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Environmental monitoring of secondhand smoke exposure
  1. Benjamin J Apelberg1,
  2. Lisa M Hepp2,
  3. Erika Avila-Tang1,3,
  4. Lara Gundel4,
  5. S Katharine Hammond5,
  6. Melbourne F Hovell6,
  7. Andrew Hyland7,
  8. Neil E Klepeis8,
  9. Camille C Madsen2,
  10. Ana Navas-Acien9,
  11. James Repace10,
  12. Jonathan M Samet11,
  13. Patrick N Breysse9
  1. 1Department of Epidemiology, Institute for Global Tobacco Control, Johns Hopkins Bloomberg School of Public Health, Baltimore, USA
  2. 2Department of Health, Behaviour, and Society, Institute for Global Tobacco Control, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland, USA
  3. 3American Academy of Pediatrics Julius B. Richmond Center of Excellence, Elk Grove Village, Illinois, USA
  4. 4Department of Indoor Environment, Lawrence Berkeley National Laboratory, California, USA
  5. 5School of Public Health, University of California, Berkeley, California, USA
  6. 6Center for Behavioural Epidemiology and Community Health, San Diego State University, San Diego, California, USA
  7. 7Department of Health Behaviour, Roswell Park Cancer Institute, Buffalo, New York, USA
  8. 8Department of Civil and Environmental Engineering, Stanford University, Stanford, California, USA
  9. 9Department of Environmental Health Sciences, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland, USA
  10. 10Secondhand Smoke Consultants, Repace Associates, Inc, Bowie, Maryland, USA
  11. 11Department of Preventive Medicine, University of Southern California, Los Angeles, California, USA
  1. Correspondence to Dr Patrick N Breysse, Department of Environmental Health Sciences, Johns Hopkins Bloomberg School of Public Health, 615N. Wolfe St, Baltimore, Maryland 21205, USA; pbreysse{at}jhsph.edu

Abstract

The complex composition of secondhand smoke (SHS) provides a range of constituents that can be measured in environmental samples (air, dust and on surfaces) and therefore used to assess non-smokers' exposure to tobacco smoke. Monitoring SHS exposure (SHSe) in indoor environments provides useful information on the extent and consequences of SHSe, implementing and evaluating tobacco control programmes and behavioural interventions, and estimating overall burden of disease caused by SHSe. The most widely used markers have been vapour-phase nicotine and respirable particulate matter (PM). Numerous other environmental analytes of SHS have been measured in the air including carbon monoxide, 3-ethenylpyridine, polycyclic aromatic hydrocarbons, tobacco-specific nitrosamines, nitrogen oxides, aldehydes and volatile organic compounds, as well as nicotine in dust and on surfaces. The measurement of nicotine in the air has the advantage of reflecting the presence of tobacco smoke. While PM measurements are not as specific, they can be taken continuously, allowing for assessment of exposure and its variation over time. In general, when nicotine and PM are measured in the same setting using a common sampling period, an increase in nicotine concentration of 1 μg/m3 corresponds to an average increase of 10 μg/m3 of PM. This topic assessment presents a comprehensive summary of SHSe monitoring approaches using environmental markers and discusses the strengths and weaknesses of these methods and approaches.

  • Secondhand smoke exposure
  • environmental monitoring
  • nicotine
  • particulate matter
  • methods

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Introduction

In this series of articles, three topic assessments summarising current knowledge about measuring secondhand smoke exposure (SHSe) are presented, covering self-reported measures, environmental measurements and biomarkers, and are based on a multidisciplinary expert meeting held in late 2008 at Johns Hopkins University, Baltimore, USA and supported by the Flight Attendant Medical Research Institute (FAMRI). The meeting addressed SHS assessment approaches to provide uniform methods for FAMRI investigators and others, and to set the stage for innovation. The topic assessments reflect the course of discussion at the meeting, along with recommendations developed from meeting participants, who were established researchers in one of the three focus areas. This article describes methods and strategies used to measure SHSe in the environment, strengths and weaknesses, and approaches discussed and recommended at the expert meeting.

Characteristics of secondhand smoke

SHS, a mixture of thousands of components many of which are toxic and carcinogenic1 is made up of the mainstream smoke exhaled by the smoker and side stream smoke expelled from the end of a lit tobacco product. SHS concentration in the indoor environment depends on the number of cigarettes smoked in a period of time, the volume of the room, the ventilation rate and other processes that eliminate pollutants from the air. These processes vary based on the physical state and properties of the SHS component being measured. In 1986, the National Research Council (NRC), USA, proposed that an environmental marker of SHSe should be ‘unique or nearly unique to the tobacco smoke so that other sources are minor in comparison, a constituent of the tobacco present in sufficient quantity such that concentrations of it can be easily detected in air, even at low smoking rates, similar in emission rates for a variety of tobacco products, and in a fairly consistent ratio to the individual contaminant of interest or category of contaminants of interest (eg, suspended particulates) under a range of environmental conditions encountered and for a variety of tobacco products’.2

Historically, SHSe has been assessed principally by measuring airborne particulate matter (PM) and gas phase nicotine. In the 1980's it was established that cigarette smoking is a potent source of fine indoor airborne PM,3 ,4 and that gas phase nicotine was a sensitive and specific marker of SHSe.5–7 Some markers are specific to tobacco smoke, while others may arise from a variety of sources. None of the environmental markers in use, however, meet all of the 1986 NRC criteria and no single component will reflect the full disease risk from the complex mixture that comprises SHS.8 ,9 The choice of method for measuring environmental SHS concentrations will therefore depend on the study's purpose.10

Evaluating sources and microenvironments

Microenvironments are defined as a fixed location in which a person is exposed to SHS or another pollutant. Typical microenvironments include home, work, hospitality venues (eg, restaurants), school, or automobile. Average SHSe of an individual is the sum of airborne concentrations within each microenvironment (cij ) multiplied by the time spent within each microenvironment (tij ), divided by the total time being considered. The following mass balance equation (adapted from the 2006 Surgeon General's Report (SGR)8), is used:Eavg=cijtijtij where concentration is a function of source strength (number of cigarettes smoked in a given unit of time), room volume, air exchange rates and other removal mechanisms (eg, deposition and chemical reaction).11–13

Table 1 lists the major microenvironments and the key factors that govern how exposure occurs within them. Many studies have described the impact of building size, construction, types of tobacco products smoked, forced or natural air movement, and proximity of smokers and non-smokers on concentrations of SHS constituents in common microenvironments.14 ,16 ,18 ,19 ,21 In indoor environments, the most influential building characteristics are generally room size and ventilation rate. The effects of forced and natural ventilation, as well as air flow in homes, on pollutant concentrations have been measured and studied theoretically.16 ,19 For outdoor settings, proximity to smokers and wind speed and direction are most influential.14 Outdoor exposure only occurs during active smoking or shortly afterwards, as even low wind speeds will rapidly disperse the smoke.

Table 1

Summary of microenvironments and the factors that govern how exposure occurs within them

Validated models can be used to estimate SHS concentrations for typical microenvironments.3 ,8 ,12 ,23 Models based on mass balance equations can predict peak concentrations or time-weighted averaged (TWA) concentrations of SHS markers, (an extensive overview of the application of modelling to predicting particulate matter from SHS is given in Repace,23 Ott,24 and Ott et al 25).

Modelling applications include assessing effectiveness of control measures,8 ,12 ,16 ,26 ,27 interpreting results of field studies,12 and conducting SHS risk assessment.28 These models can be coupled with pharmacokinetic models to estimate or interpret biomarkers for SHS dose.8 ,26

Methods for SHS environmental monitoring

A wide range of approaches has been used to evaluate SHSe. Assessment methods can be grouped based on the chemical target and the collection method (table 2).

Table 2

Summary of approaches for measuring environmental markers of secondhand smoke by chemical analyte and sampling method

Airborne sampling

Many SHS components can be measured using either active or passive sampling. Active sampling uses a pump to draw air into the sample collection device, usually a filter or adsorbent tube, depending on the constituent of interest. Passive monitoring relies on diffusion to a collection surface. Both approaches allow investigators to measure an integrated time-weighted average (TWA) concentration over the sampling period. Direct reading methods, available for some SHS components, allow for real-time measurement of concentration over a variety of time intervals.

Nicotine

Airborne nicotine has been a widely used indicator for SHS in occupational and non-occupational environments.8 ,35 ,74–76 The measurement of airborne nicotine a tobacco-specific constituent reflects tobacco smoke exposure. Sample collection methods are straightforward, and analytical methods are sensitive at low concentrations.35 ,77 ,78 Methods to measure real-time concentrations of air nicotine are not available.

Nicotine sampling is typically conducted using a passive sampler. The sampling device, first described by Hammond and Leaderer,5 is a 35 mm polystyrene sampling cassette holding a filter treated with sodium bisulfate and covered by a diffusion screen allowing air to pass at a constant flow rate. Because the effective sampling rate is relatively low (25 ml/min), passive monitors are typically deployed from days to weeks, depending on the expected nicotine concentration. Exposed filters are extracted and nicotine is typically analysed using either gas chromatography (GC) with a nitrogen/phosphorus detector (NPD), or a mass spectrometer (MS). The TWA airborne nicotine concentration is calculated by dividing the amount of nicotine collected on each filter (μg) by sampled volume of air (m3).

Nicotine can be measured for a shorter period using active sampling with an adsorbent tube or treated filters. Active sampling for nicotine is typically conducted over a span of hours rather than days or weeks. Laboratory analysis methods are similar as those for passive nicotine sampling.

Active and passive nicotine sampling have been used to estimate SHSe in a variety of microenvironments including homes, hospitals, schools, offices, personal and public transportation, and hospitality venues.74 ,76 ,79–86 As passive monitoring often requires integrating longer sampling intervals, including times without occupancy, TWA nicotine concentrations for passive sampling are usually lower than those obtained by active sampling. Both methods are highly effective, however, at discriminating between environments with and without smoking.37 The 2006 Report of the Surgeon General summarises studies in indoor venues in the USA.8 In recent years, numerous studies conducted outside the USA have assessed SHSe levels and evaluated the impacts of policies and controls to reduce exposure.18 ,74 ,87–95

Nicotine is a tracer compound for SHSe that may not always track the mixture of toxic components found in SHS. The relationship between nicotine and other compounds in SHS may vary over time and space (specifically as nicotine is removed from the air through adsorption to surfaces).

Particulate matter

PM, a widely used measure of indoor SHSe, has been assessed in homes, offices, cars and hospitality venues.22 ,43 ,91 ,93 ,96–99 table 3 summarises the key advantages and disadvantages of measuring airborne nicotine and PM for estimating SHSe. PM in indoor air can come from many sources including outdoor air. Although there are several potential sources of PM in indoor environments (eg, cooking with solid fuels, burning candles, outdoor air pollution from open windows or ventilation), tobacco smoking is often the most significant source in venues where smoking is allowed.101 In some settings, however, high background concentrations of PM from other sources makes difficult to assess the impact of SHSe directly.35 ,102

Table 3

Comparison of air nicotine and particulate matter monitoring

PM is typically classified by aerodynamic diameter, for example, PM10 is comprised of particles less than 10 μm in aerodynamic diameter. Most particles produced through tobacco smoking are smaller than 1 μm in diameter.103 For this reason, PM2.5, also known as fine PM, is frequently used as an indirect measure of SHS. Fine PM refers to PM with more potential to cause injury than larger PM because it can penetrate to the gas exchange region of the lung.104 Many studies have shown that ambient fine PM is a risk factor for increased respiratory and cardiovascular morbidity and mortality.104 As a result, the US Environmental Protection Agency regulates outdoor PM and the WHO has proposed PM guidelines for outdoor and indoor air quality.105–107 Although these standards may provide useful comparisons for measured indoor air concentrations, it is important to note that they are based on average daily or annual levels of ambient PM and are not specifically applicable to PM from SHS, although there are similarities.108

PM in indoor environments can be measured through direct reading or active sampling using a filter to collect the particles. Direct-reading devices use a pump to draw air through a light-scattering sensor measuring the real-time concentration of PM in mg/m3, which is recorded continuously are widely used.15 ,38 ,91 ,97 ,109 Direct reading PM monitors, which measure exposure in real time, may be based on other methods of analysis such as a piezobalance technique.15 ,22 ,32 ,37 ,110 Regardless of the detection principle, direct reading PM instruments must be calibrated against gravimetric methods to be used to assess SHSe directly. This is a significant limitation as gravimetric calibration factors can be very different for different aerosol sources and mixtures. If used to evaluate the relative (not absolute) contribution of smoking-related PM to different environments, calibration is less important. A calibration may be an over or under estimate and may differ based on the type of monitoring and machines used. Also, the degree of bias in light-scattering instruments increases at high relative humidity (>60%)111 and, as a result, readings of these instruments must be corrected for humidity effects.112

PM can also be measured directly using active, filter-based sampling followed by gravimetric analysis. PM collected on filters can also be speciated in a laboratory to identify the concentrations of chemical constituents, such as Polycyclic aromatic hydrocarbons (PAHs) or metals. Other types of PM measurements less widely used include ultraviolet PM, fluorescing PM and solanesol PM.

Carbon monoxide (CO)

Carbon monoxide is a gaseous byproduct of incomplete combustion,25 and has historically served as a marker for SHS.29 ,32 ,36 ,39 ,40 ,113–115 While CO is not tobacco specific and levels may increase due to ambient air pollution and indoor sources, studies have demonstrated its usefulness in discriminating between outdoor and non-smoking and smoking environments, especially if cigars are being smoked.22 ,38 ,115 ,116 CO can easily be measured using direct reading instruments containing a CO specific electronic sensor. The use of direct reading monitors makes measuring CO relatively simple.15 ,31 ,32 ,113

3-Ethenylpyridine (3-EP)

The decomposition of nicotine through pyrolysis yields vapour phase 3-EP, and 3-EP is more stable than nicotine in indoor air.50 ,117 The surface absorption rate of 3-EP is also lower than that of nicotine.50 Since 1998, a number of studies have used 3-EP as a SHS marker, mostly tobacco-industry funded,41 ,42 ,46 ,47 ,118 and have shown elevated levels of 3-EP in smoking versus non-smoking areas and high correlations with nicotine and other markers.30 ,41 ,47 Concentrations of 3-EP in the air are typically lower than those of nicotine, resulting from a greater number of non-detectable samples.8 ,118 Sampling methods for detecting 3-EP include active and passive sampling approaches. Laboratory analysis uses GC-MS or NPD.

Polycyclic aromatic hydrocarbons (PAHs)

PAHs are produced during the incomplete combustion of organic materials.25 ,119 There are over 100 different PAHs, and typical human exposure occurs to mixtures of these compounds. In addition to cigarette smoke, airborne sources of PAHs include automobile exhaust, coal combustion, wood burning and wildfires; dietary sources of PAH include grilling or charring meat. Because PAHs are not specific to tobacco, they are not routinely used as SHS markers. Some studies have shown increased concentrations of PAHs in association with greater SHSe,51 ,56 while others have demonstrated no association.57 This may be due in part to the contribution of other sources of PAHs.51 ,56 ,57 Recent studies, however, have shown that cigarettes emit of the order of 14 ng/cigarette, and they report strong correlations between PM and PAH in smoking environments.12 ,120

Although there are more than 100 PAHs, only 10–16 are routinely measured, primarily because of the analytical techniques available.121 Further, PAHs can be found in the particle phase and the vapour phase. As a result, comparisons across studies can be highly dependent on the sampling method, specific analytes measured, their physical phase and the level of background exposure. Depending on the phase of PAHs (particle or vapour), these compounds can be measured through direct reading22 or active integrated sampling, and also with real-time monitors.120 ,122 ,123 Laboratory analysis is conducted using GC-MS.

Tobacco-specific nitrosamines (TSNAs)

TSNAs such as NNK are potent carcinogens found in tobacco smoke. TSNAs metabolites, such as NNAL (4-(methylnitrosamino)-1-(3-pyridyl)-1-butanol) have been used as SHSe biomarkers and indicators of risk of cancer and respiratory disease.124 ,125 Limited data exist to date on concentrations of NNK or other TSNAs in indoor air following tobacco smoking.61 ,62 The studies that have been published were conducted in controlled environments, rather than in field settings.51 ,62 Given the specificity to tobacco and the health risk implications of TSNAs, further research is needed to characterise the feasibility and utility of measuring this class of compounds in indoor air as SHSe markers.

Other constituents

Many other constituents of tobacco smoke have been evaluated as SHSe markers.31 ,40 ,42 ,51 ,63 These include nitrogen oxides, aldehydes, metals and volatile organic compounds; all are non-specific to tobacco smoke but are present in it. Because of their non-specificity to SHS, these analytes are often measured in conjunction with others.

Dust/surface sampling

Dust or surface nicotine concentration can be a surrogate for long-term SHSe and may reflect the potential for indirect exposure. Dust and surface samples have been collected using a handheld vacuum cleaner containing a filter and cotton wipes treated with ascorbic acid.67–70 ,72 ,73 ,109 ,126 ,127 Carpets tend to accumulate more contaminants than hard surfaces and are more likely to represent long-term reservoirs of tobacco smoke constituents. Nicotine has been measured in dust samples using GC-MS67 with findings reported as concentration in ng/mg dust or in units of μg/m2 (dust loading). Wipe samples are analysed with HPLC-tandem mass spectrometry. Nicotine concentrations are typically reported as the mass of nicotine per wipe or per square metre of surface area.

Correlations between house dust nicotine levels and urinary cotinine concentrations and between self-reported smoking in the home have been reported.67 ,70 ,71 In particular, long-term smoking behaviour was predictive of dust nicotine concentrations, suggesting that dust nicotine concentration reflects long-term, cumulative smoking habits, rather than just current smoking behaviour. Studies have suggested that it may be easier to eliminate tobacco-related compounds from air, and that surfaces and dust are long-term reservoirs of tobacco smoke contamination.67 ,70–73 ,126 ,128 ,129 Contaminated microenvironments have been described as a source of third-hand smoke (THS) exposure.130 This concept appears useful because it discriminates differences in toxic agents due to ageing of chemicals from cigarettes and because it offers distinct sources of exposure through physical contact. More research is needed on the dynamics of THS exposure.

Correlations between airborne nicotine, particulate matter and smoking intensity

Nicotine and PM have been among the most widely used environmental SHSe markers. These components have most often been measured separately, so that their relationship to each other has received little attention. In this section, the relationship between airborne nicotine concentrations, PM concentrations, and reported smoking intensity in indoor environments is addressed. Knowledge of relationships among these quantities is useful for retrospective exposure assessment, litigation, or to predict likely exposures and risks.

Nicotine and particulate matter (PM)

Several studies have characterised the relationship between nicotine and PM concentrations in indoor environments (table 4). In all, 17 published articles were identified using PubMed in late 2008 that reported 20 correlations. Correlations between air nicotine and PM concentrations ranged from 0.41 to 0.98.5 ,32 ,34 ,35 ,46 ,79 ,82 ,91 ,131–139 One tobacco industry-funded study conducted in several countries throughout Asia, Europe and North America reported widely disparate findings and was excluded from the summary described here.41

Table 4

Studies reporting the particulate matter to airborne nicotine relationship (ratio) in indoor environments

These correlations were used to generate a regression slope of the relationship between nicotine and PM concentrations, weighted by the number of samples in the study. The slopes for respirable suspended particles (RSP) and PM2.5 were analysed separately and found to be similar. This is not surprising since in environments where SHS is the dominant source of PM, RSP and PM2.5 samples will provide similar exposure estimates. A weighted slope of 10.3 μg/m3 PM per μg/m3 of airborne nicotine was estimated, which is in agreement with the slope reported in the 2006 SGR8 which concludes, ‘for each microgram of atmospheric nicotine in the various environments where people spend time, there is an estimated increase of about 10 μg in secondhand smoke particle concentrations’.8

Although the findings from most studies were generally consistent, variability between nicotine and PM has been reported and could be due to several factors. First, PM can be generated from other non-smoking sources in the indoor environment. Second, several size cut-offs have been used to measure PM in relation to SHS. For example, Rumchev et al 138 measured PM10, Bolte et al 34 measured PM2.5, and Ellingsen et al 132 reported measuring airborne dust collected on filters with a pore size=1.0 μm. In addition, the collection sampling times between and among studies varied dramatically, from several hours to more than 2 weeks. For example, Bolte et al 34 sampled air nicotine and PM actively for 4 h, Rumchev et al 138 collected PM actively and nicotine passively for 24 h, and Agbenyikey et al 91 collected PM actively for 30 min and nicotine passively for 7 days. It is expected that correlations between samples collected over different timeframes would be lower than for samples collected for the same period.

Variability in the relationship between nicotine and PM may also depend on the smoking history of the environment and the characteristics of the indoor space, including wall and floor composition.140 Although nicotine can be measured in the particle phase, it is found mostly in the vapour phase in SHS. Vapour phase nicotine has different removal processes than particles (eg, adsorption to surfaces and re-emission into the environment).131 ,140 Despite variation across studies, a moderate to strong correlation was most often found between concentrations of these two SHS tracers.

Nicotine and smoking intensity in field settings

Few studies describe the slope of the relationship between nicotine concentration and cigarettes smoked. Leaderer and Hammond35 report that for each cigarette smoked, week-long air nicotine concentrations measured in the main living area of residences increased by 0.026 μg/m3, on average. Among 12 studies identified using PubMed in late 2008, the correlations ranged from 0.25 to 0.88. One limitation to comparing the associations is the differing characterisations of smoking intensity. For example, Berman et al 141 used ‘cigarettes per day smoked in the home’, while O'Connor et al 142 used ‘total number of smokers to whom the subject was exposed’.143 Varying SHSe indices have been used, including hours of SHSe, number of smokers and proximity. The majority of measures for cigarettes smoked are questionnaire based, while some studies employed more detailed information including daily records of children's exposure kept by parents144 or observation during the sampling time.139 Overall, the expected positive association between cigarettes smoked and air nicotine concentration in real-world field settings has been established.

Particulate matter and smoking intensity in field settings

The literature generally suggests an increase of 1 μg/m3 of PM for each cigarette over an extended period of time.69 ,145 ,146 Across studies reviewed, correlations in field locations ranged from 0.44 to 0.82.12 ,34 ,35 ,69 ,135 ,147–151 The descriptors used for cigarettes smoked in these studies are even more varied than those used in the nicotine studies. For example, Hyland et al use active smoker density (eg, average number of burning cigarettes per 100 cubic metres),147 Bolte et al use number of smokers in the location,34 Brauer et al use the average number of burning cigarettes counted,148 while Leaderer and Hammond et al use the number of self-reported cigarettes smoked during the sampling period.35 These were also collected through self-reported questionnaires or observation. Even though PM can be produced by sources other than cigarette smoking, it is clear that there is a positive relationship in field settings between the amount of smoking taking place and PM concentrations.

Environmental SHS monitoring has numerous applications in research and policy development, including studies on the adverse health effects of SHSe, research supporting development and evaluation of smoke-free legislation, and evaluations of the impact of interventions and control measures to reduce SHSe (table 5).

Table 5

Hierarchy of secondhand smoke exposure assessment using environmental markers for epidemiological studies

Conclusions

This topic assessment summarises the most widely used methods and applications for SHS environmental monitoring, including vapour-phase nicotine and respirable PM. Air nicotine measurement has the advantage of being tobacco specific. Additionally, sample collection methods are relatively straightforward, and analytical methods are sensitivity at low concentrations. However, to date, methods to measure real-time concentrations of air nicotine are not available, and therefore laboratory analysis is necessary. Airborne PM in indoor environments can be measured through direct reading or active gravimetric sampling. Direct reading instruments generate real-time concentrations; however, although tobacco smoking remains a significant source of PM in venues where smoking is allowed, in some settings, high background concentrations may make it difficult to assess small increases or changes in SHSe directly. In general, when nicotine and PM are measured in the same setting using a common sampling period, an increase in nicotine concentration of 1 μg/m3 corresponds to an average increase of 10 μg/m3 of PM. TSNAs, which are potent human carcinogens, may prove to be particularly useful SHS markers. However, to date, limited field studies have been undertaken to validate their use. In more recent years, environmental SHS monitoring has included nicotine measurement in dust and on surfaces in homes and other indoor environments to assess long-term SHSe and the potential for indirect exposure. Future studies should focus on validating dust measures as surrogates for long-term SHSe and as a possible route for indirect exposure, particularly for children. Environmental SHS monitoring should continue to provide important evidence needed to develop and implement tobacco control policies around the world.

Acknowledgments

The authors would like to thank Nicole Ammerman and Charlotte Gerczak for their technical and editing assistance, respectively. The authors would also like to thank Drs Wael Al-Delaimy, David L Ashley, Neal L Benowitz, John T Bernert, Dana Best, K Michael Cummings, Geoffrey Fong, Stephen Hecht, Sungroul Kim, Jonathan Klein, Robert McMillen and Jonathan P Winickoff for their participation in the expert meeting.

References

Footnotes

  • Funding This work was supported by grants from the Flight Attendant Medical Research Institute to the Johns Hopkins Center of Excellence; the University of California, San Francisco Bland Lane Center of Excellence; and the American Academy of Pediatrics Julius B Richmond Center of Excellence. The funding organisation had no role in the preparation of the manuscripts.

  • Competing interests None.

  • Provenance and peer review Not commissioned; externally peer reviewed.

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