scholar] [CrossRef]
  62. Venn, A.J.; Cooper, M.; Antoniak, M.; Laughlin, C.; Britton, J.; Lewis, S.A. Effects of volatile organic compounds, damp, and other environmental exposures in the home on wheezing illness in children. Thorax 2003, 58, 955–960. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  63. Araki, A.; Kanazawa, A.; Kawai, T.; Eitaki, Y.; Morimoto, K.; Nakayama, K.; Shibata, E.; Tanaka, M.; Takigawa, T.; Yoshimura, T.; et al. The relationship between exposure to microbial volatile organic compound and allergy prevalence in single-family homes. Sci. Total Environ. 2012, 423, 18–26. [Google Scholar] [CrossRef] [Green Version]
  64. Mendes, A.; Papoila, A.L.; Carreiro-Martins, P.; Bonassi, S.; Caires, I.; Palmeiro, T.; Aguiar, L.; Pereira, C.; Neves, P.; Mendes, D.; et al. The impact of indoor air quality and contaminants on respiratory health of older people living in long-term care residences in Porto. Age Ageing 2016, 45, 136–142. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  65. Diez, U.; Rehwagen, M.; Kampczyk, U.R.; Wetzig, H.; Schulz, R.; Richter, M.; Lehmann, I.; Borte, M.; Herbarth, O. Redecoration of apartments promotes obstructive bronchitis in atopy risk infants—Results of the LARS Study. Int. J. Hyg. Environ. Health 2003, 206, 173–179. [Google Scholar] [CrossRef]
  66. Norback, D.; Bjornsson, E.; Janson, C.; Widstrom, J.; Boman, G. Asthmatic symptoms and volatile organic compounds, formaldehyde, and carbon dioxide in dwellings. Occup. Environ. Med. 1995, 52, 388–395. [Google Scholar] [CrossRef] [PubMed]
  67. Diez, U.; Kroessner, T.; Rehwagen, M.; Richter, M.; Wetzig, H.; Schulz, R.; Borte, M.; Metzner, G.; Krumbiegel, P.; Herbarth, O. Effects of indoor painting and smoking on airway symptoms in atopy risk children in the first year of life results of the LARS-study. Leipzig Allergy High-Risk Children Study. Int. J. Hyg. Environ. Health 2000, 203, 23–28. [Google Scholar] [CrossRef]
  68. Hart, J.E. Invited commentary: Epidemiologic studies of the impact of air pollution on lung cancer. Am. J. Epidemiol. 2014, 179, 452–454. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  69. Zhang, Z.F.; Zhang, H.; Zhang, X.M.; Liu, L.Y.; Li, Y.F.; Sun, W. Indoor occurrence and health risk of formaldehyde, toluene, xylene and total volatile organic compounds derived from an extensive monitoring campaign in Harbin, a megacity of China. Chemosphere 2020, 250, 126324. [Google Scholar] [CrossRef] [PubMed]
  70. WHO. Global Health Observatory Exposure to Ambient Air Pollution. 2016. Available online: https://www.who.int/gho/phe/outdoor_air_pollution/exposure/en/ (accessed on 2 October 2020).
  71. Bates, J.T.; Weber, R.J.; Abrams, J.; Verma, V.; Fang, T.; Klein, M.; Strickland, M.J.; Sarnat, S.E.; Chang, H.H.; Mulholland, J.A.; et al. Reactive Oxygen Species Generation Linked to Sources of Atmospheric Particulate Matter and Cardiorespiratory Effects. Environ. Sci. Technol. 2015, 49, 13605–13612. [Google Scholar] [CrossRef]
  72. Pettit, T.; Irga, P.J.; Torpy, F.R. Functional green wall development for increasing air pollutant phytoremediation: Substrate development with coconut coir and activated carbon. J. Hazard. Mater. 2018, 360, 594–603. [Google Scholar] [CrossRef] [PubMed]
  73. Sinha, J.; Kumar, N. Mortality and Air Pollution Effects of Air Quality Interventions in Delhi and Beijing. Front. Environ. Sci. 2019, 7, 1–10. [Google Scholar] [CrossRef]
Figure 1. Study specific effect size of the association between volatile organic compound (VOC) exposure and four different health outcomes: development of asthma, wheezing, throat irritation and others (which included respiratory symptoms and diseases). The red dash line represents the average effect size.
Figure 1. Study specific effect size of the association between volatile organic compound (VOC) exposure and four different health outcomes: development of asthma, wheezing, throat irritation and others (which included respiratory symptoms and diseases). The red dash line represents the average effect size.
Ijerph 18 01578 g001
Figure 2. Effect size distribution by disease/symptom types (A) and air pollution types (B).
Figure 2. Effect size distribution by disease/symptom types (A) and air pollution types (B).
Ijerph 18 01578 g002
Table 1. List of studies included in the meta-analysis. (TI = throat irritation; SBD = sleep breathing disorder; US = United States; UK = United Kingdom; COPD = chronic obstructive pulmonary diseases; all ages: no specific age break up was available).
Table 1. List of studies included in the meta-analysis. (TI = throat irritation; SBD = sleep breathing disorder; US = United States; UK = United Kingdom; COPD = chronic obstructive pulmonary diseases; all ages: no specific age break up was available).
ID *Ref. IDCountryStudy YearOutcome VariableSample SizeAge (Year)Effect Size
1[21]France2011Asthma1012All ages0.05
2[22]France2019Asthma109All ages0.87
9[23]Australia2002Asthma1921–180.00
10[24]US2003Asthma881–180.11
11[25]Australia1999Asthma1481–180.15
12[26]France2013Asthma951–180.56
13[27]France2010Asthma1141–181.09
14[28]Sweden2010Asthma4001–180.19
19[29]France2012Asthma65901–180.09
20[30]France2013Asthma89718–600.50
21[31]US2007Asthma55018–600.22
22[32]China2013Asthma268All ages0.44
23[33]Finland2008Asthma1371–180.48
26[34]US2010Asthma1480All ages0.42
33[35]France2013Asthma42091–180.27
37[36]Japan2004Asthma31718–600.68
38[37]US2003Asthma241–180.32
40[38]Argentina2009Asthma11831–180.01
42[39]Japan2011Asthma39360+0.89
44[40]Sweden2007Asthma10141–180.32
45[41]Europe2020Asthma51751–180.46
48[42]China2020Asthma12018–600.16
49[43]The Netherlands2017Asthma23All ages0.21
Asthma = effect size ~0.37; 95% CI = 0.25–0.49; n = 23
3[44]Australia1995Wheezing8631–18−0.03
8[45]Canada2018Wheezing290060+0.07
4[46]UK2008Wheezing71621–180.16
16[47]UK2006Wheezing2001–180.17
18[48]China2008Wheezing19931–180.10
25[49]United Arab Emirates2012Wheezing1590All ages0.27
27[50]Iran2019Wheezing45618–600.69
28[51]South Africa2017Wheezing10651–180.11
31[52]Germany2014Wheezing4651–180.76
41[53]Portugal2008Wheezing16071–180.28
Wheezing = effect size ~0.26; 95% CI = 0.10–0.42; n = 10
6[54]Malaysia2017TI4621–180.39
7[55]Japan2010TI12060+0.34
30[56]China2015TI41718–600.03
32[57]Korea2014TI15918–600.67
35[58]Japan2012TI395018–600.53
36[59]Japan2009TI343All ages0.19
43[60]Japan2018TI107All ages0.12
46[61]US1995TI41–180.17
Throat irritation = effect size ~0.31; 95% CI = 0.15–0.46; n = 8
15[62]UK2003Rhinitis62618–600.47
24[63]Japan2012Rhinitis609All ages0.00
29[64]Portugal2016Rhinitis14360+0.49
5[65]US2003Bronchitis1861–180.65
17[66]Sweden1995SBD8818–601.05
39[67]Germany2000COPD6491–180.40
34[68]Canada2014Lung cancer445Others0.19
47[69]China2020Lung cancer0Others0.18
Others = effect size ~0.43; 95% CI = 0.20–0.66; n = 8
* represents ID shown in Figure 1.
Table 2. Sample age by reported health outcomes of the studies included in the meta-analysis.
Table 2. Sample age by reported health outcomes of the studies included in the meta-analysis.
Age Group (Year)AsthmaWheezingThroat IrritationOtherTotal
1–181372224
18–60413210
60+11114
All ages (non-specific)51219
Others00022
Total23108849
Table 3. Effect size (Cohen’s d) by country.
Table 3. Effect size (Cohen’s d) by country.
Country NameEffect Size (95% CI; n)
Australia0.04 (−0.07–0.15; 3)
Japan0.39 (0.16–0.63; 7)
France0.49 (0.20–0.78; 7)
Canada0.13 (0.02–0.25; 2)
Sweden0.52 (−0.01–1.05; 3)
United Kingdom0.27 (0.07–0.47; 3)
United States0.36 (0.21–0.50; 6)
Malaysia0.39 (NA, 1)
China0.28 (0.10–0.45; 5)
Finland0.48 (NA, 1)
United Arab Emirates0.27 (NA, 1)
Iran0.69 (NA, 1)
South Africa0.11 (NA, 1)
Portugal0.39 (0.19–0.59; 2)
Germany0.58 (0.23–0.93; 2)
Korea0.67 (NA, 1)
Europe0.46 (NA, 1)
Argentina0.01 (NA, 1)
The Netherlands0.52 (NA, 1)
Total0.37 (0.29–0.44; 49)
NA = 95% confident interval was not computed, because of an inadequate number of studies.
Table 4. Disease/symptom specific effects size by age groups.
Table 4. Disease/symptom specific effects size by age groups.
Disease/SymptomsAge GroupAll Ages (Non-Specific)
1–1818–6060+
Asthma0.31 (0.15–0.47; 13)0.39 (0.15–0.63; 4)0.89 (NA, 1)0.40 (0.13–0.67; 5)
Wheezing0.22 (0.03–0.41; 7)0.69 (NA, 1)0.07 (NA, 1)0.27 (NA, 1)
Throat Irritation0.28 (0.07–0.49; 2)0.41 (0.03–0.79; 3)0.34 (NA, 1)0.15 (0.09–0.22; 2)
Other0.52 (0.28–0.77; 2)0.76 (0.19–1.33; 2)0.49 (NA, 1)-
Total0.30 (0.19–0.41; 24)0.50 (0.31–0.69; 10)0.45 (0.11–0.78; 4)0.29 (0.11–0.46; 9)
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Alford, K.L.; Kumar, N. Pulmonary Health Effects of Indoor Volatile Organic Compounds—A Meta-Analysis. Int. J. Environ. Res. Public Health 2021, 18, 1578. https://doi.org/10.3390/ijerph18041578

AMA Style

Alford KL, Kumar N. Pulmonary Health Effects of Indoor Volatile Organic Compounds—A Meta-Analysis. International Journal of Environmental Research and Public Health. 2021; 18(4):1578. https://doi.org/10.3390/ijerph18041578

Chicago/Turabian Style

Alford, Kyle L., and Naresh Kumar. 2021. "Pulmonary Health Effects of Indoor Volatile Organic Compounds—A Meta-Analysis" International Journal of Environmental Research and Public Health 18, no. 4: 1578. https://doi.org/10.3390/ijerph18041578

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop