Exposure to nitrosamines in thirdhand tobacco smoke increases cancer risk in non-smokers
Graphical abstract
Introduction
Each year 600,000 people die worldwide from exposure to environmental tobacco smoke (Oberg et al., 2011), also called second hand smoke (SHS). As numerous countries have introduced smoking bans in public places (WHO, 2010), domestic environments have become the main sources of passive smoking exposure (WHO, 2007). However, the risks of tobacco exposure do not end when a cigarette is extinguished and non-smokers, especially children, are also at risk through contact with surfaces and dust contaminated with residual smoke gases and particles, the so-called third hand smoke (THS) (Matt et al., 2004, Matt et al., 2011a). Over 40% of children have at least one smoking parent (Oberg et al., 2011) and numerous studies have demonstrated the association between prenatal and early stage childhood diseases and the smoking habits of their parents (Cook and Strachan, 1999). Although there is a general public awareness about the harms of SHS, the general public are more sceptical about THS, with a study in 2009 finding that 62.5% of non-smokers and 43% of smokers agreed that THS harms children (Winickoff et al., 2009). A study of parents' attitudes found that fathers and heavy smokers (> 10 cigarettes per day) were less likely to believe that THS was harmful (Drehmer et al., 2012). The specific role of THS in tobacco-related illnesses has been questioned by the public health community (Matt et al., 2011a), however, a recent study demonstrated that chemical species associated with THS are genotoxic in human cell lines (Hang et al., 2013). Evidence of the chemical toxicity of THS is necessary to improve understanding of the risks of THS-polluted environments and to design educational strategies for families and the general public to allow them to make more informed decisions.
Nicotine is the most abundant organic compound emitted during smoking (IARC, 2004) and is considered a good marker of tobacco exposure. After cigarette smoking, nicotine deposits almost entirely on indoor surfaces, where it can be released again to the gas phase or react with ozone, nitrous acid and other atmospheric oxidants producing secondary pollutants, such as tobacco-specific nitrosamines (TSNAs) (Sleiman et al., 2010). Fig. 1 shows the structures and reaction pathways of formation of the main TSNAs. Of the TSNAs identified, N′-nitrosonornicotine (NNN) and 4-(methylnitrosoamino)-1-(3-pyridyl)-1-butanone (NNK) are the most prevalent and most active carcinogens in tobacco products (Hecht, 2003, Hecht and Hoffmann, 1988), inducing tumours in the lung, liver, nasal cavities, oesophagus and exocrine pancreas, and are classified as carcinogenic for humans (Group 1 International Agency for Research on Cancer, IARC) (IARC, 2007). Whilst some TSNAs can be directly produced during tobacco smoking, several studies have suggested that airborne NNK concentrations in sidestream cigarette smoke can increase by 50–200% per hour during the first 6 h after cigarettes are extinguished (Schick and Glantz, 2007). Moreover, NNK can further degrade and its main metabolite, 4-(methylnitrosoamino)-1-(3-pyridyl)-1-butanol (NNAL), is considered to have similar adverse health effects (Hecht, 2008).
Given the low volatility of TSNAs and the high levels of nicotine typically found in environments contaminated with tobacco, TSNAs can persist for weeks to months in THS. Several studies have detected nicotine in indoor dust and surfaces (Kim et al., 2008, Matt et al., 2011a) and recent studies have demonstrated a correlation between the number of cigarettes smoked and the presence of nicotine and polycyclic aromatic hydrocarbons (PAHs) (Hoh et al., 2012) in settled house dust. The health risk from THS will be substantially controlled however by the prevailing levels of TSNAs. Whilst these species have been seen directly in tobacco smoke (Mahanama and Daisey, 1996), there has been no measurement of their presence in THS.
Here we report the detailed determination of nicotine and five TSNAs (indicative of a tobacco smoking source) and eight non-specific volatile N-nitrosamines (commonly released during tobacco smoking, but likely to have additional environmental sources), in settled house dust samples from homes occupied by smoking or non-smoking occupants. The complete list of these target compounds is shown in Table 1. We have calculated the cancer risk related to exposure to observed concentrations of the carcinogen N-nitrosamines and TSNAs through non-dietary ingestion and dermal exposure by age group. For the first time, we use ambient observations to constrain risk assessment estimations of exposure to these carcinogens in THS, based on real-world measurements.
Section snippets
Sample collection and preparation
A total of 46 house dust samples were collected from private homes, using conventional vacuum cleaners in regular use in households between October 2011 and May 2012 in the area of Tarragona (north-eastern Spain). We have selected those samples whose residents have lived in their current home for at least one year. A questionnaire was designed to collect information about the house and any activity that might affect chemical loading (see Supplementary Material, Table S1). A summary of the
Nicotine and nitrosamines in settled house dust
A summary of the concentrations of the 14 target compounds analysed in this study in house dust samples collected in the homes classified as smokers' and non-smokers' is shown in Table 3. The number of occurrences of each compound in the samples is also indicated. As expected, the total concentrations of the 14 target compounds in house dust were higher in smokers' homes than in the non-smokers' ones, with total abundances up to a factor of 60 higher, and with median concentrations around a
Discussion
Since the detection of nicotine in house dust for the first time by Hein et al. in 1991 (Hein et al., 1991), the contamination of residential homes with THS has been demonstrated mainly based on the occurrence of nicotine, 3-ethenylpyridine and polycyclic aromatic hydrocarbons in dust, air and surfaces of smokers' homes and non-smokers' homes formerly occupied by smokers (Hoh et al., 2012, Matt et al., 2004, Matt et al., 2011b, Singer et al., 2003). The potential role of THS in tobacco-related
Conclusions
In this study, we have determined the presence of nicotine, eight volatile N-nitrosamines and 5 TSNAs in settled house dust samples from smokers' and non-smokers' homes. Our study demonstrates for the first time the widespread presence of tobacco related carcinogens in house dust, even in “smoke free” environments. Cancer risk assessment of the carcinogen compounds showed that settled dust is a major route of exposure to TSNAs in children and non-smokers who are not directly exposed to
Acknowledgments
NR, MZO, ACL and JFH want to acknowledge the financial support of the UK Natural Environment Research Council (Grant NE/J008532/1) and FB and RMM the support of the Direcció General de Recerca of the Government of Catalonia through project 2009SGR223. The authors acknowledge Dr J. Ferré for the statistical discussions, Dr M. Pedrouzo for the lab assistance and the householders of the selected homes for their kind help on collecting the settled dust samples and answering the survey.
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