1. Exposure Data

1.2. Chemical composition of tobacco smoke

1.2.1 Smoke from cigarettes

One cubic cm of fresh, un-aged cigarette mainstream smoke [the smoke emerging from the mouth end of a cigarette during smoking] has about 4 × 10⁹ particles with a mean diameter of about 0.2 µm (Borgerding & Klus, 2005). The size of the particles increases as the smoke ages. Temperatures in the burning cone of the cigarette are about 800 °C during the smoulder period between puffs and increase to 910–920 °C at the periphery of the cone during puffing (Borgerding & Klus, 2005). Hydrogen is generated in the glowing cone, resulting in an oxygen deficient reducing atmosphere (Borgerding & Klus, 2005). The approximate composition of mainstream smoke of a plain cigarette is summarized in Table 1.1 (Borgerding & Klus, 2005). The total particulate matter, after subtraction of the amounts of nicotine and water, is referred to as ‘tar’.

Table 1.1

Approximate chemical composition of mainstream smoke generated by a plain cigarette.

Over 5300 compounds have been identified in tobacco smoke (Rodgman & Perfetti, 2009). Classes of compounds include but are not limited to neutral gases, carbon and nitrogen oxides, amides, imides, lactams, carboxylic acids, lactones, esters, aldehydes, ketones, alcohols, phenols, amines, N-nitrosamines, N-heterocyclics, aliphatic hydrocarbons, monocyclic and polycyclic aromatic hydrocarbons (PAHs), nitriles, anhydrides, carbohydrates, ethers, nitro compounds and metals (Rodgman & Perfetti, 2009).

The addictive properties of tobacco smoke are attributed to nicotine, the principal tobacco alkaloid in smoke (Hukkanen et al., 2005). Minor tobacco alkaloids include nornicotine, anatabine and anabasine (Hukkanen et al., 2005). The tobacco alkaloids are not generally considered carcinogenic, but are accompanied by carcinogens in each puff of smoke.

There are over 70 carcinogens in tobacco smoke that have been evaluated by the IARC Monographs programme as having sufficient evidence for carcinogenicity in either laboratory animals or humans (IARC, 2004a). The different chemical classes of carcinogens and representatives of each are presented in Table 1.2 (IARC, 2004a). Sixteen of these – benzo[a]pyrene (BaP), 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone (NNK) and N′-nitrosonornicotine (NNN), 2-naphthylamine, 4-aminobiphenyl, formaldehyde, 1,3-butadiene, benzene, vinyl chloride, ethylene oxide, arsenic, beryllium, nickel compounds, chromium VI, cadmium, and polonium-210 – are classified as carcinogenic to humans (Group 1). Structures of some representative carcinogens in cigarette smoke are shown in Fig. 1.1. There are other likely carcinogens in cigarette smoke that have not been evaluated by the IARC Monographs programme. These include, for example, PAHs with incompletely characterized occurrence levels and carcinogenic activities; over 500 PAHs have been identified (Rodgman & Perfetti, 2006).

Table 1.2

Tobacco smoke carcinogens evaluated in the IARC Monographs.

Fig. 1.1

Structures of some representative tobacco smoke carcinogens

PAHs, tobacco-specific N-nitrosamines, aromatic amines, aldehydes and certain volatile organics likely contribute significantly to the carcinogenic activity of tobacco smoke (Hecht, 2003).

In the early part of the 20^th century, PAHs were identified as carcinogenic constituents of coal tar (Phillips, 1983). They are products of incomplete combustion of all organic matter and occur, always as complex mixtures, in tars, soots, broiled foods, vehicle engine exhaust and tobacco smoke. PAHs are generally locally acting carcinogens, and some, such as the prototypic compound BaP, have strong carcinogenic activity on mouse skin and in rodent lung. Heterocyclic analogues of PAHs also occur in cigarette smoke. Concentrations of individual PAHs in mainstream cigarette smoke are generally in the range of 1–50 ng per cigarette (IARC, 2004a).

Among the carcinogenic N-nitrosamines in tobacco smoke are tobacco-specific N-nitrosamines, which are derived from, and structurally related to, the tobacco alkaloids. Two of the most important of these are NNK and NNN (Hecht & Hoffmann, 1988). Levels of NNK and NNN in cigarette smoke vary depending on tobacco type and other factors, but are frequently in the range of 50–200 ng per cigarette (IARC, 2004a).

Aromatic amines were first identified as human carcinogens from industrial exposures in the dye industry in the early part of the 20^th century. They include the well known human bladder carcinogens 2-naphthylamine and 4-aminobiphenyl which, along with other isomers, are found in cigarette smoke, but their levels are generally quite low (1–20 ng per cigarette) (IARC, 2004a).

Aldehydes such as formaldehyde and acetaldehyde occur widely in the human environment and are also found in human blood. Concentrations of acetaldehyde and formaldehyde in cigarette smoke are far higher than those of PAHs, N-nitrosamines or aromatic amines but their carcinogenic activities are weak (Hecht, 2003). Cigarette mainstream smoke typically contains 10–30 µg formaldehyde/cigarette and 800–900 µg acetaldehyde/cigarette (IARC, 2004a).

Volatile hydrocarbons in cigarette smoke include 1,3-butadiene, a powerful multiorgan carcinogen in the mouse, and benzene, a known human leukaemogen. 1,3-Butadiene (20–40 µg/cigarette) and benzene (12–50 µg/cigarette) are two of the most prevalent strong carcinogens in cigarette smoke (IARC, 2004a).

In summary, cigarette smoke is an exceedingly complex mixture which contains over 5300 compounds including multiple toxicants and carcinogens.

1.2.2 Smoke from other tobacco products

Some constituents have been measured in roll-your-own cigarettes, and their levels are comparable to or higher than those in commercial brands. Carcinogen and toxicant levels expressed per unit are higher in cigars than in cigarettes because of their larger size, and in some instances are also higher per litre of smoke. Levels of nicotine and tobacco-specific nitrosamines were comparable in bidis and commercial Indian cigarettes; bidis also contain high levels of eugenol, as do kreteks. Levels of NNK and NNN in chuttas were considerably higher than in standard cigarettes (IARC, 2004a).

1.3. Prevalence of tobacco smoking

1.3.1 Data collection and methods

Data on smoking tobacco are available from WHO's Global Infobase (www.who.int/infobase) and the WHO Global Health Observatory (www.who.int/gho/en) – repositories of information on tobacco use and other risk factors in young people (13–15 years old) and adults (aged 15 years and over). The data span several years and are acquired from government reports, journals and unpublished sources. WHO has in the recent past used and modelled these data to produce estimates of tobacco smoking prevalence, published in the WHO Reports on the Global Tobacco Epidemic. For a complete explanation of methods used, the reader is referred to the Technical Note on Prevalence in the 3^rd WHO Report on the Global Tobacco Epidemic (WHO, 2011). The six WHO regions are: EMRO, Eastern Mediterranean Region; EURO, European Region; AFRO, African Region; WPRO, Western Pacific Region; SEARO, South East Asian Region; AMRO, Region of the Americas. A listing of the countries in each region can be viewed at http://www.who.int/about/structure/en/index.html.

1.3.2 Distribution of smokers by WHO region and country

WHO estimates that in 2009, there was about 1.1 billion adult smokers worldwide, representing nearly a quarter (22%) of the global adult population (WHO, 2011). A disaggregation by the six WHO regions (Fig. 1.2) shows that over a third of smokers worldwide live in WPRO (highly influenced by the People’s Republic of China), followed by SEARO, which has around a fifth of the world’s smokers (influenced by India and Indonesia).

Fig. 1.2

Proportion of adult smokers by WHO region in 2009

The number of smokers in any country is a function of both the prevalence of smoking and the size of the population. A further disaggregation of the regions by country shows that a few countries account for a large proportion of tobacco smokers. Ranked in descending order of the number of smokers, the five countries of China, India, United States of America (USA), Russian Federation and Indonesia account for about 52% of adult smokers in the world, with China and India alone accounting for 40% (Fig. 1.3). Furthermore, nearly two-thirds of the world’s smokers live in only ten countries of the world.

Fig. 1.3

Proportion and cumulative percentage of smokers in high-burden countries, in men (A) and women (B) in 2009

1.3.3 Distribution of smokers by sex

With a global average smoking prevalence of 36%, men account for just over 80% of all smokers. The male adult prevalence is 4–5 times that for women, at 8%. This difference varies across WHO regions. Smoking among men, concentrated in the five countries of China, India, Indonesia, Russian Federation and USA (Fig. 1.3), accounts for about 56% of global smoking among men. Women smokers are mostly concentrated in EURO and AMRO. These two regions account for 40% and 26% of all women smokers globally, respectively. The prevalences for women in these two regions are about half of those in men, whereas the difference is substantially greater in the other regions. Just as men smoke more than women everywhere, so too among young people, boys generally smoke more than girls. There is an increasing concern, however, that the gap may diminish, not because of a reduction in boys prevalence but because of an increase in the proportion of girls who are taking up smoking (Warren et al., 2006).

1.3.4 The four stage smoking model

(a) The four stages of tobacco use

Lopez et al. (1994) used trend data on smoking prevalence and tobacco attributable mortality to show the evolution of tobacco use in a country. Four stages of smoking and attributable mortality have been identified to represent the growth and eventual decline of smoking among men and women (Fig. 1.4).

Fig. 1.4

The four stages of the tobacco epidemic

Stage 1 is characterized by low smoking prevalence in men (less than 15%) and very low in women (less than 10%). Death and disease from smoking are not apparent in this phase, as nearly all health effects from smoking are related to past smoking habits and their cumulative effects rather than current smoking. In Stage 2, smoking prevalence in men rapidly increases while it increases more slowly in women. Towards the end of this stage, smoking prevalence in men typically peaks to lie at 50–60%, with 10% of deaths in men attributable to smoking; deaths in women are comparatively fewer. After a protracted period of high smoking prevalence, Stage 3 shows a decline in smoking prevalence in men to around 40%. Smoking prevalence in women peaks and then begins to decline; towards the end of this stage the gap between men's and women's prevalence starts to narrow. However, smoking attributable deaths in men increase from around 10% to 25–30% within a span of three decades; in women the deaths are increasing but are still quite low. In the final Stage 4, smoking prevalences in both men and women continue to decline albeit relatively slowly in comparison with Stage 3, with the gap substantially narrowing to lie at around five percentage points, and as little as one percentage point in some countries. In Stage 4, smoking mortality in men peaks to between 30–35% and then declines to below 30% at the end of this period. In women, the health effects from past smoking persist, with increasing mortality, but remain lower than in men, and recently have begun to decline in some countries.

(b) Smoking prevalence worldwide

Using prevalence data for men and women collected in 2006 for 140 countries, WHO determined at which stage of the tobacco epidemic countries are in the model of Lopez et al. (1994). In Fig. 1.5, countries have been ranked by smoking prevalence in men in ascending order for Stages 1 and 2, and then in descending order for Stages 3 and 4. (Smoking prevalence in men is almost always higher than in women, with a few exceptions observed in the fourth stage.) While most countries fit the classification, there are a few exceptions, most of which in the last stage. Prevalence between Stage 3 and Stage 4 is discontinuous in both sexes. This is due to the classification followed, which puts countries with a relatively narrow difference in prevalence between men and women in Stage 4 even though their prevalence is largely comparable with those in Stage 3.

Fig. 1.5

Prevalence of smoking in 140 countries in 2009, staged according to the model by Lopez

Most African countries fall in the first stage of the smoking model, characterized by low smoking prevalence in men and very low prevalence in women. Three of the five high burden countries fall in stage 2 (India, Indonesia and China), with the rest comprising a combination of countries from Africa, South East Asia, eastern Europe and the Middle East. At this stage smoking prevalences in women continue to remain very low, most countries having a prevalence in adult women of less than 10%.

Stage 3 includes the fourth high burden country (Russian Federation), along with countries in eastern Europe, South America and western Europe, which fall at the end of Stage 3. Stage 4 is populated entirely by the developed countries of western Europe, North America and Oceania. The USA, the fifth high burden country, fall in the last stage as a result of the relatively small difference in the smoking prevalence between men and women compared to the other intermediate stages. As mentioned before, Stage 4 includes countries where the smoking prevalence is higher in women than in men, with a small (< 8%) difference.

(c) Age-specific prevalence

Age-specific prevalence for men and women aged 15 years or older is presented for six representative countries for current smoking (Fig. 1.6). There are wide variations in age-specific prevalence between these countries. In men, prevalence varies from less than 10% to 75% in the 15–19 years age range to lie between 10% and 55% in the oldest age range. Prevalence among women varies from less than 1% to as high as 45% in young adults (15–19 years). Unlike men, prevalence in women tends to converge after age 50, lying within 15 percentage points. Prevalence in women is almost always lower than in men in all age groups.

Fig. 1.6

Age-specific rates of smoking prevalence, in men and women in 2009

Initiation of smoking is shifting, and is taking place at earlier ages in both developed and developing countries. In developed countries, quitting smoking is also shifting to occur at a younger age, whereas in developing countries there is no such evidence.

(d) Smoking in youth

Information on smoking habits in youth are collected from a variety of youth surveys that include the Global Youth Tobacco Survey (GYTS), Global school-based Student Health Survey (GSHS) and Health Behaviour in School Aged Children (HBSC). Some countries have their own youth surveys, or have them as part of a general health or household survey, such as the Student Survey in Argentina, the Youth Smoking Survey in Canada, and New Zealand's Tobacco Survey.

The GYTS is a school-based survey designed to monitor tobacco use among youths aged 13 to 15 years. The GYTS uses a standard set of questions and sampling methods in over 160 countries. The survey has core questions that span seven thematic areas pertinent to tobacco. In addition to these, countries can include country-specific questions that allow assessment of tobacco use unique to the country. To assess prevalence of smoking, students are asked to report their smoking habits for both cigarettes and other tobacco products that they may have consumed over the past 30 days. Since its inception in 1999, the GYTS has covered over 2 million students. Although most GYTS are national surveys, in some countries they are limited to subnational locations. Further, countries conduct the GYTS in different years, rendering comparison for the same year difficult.

Prevalence of current tobacco use [including smokeless tobacco] in youth in 2004–09 for fourteen high burden low and middle income countries is shown in Fig. 1.7. The Russian Federation has the highest prevalence of current tobacco use among the high burden countries for which national data are available. Further, in the Americas and Europe the difference in prevalence between boys and girls is smaller than in other regions. In contrast, in Egypt, India and Thailand, prevalences in boys are significantly higher than in girls.

Fig. 1.7

Prevalence of current tobacco use in youth for selected countries, 2005–2009

Fig. 1.8 shows the range of current tobacco use by WHO region for boys and for girls and for both sexes combined. There are wide variations in current tobacco use within each region. The largest variations are observed in EMRO and SEARO irrespective of sex, reflecting potentially disparate initiation rates in countries within the region. In AFRO, the range of current tobacco use between boys and girls is virtually the same. In some countries (e.g. Argentina, Peru, Sierra Leone, Bulgaria, Croatia, Cook Islands, New Zealand), tobacco use in girls exceeds that in boys; but overall boys and girls show remarkably similar propensity to take up tobacco use.

Fig. 1.8

Range of prevalence of current tobacco use in youth, 2005–2009, by WHO region

Warren et al. (2006) present global estimates and regional averages for current tobacco smoking in youth using GYTS data spanning 1999–2005. Their estimates show that one in five boys and one in seven girls currently smoke tobacco. Prevalence of current smoking for both boys and girls combined was highest in AMRO (22.2%) and lowest in WPRO (11.4%). AMRO have the highest average for current tobacco smoking for boys (24%) and for girls (20.4%) whereas the lowest prevalence was in WPRO among boys (15%) and in SEARO among girls (7.1%).

2. Cancer in Humans

3. Cancer in Experimental Animals

3.1. Mainstream tobacco smoke

3.1.1 Mouse

There have been multiple studies of the carcinogenic potential of tobacco smoke in mice (Table 3.1). Lifetime exposure of several mouse strains to cigarette smoke failed to result in the production of lung tumours (Harris & Negroni, 1967; Otto & Elmenhorst, 1967; Henry & Kouri, 1986). However, studies involving lifetime exposure of C57BL mice to a mixture of flue-cured or air-cured cigarette smoke or to the gas phase of flue-cured cigarette smoke led to significant increases in the number of lung tumours (adenomas) (Harris et al., 1974). Similarly, lifetime exposure of Snell’s mice to the gas phase of cigarette smoke led to an increased incidence of lung adenocarcinomas (Leuchtenberger & Leuchtenberger, 1970). Exposure of B6C3F₁ female mice to smoke for lifetime led to increased incidence of lung adenomas, bronchiolar papillomas and lung adenocarcinomas in smoke-exposed mice. In addition, the occurrence of squamous cell carcinomas of the nasal cavity in smoke-exposed mice was increased (Hutt et al., 2005). In a recent study, Swiss mice were exposed whole-body to cigarette smoke for 120 days, starting within 12 hours of the birth. Smoke-exposed mice developed microscopic lung tumours beginning only 75 days after birth and reaching an overall incidence of 78.3% after 181–230 days. The mean lung tumour multiplicity was 6.1 and 13.6 tumours per mouse in males and females, respectively. In addition, malignant tumours, some of which may have had a metastatic origin, were detected in the urinary tract of smoke-exposed mice (Balansky et al., 2007).

Table 3.1

Carcinogenicity in response to mainstream tobacco smoke in animals.

3.1.2 Rat

Several studies have evaluated the carcinogenic potential of mainstream tobacco smoke in rats (Table 3.1). Exposure of Wistar rats to cigarette smoke for lifetime did not increase the lung tumour incidence (Davis et al., 1975). In contrast, exposure of Fischer 344 rats to a mixture of non-filter cigarette smoke for 128 weeks resulted in an increased incidence of nasal and lung tumours. There was also an increase in subcutaneous sarcomas at forelimb ulceration sites (Dalbey et al., 1980). CDF rats were exposed to low-dose cigarette smoke (LCS) or high-dose cigarette smoke (HCS) for 126 weeks. The incidence of lung tumours was significantly higher only in female rats that received HCS (Finch et al., 1995). In a recent study, Fischer 344 rats received whole body exposure to smoke containing either 100 mg (LCS) or 250 mg (HCS) total particulate matter/m³ for 30 months. This led to significant increases in the incidence of lung and nasal cavity tumours in male rats treated with HCS but not with LCS. In female rats, there were significant increases in the incidence of lung adenomas in animals treated with HCS and of all lung tumours in animals treated with both LCS and HCS. There was also a significant increase in the occurrence of nasal cavity tumours in female rats treated with HCS (Mauderly et al., 2004).

3.1.3 Hamster

Four studies have evaluated the ability of mainstream tobacco smoke to induce tumours in hamsters (Table 3.1). Syrian golden hamsters were exposed to either a mixture of German reference cigarette smoke or of dark air-cured cigarette smoke for lifetime. There were increases in the incidence of laryngeal carcinomas in hamsters exposed to both smoke preparations (Dontenwill et al., 1973). In a subsequent study, hamsters were exposed to a mixture of German reference cigarette smoke containing 1.5 mg nicotine, 0.173 mg phenol and 12.7 mL carbon monoxide/cigarette for lifetime. The incidence of laryngeal tumours in smoke-exposed hamsters was higher than in controls (Dontenwill et al., 1977). BIO male hamsters exposed to a mixture of US reference smoke for 100 weeks developed laryngeal and nasopharyngeal tumours (Bernfeld et al., 1974). In a subsequent study, male BIO hamsters exposed to smoke from commercial British filter cigarettes developed higher incidence of laryngeal tumours than controls (Bernfeld et al., 1979).

3.2. Co-administration of tobacco smoke with known carcinogens and other agents

Study design and results of the studies on co-administration of tobacco smoke with known carcinogens and other agents are summarized in Table 3.2.

Table 3.2

Carcinogenicity in response to exposure to mainstream tobacco smoke in conjunction with exposure to known carcinogens or other agents in animals.

3.2.1 Rat

(a) Benzo[a]pyrene

Wistar rats received a single intratracheal instillation of 2 mg benzo[a]pyrene followed by lifetime exposure to cigarette smoke. This treatment led to a low incidence of lung tumours that was not significantly higher than in controls (Davis et al., 1975). In another study Wistar rats were given intratracheal instillations of benzo[a]pyrene mixed with ferric oxide and exposed to cigarette smoke either during initiation and post-initiation or only after treatment with benzo[a]pyrene/ferric oxide (post-initiation). Inhalation of cigarette smoke during the initiation and post-initiation phases of carcinogenesis resulted in a higher lung tumour (squamous-cell carcinoma) multiplicity than that seen in rats exposed during the post-initiation phase only (Gupta et al., 1990).

(b) Radon progeny

Sprague-Dawley rats were exposed to radon progeny at cumulative doses of 4000, 500 or 100 work-level-months (WLM), with or without concurrent exposure to cigarette smoke by inhalation for one year. Rats exposed to 4000 WLM radon progeny, without exposure to smoke, developed lung carcinomas (17/50). Thirty four carcinomas were seen in 50 rats exposed to radon and cigarette smoke. The 500 WLM radon progeny group exposed to radon only had 2/28 lung carcinomas as compared with 8/30 rats exposed to radon and cigarette smoke. No tumours were observed in rats treated with 100 WLM radon and one carcinoma was seen among 30 rats exposed to 100 WLM radon and cigarette smoke. Seventy five percent of the lung tumours were squamous-cell carcinomas, 20% were adenocarcinomas, and the remainder were undifferentiated carcinomas (Chameaud et al., 1982).

(c) Plutonium oxide

CDF®/CrlBR rats were exposed to either filtered air or mainstream cigarette smoke at concentrations of either 100 or 250 mg total particulate matter/m³ (LCS and HCS groups, respectively). At 12 weeks, rats were removed from smoke chambers and exposed nose-only to plutonium oxide (²³⁹PuO₂) then returned to the smoke chambers one week later for 30 months of continuous exposure to either filtered air or cigarette smoke. The incidence and multiplicity of lung tumours (adenocarcinomas, squamous-cell carcinomas, adenosquamous carcinomas) in animals exposed to both concentrations of cigarette smoke and ²³⁹PuO₂ were higher than those in animals exposed to ²³⁹PuO₂, LCS or HCS alone (Finch et al., 1995).

3.2.2. Hamster

(a) 7,12-Dimethylbenz[a]anthracene

Groups of 160 Syrian golden hamsters received 7,12-dimethylbenz[a]anthracene (DMBA) intratracheally, followed by cigarette smoke for life, or treated with cigarette smoke or DMBA only. A total of 32 squamous-cell carcinomas of the larynx were observed in animals treated with both DMBA and cigarette smoke, in comparison with 17 in hamsters exposed to cigarette smoke only and none in hamsters treated with DMBA alone (Dontenwill et al., 1973). Similar results were reported from other experiments in which Syrian golden hamsters were exposed to DMBA and cigarette smoke (Hoffmann et al., 1979).

(b) N-Nitrosodiethylamine

Groups of hamsters received a single subcutaneous injection of N-nitrosodiethylamine (NDEA) and then were exposed to smoke from unfiltered cigarettes, filtered cigarettes and sham smoke. Controls were exposed to either unfiltered cigarette smoke, filtered cigarette smoke or sham smoke. In the NDEA-smoke-treated groups, epithelial hyperplasias and/or papillomas of the larynx were induced at higher frequency than in controls (Takahashi et al., 1992). Hamsters exposed to cigarette smoke in air also received 12 weekly subcutaneous injections of NDEA (total dose, 10 mg/hamster). Treatment with NDEA only resulted in both benign and malignant tumours of the respiratory tract, and co-exposure to cigarette smoke potentiated the development of tumours in the nasal cavity (Harada et al., 1985).

3.3. Smoke condensates

Study design and results of the studies on administration of tobacco smoke condensates are summarized in Table 3.3.

Table 3.3

Carcinogenicity in response to exposure to cigarette-smoke condensate in animals.

3.3.1 Skin application

(a) Mouse

Cigarette-smoke condensate produces both benign and malignant tumours on mouse skin. The carcinogenic potency of the cigarette-smoke condensate depends upon tobacco variety, composition of cigarette paper and the presence of additives (Wynder et al., 1957; Gargus et al., 1976; Gori, 1976).

(b) Rabbit

Cigarette-smoke condensate induced skin papillomas and carcinomas when applied to the ears of rabbits for lifetime (Graham et al., 1957).

3.3.2 Intrapulmonary administration

Injection of 24 mg cigarette-smoke condensate into the lungs of female Osborne Mendel rats led to the development of squamous cell carcinomas (Stanton et al., 1972). These observations were confirmed by Dagle et al. (1978) who observed a dose-dependent incidence of lung carcinomas when cigarette-smoke condensate prepared from two types of cigarettes were given.

3.3.3 Initiation-promotion skin painting studies

Cigarette-smoke condensate and its fractions can act as skin co-carcinogens in Swiss and SENCAR mice when tested in conjunction with croton oil (Hoffmann & Wynder, 1971) or DMBA (Wynder & Hoffmann, 1961; Meckley et al., 2004a, b; Hayes et al., 2007).

3.3.4 Bidi smoke

Swiss albino mice administered 1 mg bidi smoke condensate in dimethyl sulfoxide (DMSO) by oral gavage developed haemangiomas (4/15), stomach carcinoma (1/15), and esophageal carcinoma (1/15), whereas no tumours were observed in controls (Pakhale et al., 1988).

4. Other Relevant Data

4.1. Overview of the mechanistic evidence for the carcinogenicity of tobacco

4.1.1 Conceptual model of the carcinogenesis of tobacco and tobacco smoke

A conceptual model for understanding mechanisms by which tobacco smoke causes cancer is shown in Fig. 4.1 (Hecht, 1999, 2003). This model also applies to smokeless tobacco and other forms of smoked tobacco and, in theory, to second-hand tobacco smoke since it contains all of the same carcinogens and toxicants as mainstream cigarette smoke, although at lower doses.

Fig. 4.1

Conceptual model for understanding mechanisms of tobacco carcinogenesis

The major accepted mechanistic pathway is summarized in the central track of Fig. 4.1. Smokers inhale carcinogens which, either directly or after metabolism, covalently bind to DNA, forming DNA adducts. DNA adducts are central to chemical carcinogenesis because they can cause miscoding and permanent mutations. If these mutations occur in critical regions of oncogenes and tumour suppressor genes, which are essential in growth control, the result can be loss of normal cellular proliferation mechanisms, genomic instability, and cancer. A study that sequenced 623 cancer-related genes in 188 human lung adenocarcinomas validated this premise by finding multiple somatic mutations in critical growth control genes, consistent with the chronic bombardment of cellular DNA by tobacco smoke carcinogens and their metabolically activated forms (Ding et al., 2008).

Each step of this conceptual model is considered in detail below.

Most people begin smoking cigarettes when they are teenagers, and become addicted to nicotine. Nicotine is not generally considered to be a carcinogen (Schuller, 2009), but it is accompanied in each puff of each cigarette by a complex mixture of carcinogens and toxicants. There are over 60 carcinogens in cigarette smoke that have been evaluated in the previous IARC Monograph as having sufficient evidence for carcinogenicity in laboratory animals (IARC, 2004a), sixteen of which are considered to be carcinogenic to humans (Group 1). There are also many other carcinogens and potential carcinogens in cigarette smoke that have not been evaluated (Rodgman & Perfetti, 2006; see Section 1.1). Structures of tobacco smoke constituents and biomarkers discussed here are presented in Fig. 4.2.

Fig. 4.2

Structures of compounds discussed in the text

Numerous studies demonstrate the uptake of tobacco smoke carcinogens and toxicants by smokers, and showed higher levels of their metabolites in urine and blood of smokers than non-smokers (Sections 4.1.1 and 4.1.2). There are substantial differences in carcinogen exposure among people because of the number and types of cigarettes they smoke and the ways in which they smoke them. These differences can be monitored in part by biomarkers of exposure such as urinary metabolites or haemoglobin adducts (Section 4.1.2). Haemoglobin adducts of multiple aromatic amines and volatile carcinogens have been demonstrably related to tobacco (Hatsukami et al., 2006a). There may also be differences in carcinogen exposure due to genetic variations (Section 4.2).

The body’s response to cigarette smoke constituents is similar to its response to pharmaceutical agents and other foreign compounds. Drug metabolizing enzymes, most frequently CYPs, convert these compounds to more water soluble forms, facilitating excretion. During this natural protective attempt, some reactive intermediates are formed. These intermediates are frequently electrophilic (electron seeking, or bearing a partial or full positive charge). Electrophilic intermediates may react with water, generally resulting in detoxification, or may covalently bind to nucleophilic (electron rich) sites in DNA, forming DNA adducts (Guengerich, 2001; Jalas et al., 2005), which are critical in the carcinogenic process (see Section 4.1.3c). CYP1A1 and CYP1B1, repeatedly shown to be inducible by cigarette smoke via interactions of smoke compounds with the aryl hydrocarbon receptor (AhR), are particularly important in the metabolic activation of PAHs, while CYP2A13 is critical for the metabolism of NNK (Nebert et al., 2004; Jalas et al., 2005). The inducibility of certain CYPs may be a critical aspect of cancer susceptibility in smokers (Nebert et al., 2004). CYP1A2, CYP2A6, CYP2E1 and CYP3A4 are also important in the metabolism of cigarette smoke carcinogens to DNA binding intermediates (Jalas et al., 2005), and aldo-keto reductase enzymes, also induced by tobacco smoke (Quinn et al., 2008), are involved in the metabolism of NNK, BaP and other tobacco smoke carcinogens. Competing with this process of “metabolic activation” resulting in DNA binding is the intended metabolic detoxification, which leads to harmless excretion of carcinogen metabolites, and is also catalysed by CYPs and a variety of other enzymes including GSTs, uridine diphosphate-glucuronosyl transferases (UGTs), and arylsulfatases. The relative amounts of carcinogen metabolic activation and detoxification differ among individuals. It is widely hypothesized that this balance will affect cancer risk with those having higher activation and lower detoxification capacity being the most susceptible. This premise is supported in part by molecular epidemiologic studies of polymorphisms, or variants in more than 1% of the population, in certain genes coding for these enzymes (Vineis et al., 2003; Carlsten et al., 2008).

DNA adducts are thought to be a critical lesion in carcinogenesis. Many investigations demonstrate the presence of DNA adducts in human tissues, and some of these are summarized in Section 4.1.2c. There is massive evidence, particularly from studies which use relatively non-specific DNA adduct measurement methods, that DNA adduct levels in the lung and other tissues of smokers are higher than in non-smokers, and some epidemiologic data link these higher adduct levels to increased cancer risk (IARC, 2004b; Veglia et al., 2008). However, there is much more limited evidence from studies using specific carcinogen-derived DNA adducts as biomarkers (Pfeifer et al., 2002). Oxidative DNA damage has also been observed, and this may result partially from exposure to metals in cigarette smoke (Stavrides, 2006).

Cellular DNA repair systems can excise DNA adducts and restore normal DNA structure (Christmann et al., 2003). These complex multiple systems include direct base repair by alkyltransferases, removal of DNA damage by base and nucleotide excision repair, mismatch repair, and double strand repair. If these DNA repair systems are unsuccessful in fixing the damage, then the DNA adducts can persist, increasing the probability of a permanent mutation. There are polymorphisms in genes coding for some DNA repair enzymes. If these variants lead to deficient DNA repair, the probability of cancer development can increase (Vineis et al., 2009).

DNA adducts can cause miscoding during replication when DNA polymerase enzymes misread the DNA adduct and consequently insert the wrong base opposite to it. There is some specificity in the relationship between specific DNA adducts formed from cigarette smoke carcinogens and the types of mutations which they cause. G to T and G to A mutations have often been observed (Section 4.1.3) (Hecht, 1999). Extensive studies have characterized the mutations which occur because of specific carcinogen-DNA adducts (Delaney & Essigmann, 2008). Mutations have been reported in the KRAS oncogene in lung cancer and in the TP53 tumour suppressor gene in a variety of cigarette smoke-induced cancers (Ahrendt et al., 2001; Pfeifer et al., 2002; Ding et al., 2008). The cancer causing role of these genes has been firmly established in animal studies (Lubet et al., 2000; Johnson et al., 2001). A selection and promotion process may also play a role in the final mutation spectrum seen in genes in smoking-associated tumours (Rodin & Rodin, 2005; Sudo et al., 2008).

Urinary mutagenicity, sister chromatid exchanges, micronuclei in buccal cells, and other genetic effects have been consistently observed in smokers at higher levels than in non-smokers (IARC, 2004a; Proia et al., 2006). In addition to mutations, numerous cytogenetic changes are observed in lung cancer, and chromosome damage throughout the field of the aerodigestive tract is strongly associated with cigarette smoke exposure. Mutations resulting from DNA adducts can cause loss of normal cellular growth control functions, via a complex process of signal transduction pathways, ultimately resulting in genomic instability, cellular proliferation and cancer (Ding et al., 2008). Apoptosis, or programmed cell death, is a protective process, and can remove cells which have DNA damage, thus serving as a counterbalance to these mutational events. The balance between apoptotic mechanisms and those suppressing apoptosis will have a major impact on tumour growth.

While the central track of Fig. 4.1 is the major pathway by which tobacco smoke carcinogens cause cancer, other mechanisms also contribute, as indicated in the top and bottom tracks (Hecht, 2003). Nicotine, NNK, and NNN bind to nicotinic and other cellular receptors, resulting in activation of serine/threonine kinase Akt (also known as protein kinase B), protein kinase A, and other changes. Nicotine and NNK increase expression of survivin, an inhibitor of apoptosis in normal human bronchial epithelial cells, and survivin mRNA is detected in bronchial brush samples from heavy smokers (Jin et al., 2008). This can cause decreased apoptosis, increased angiogenesis, and increased transformation (Heeschen et al., 2001; West et al., 2003). Thus, although nicotine is not carcinogenic, it may enhance carcinogenicity in various ways (Schuller, 2009). Cigarette smoke also contains well established oxidants, co-carcinogens, tumour promoting fractions, and inflammatory agents, as well as cilia-toxic compounds such as acrolein, which impede clearance. Many studies demonstrate the co-carcinogenic and cytotoxic effects of catechol, an important constituent of cigarette smoke. An epigenetic pathway frequently observed in tobacco-induced cancers is enzymatic methylation of promoter regions of genes such as p16 and FHIT [fragile histidine triad gene, a gene coding for a dinucleoside 5′, 5′′′- P¹, P³-triphosphate hydrolase, a putative tumour suppressor protein] resulting in gene silencing, which are also strongly implicated in tobacco-induced lung cancer (D’Agostini et al., 2006; Bhutani et al., 2008). When this occurs in tumour suppressor genes, the result can be unregulated proliferation (Belinsky, 2005). Inflammation due to smoking is associated with tumour promotion and activation of factors such as NFκB. Inflammation also plays a role in chronic obstructive pulmonary disease (COPD), which in turn is an independent risk factor for lung cancer (Smith et al., 2006; Turner et al., 2007; Lee et al., 2008a).

This conceptual model can be applied to smokeless tobacco products. Smokeless tobacco products have much lower levels of carcinogens and toxicants that result from combustion, so the effects of these agents are not seen to a significant extent. The most prevalent strong carcinogens in smokeless tobacco are the tobacco-specific nitrosamines; other nitrosamines, PAHs, aldehydes and metals are also present, and there are large amounts of some inorganic salts that may contribute to inflammation (IARC, 2007a; Stepanov et al., 2008). An additional factor in carcinogenesis by betel quid with tobacco is the basic pH resulting from addition of slaked lime to the quid, leading to oxidative damage and inflammation (IARC, 2004b).

Multiple studies demonstrate that tobacco-specific nitrosamines are absorbed and metabolised in smokeless tobacco users (IARC, 2007a).

There is evidence for DNA adduct formation in oral tissues of smokeless tobacco users, and sister chromatid exchanges, chromosomal aberrations, and micronuclei – consequences of DNA adduct formation – have been reported (Proia et al., 2006; Warnakulasuriya & Ralhan, 2007). Many studies have demonstrated RAS and TP53 mutations in smokeless tobacco users (Warnakulasuriya & Ralhan, 2007) consistent with the conceptual framework.

Oxidative stress and reactive oxygen species could play a significant role in cancer induction in smokeless tobacco users, particularly at high pH (Boffetta et al., 2008). Chronic local inflammation and irritation induced by smokeless tobacco and its constituents could have a tumour promoting or co-carcinogenic effect (Boffetta et al., 2008). Upregulation of cyclooxygenase-2, involved in prostaglandin synthesis and inflammation, has been observed in animal studies upon exposure to smokeless tobacco (Boffetta et al., 2008). Smokeless tobacco products have relatively high levels of sodium chloride (NaCl), which could contribute to inflammation, tumour promotion, and co-carcinogenesis. Cancer of the oral cavity is strongly associated with tobacco smoking (IARC, 2004a) or chewing (IARC, 2007a) and alcoholic beverage drinking (IARC, 2010a) However only a fraction of exposed subjects develop tumours, which suggests that other exposures such as HPV may be independently involved or act as cofactors. HPV is known to infect the oral cavity of healthy individuals and several HPV-related lesions have been characterized (IARC, 2007b). Herpes simplex virus has also been shown to enhance the carcinogenicity of smokeless tobacco products in animal studies (Park et al., 1986). These factors may contribute significantly to the local carcinogenic effects characteristic of smokeless tobacco use.

4.1.2 Absorption, distribution, metabolism and excretion

There are examples of toxicant and carcinogen metabolism and excretion for representatives of virtually every major class of compounds; some of these are summarized in Table 4.1. Nicotine and five of its urinary metabolites – cotinine, 3′-hydroxycotinine and their glucuronides, and nicotine glucuronide – comprise about 73–96% of the nicotine dose (Hukkanen et al., 2005), and are found in blood, sweat, hair and toenails (Al Delaimy, 2002; Hukkanen et al., 2005; Stepanov et al., 2007; Al Delaimy & Willett, 2008). Metabolites of various polycyclic aromatic hydrocarbons including pyrene, phenanthrene, fluorene, and benzo[a]pyrene have been quantified in human urine and are higher in smokers than in non-smokers (Hecht, 2002; Hecht et al., 2005a; Jacob et al., 2007; Hansen et al., 2008). Metabolites of tobacco-specific nitrosamines – NNAL and its glucuronides (total NNAL) from NNK; and NNN and its glucuronides (total NNN) from NNN – are present in human urine (Hecht, 2002; Stepanov & Hecht, 2005; Hecht et al., 2008a; Stepanov et al., 2008). Total NNAL has also been quantified in blood and toenails (Hecht et al., 2002; Stepanov et al., 2007). Aromatic amine-haemoglobin adducts have been frequently measured in human blood, and their levels increase with smoking (Hecht, 2002; Hatsukami et al., 2006a). Mercapturic acids of several tobacco smoke compounds such as benzene, 1,3-butadiene, acrolein, and ethylene oxide are present in human urine and are related to smoking (Carmella et al., 2009). Haemoglobin adducts of acrylonitrile and related compounds are elevated in smokers’ blood, and levels of metals such as Cd are increased in smokers’ urine (Carmella et al., 2002; IARC, 2004b).

Table 4.1

Examples of toxicant or carcinogen metabolites in tobacco users.

All of the metabolites listed in Table 4.1 are elevated in cigarette smokers; in studies of second-hand smoke exposure, only nicotine metabolites and urinary total NNAL are consistently increased in exposed versus non-exposed subjects, although one very large study also observed an increase in PAH metabolites (Pirkle et al., 2006; Hecht, 2008; Suwan-ampai et al., 2009). Smokeless tobacco users have significantly raised levels of nicotine metabolites and tobacco-specific nitrosamine metabolites compared to non-tobacco users (Hecht et al., 2007).

4.1.3 Biomarkers

Tobacco carcinogen biomarkers are quantifiable entities that can be specifically related to tobacco carcinogens. Specificity to a given carcinogen is critical because tobacco carcinogens vary widely in their potency and target organs.

Considering the mechanistic framework outlined in Fig. 4.1, one could visualize various types of biomarkers. Currently, biomarkers of carcinogen/toxicant dose, reflecting the second box of the central track of Fig. 4.1, are by far the most extensively used and validated. The second most common are measurements of DNA adducts (or protein adducts as their surrogates), but fewer of these have both practical utility and validation with respect to tobacco carcinogen specificity.

The use of tobacco carcinogen biomarkers bypasses many uncertainties in estimation of dose. The most commonly used estimation of dose is self-reported number of cigarettes/day, but this is not a very good marker. It may not be reported accurately and it provides no information on the way in which the cigarettes were smoked, which is critical when one considers the common phenomenon of smoker’s compensation. Brand information together with machine smoking measurements of specific components is another way of obtaining a measure of dose. However, machine smoking measurements are known to have limitations and the application of a given machine smoking protocol to a given smoker requires smoking topography measurements for that smoker. A disadvantage of tobacco carcinogen biomarkers is that they are affected to some extent by individual differences in metabolism, which may complicate interpretation of dose.

(a) Urinary biomarkers

Probably the most practical and, to date, the most extensively applied tobacco carcinogen biomarkers are urinary metabolites of tobacco carcinogens, and these have been comprehensively reviewed (Hecht, 2002; IARC, 2004a). Advantages include the ready availability of samples, and concentrations in urine that are easily quantifiable using modern analytical chemistry methods, most frequently liquid chromatography-tandem mass spectrometry (LC-MS/MS). The urinary metabolites listed in Table 4.1 have all been used as biomarkers and all are validated with respect to exposure in cigarette smokers (Carmella et al., 2009). Total nicotine equivalents (the sum of nicotine and the five metabolites in Table 4.1) is a particularly effective way of estimating nicotine dose from tobacco products.

Total NNAL, the sum of NNAL and its glucuronides, is a highly useful biomarker of NNK exposure (Hecht, 2002, 2003; Hatsukami et al., 2006a). The tobacco-specificity of NNK, and therefore total NNAL, is a key feature of this biomarker because studies in which it is applied are not confounded by other environmental or dietary exposures. It also has a considerably longer half-life than cotinine and several other urinary biomarkers. Total NNAL has been used in numerous studies that estimated uptake of NNK in smokers under varying circumstances. In one example, smokers reduced their number of cigarettes smoked per day, but there was not a corresponding decrease in NNK uptake due to compensation (Hecht et al., 2004). In another study, NNK and PAH uptake, estimated by total NNAL and 1-hydroxypyrene, respectively, were compared in smokers of regular, light, and ultra-light cigarettes, and found to be similar, consistent with epidemiologic studies that demonstrate no protection against lung cancer in smokers of light compared to regular cigarettes (Hecht et al., 2005b). Other studies evaluated NNK uptake in smokers who switched from their current cigarette brand to products advertised as being less hazardous, but the results generally did not support these claims (Hatsukami et al., 2004). One of the most useful applications of total NNAL has been in studies of non-smokers exposed to second-hand tobacco smoke (Hecht, 2003). The sensitivity and specificity of this biomarker are ideal for such studies, and it is the most commonly elevated tobacco carcinogen biomarker in non-smokers exposed to second-hand smoke. Total NNAL has also found utility in establishing NNK uptake in smokeless tobacco users (Hecht et al., 2002, 2007, 2008a, b; Hecht, 2008)

The relationship of urinary total NNAL to lung cancer was demonstrated in a study of stored urine samples collected years before diagnosis of lung cancer from smokers in Shanghai, China and Singapore (Yuan et al., 2009). There was a significant relationship between total NNAL and lung cancer incidence, after correction for numbers of cigarettes smoked per day and duration of smoking. An 8.5 fold increased risk for lung cancer was observed for those smokers in the highest tertile of total NNAL and cotinine, relative to smokers with the same smoking history but in the lowest tertiles of total NNAL and cotinine. Urinary biomarkers were also used to demonstrate higher uptake of nicotine and NNK per cigarette in smokers with polymorphisms in the nicotinic acetylcholine genes associated with lung cancer in genome-wide association studies (see Section 4.2; Le Marchand et al., 2008). Collectively, these results indicate that urinary total NNAL is not only a biomarker of exposure, but also a biomarker of risk for lung cancer.

(b) Serum and saliva metabolites

Serum and saliva metabolites have been used as biomarkers much less often than urine metabolites. The most frequently measured tobacco smoke toxicant in serum and saliva is cotinine, documented as a useful biomarker of cigarette smoking in many studies (Lee, 1999; Hukkanen et al., 2005). Total NNAL can be readily quantified in serum and its levels remain relatively constant in a given smoker sampled at bimonthly intervals over a one year period. Consistent with the results described above, one study showed a significant relationship between total NNAL in prospectively collected serum samples from smokers and lung cancer risk (Church et al., 2009). Other biomarkers that have been measured in serum include cadmium, benzene, styrene and r-1,t-2,3,c-4-tetrahydroxy-1,2,3,4-tetrahydrophenanthrene (PheT) (IARC, 2004a; Church et al., 2009).

(c) DNA adducts

Fig. 4.3 presents an overview of metabolism and DNA adduct formation from eight tobacco smoke compounds (clockwise from top left): BaP, NNK, N-nitrosodimethylamine (NDMA), NNN, acrolein, ethylene oxide, acetaldehyde and 4-aminobiphenyl. Evidence exists for DNA adduct formation from each of these carcinogens in smokers, based on studies carried out with tissues or blood cells. DNA adduct biomarkers have been applied mainly in studies of smokers, and there is far less evidence from studies of second-hand tobacco smoke or smokeless tobacco use.

Fig. 4.3

Overview of metabolism and DNA adduct formation from eight tobacco smoke constituents

The structures of DNA adducts of tobacco smoke carcinogens have been characterized in detail, but a complete description of these structures is beyond the scope of this section. Selected DNA adduct structures are shown in Fig. 4.4. A major DNA adduct of BaP results from trans- addition of the benzo[a]pyrene diol epoxide (BPDE) to the N²-position of dG (Szeliga & Dipple, 1998). Pyridyloxobutyl (POB)-DNA adducts of NNK and NNN are formed at the 7- and O⁶-positions of deoxyguanosine dG, the O²-position of thymidine, and the O²-position of deoxycytidine (Hecht, 2008). They can be measured in part as 4-hydroxy-1-(3-pyridyl)-1-butanone (HPB) released upon hydrolysis. Metabolic activation of NNK also leads to 7-methyl-dG and O⁶-methyl-dG, identical to the DNA adducts formed from NDMA and other DNA methylating agents (Hecht, 2008). Ethylating agents and ethylene oxide in cigarette smoke also alkylate dG (Zhao et al., 1999; Singh et al., 2005). Acrolein and crotonaldehyde react with DNA to produce exocyclic 1,N²-dG adducts, while acetaldehyde forms a Schiff base adduct with the exocyclic N² amino group of dG. There is evidence for the presence of all these DNA adducts in tissues or blood cells of smokers, but there are also many studies in which these specific adducts have been sought but not found (Boysen & Hecht, 2003).

Fig. 4.4

Structures of some DNA adducts of tobacco smoke constituents

Measurement of these DNA adducts as biomarkers potentially can provide the most direct link between cellular exposure and cancer, because DNA adducts are so critical in carcinogenesis. However, it is challenging because their levels are extremely low, frequently ranging from 1 per 10⁶ to 1 per 10⁸ normal bases, and the tissue or blood samples containing them are usually available in only small quantities. Fortunately, the routine detection of amol levels [attomole, equivalent to 10 moles] of DNA adducts by conventional LC-MS/MS techniques is now feasible (Singh & Farmer, 2006). There are still relatively few examples of quantitation of specific DNA adducts of tobacco carcinogens in tissues of smokers using mass spectrometry, high pressure liquid chromatography (HPLC)-fluorescence, HPLC with electrochemical detection, or postlabelling techniques (Pfeifer et al., 2002). A much larger body of work has used the highly sensitive, but relatively non-specific ³²P-postlabelling and immunoassay methods of DNA adduct detection. Although the adducts detected using ³²P-postlabelling are often referred to as “aromatic DNA adducts,” there is strong evidence that they are not related to PAHs (Arif et al., 2006). Adduct levels are generally higher in lung tissues of smokers than non-smokers while studies using blood DNA have produced varied results. Adducts have also been detected in the larynx, oral and nasal mucosa, bladder, cervix, breast, pancreas, stomach, placenta, foetal tissue, cardiovascular tissues, sputum, and sperm of smokers (IARC, 2004a). A meta-analysis of the relationship of DNA adduct levels in smokers to cancer, as determined by ³²P-postlabelling in the majority of studies or enzyme linked immunosorbent assay (ELISA), demonstrated a positive relationship in current smokers (Veglia et al., 2003; 2008).

(d) Protein adducts

Carcinogen-haemoglobin (Hb) and serum albumin adducts are regarded as surrogates for DNA adduct measurements. Although these proteins are not targets for carcinogenesis, virtually all carcinogens that react with DNA will also react with protein. Advantages of haemoglobin adducts include the ready availability of haemoglobin from blood and the relatively long lifetime of the erythrocyte in humans – 120 days –,which provides an opportunity for adducts to accumulate. Studies on protein adducts in smokers have been comprehensively reviewed (IARC, 2004a).

Haemoglobin adducts of aromatic amines are a highly informative type of carcinogen biomarker, with levels that are consistently higher in smokers than non-smokers, particularly for 3-aminobiphenyl and 4-aminobiphenyl-Hb adducts. Haemoglobin binds aromatic amines efficiently because heme accelerates the rate of nitrosoarene formation from the hydroxylamine, which is produced metabolically from the aromatic amine by CYP1A2 (Fig. 4.3; Skipper & Tannenbaum, 1990). Binding of the nitrosoarene occurs at the β-93 cysteine residue of human haemoglobin; the adduct is hydrolysed releasing the free amine, which is quantified by GC-MS (Skipper & Tannenbaum, 1990). Adduct levels are clearly related to cigarette smoking (Skipper & Tannenbaum, 1990). Adducts that form at the terminal valine of haemoglobin are also useful biomarkers: examples include those derived from ethylene oxide, acrylonitrile and acrylamide (Bergmark, 1997; Fennell et al., 2000). Ethylated N-terminal valine of haemoglobin is also higher in smokers than in non-smokers (Carmella et al., 2002).

HPB-releasing Hb adducts of NNK and NNN have been quantified in studies of smokers and smokeless tobacco users (IARC, 2004a, 2007a). These adducts are thought to be tobacco-specific, but some studies report their presence in non-smokers (Falter et al., 1994; Schlöbe et al., 2008).

4.1.4 Genetic and related effects

(a) Mutagenicity and cytogenetic effects

Tobacco smoke and its condensates are mutagenic in a wide variety of test systems from bacteria to mammalian cells in culture to rodents and humans (DeMarini, 2004; IARC, 2004a; Husgafvel-Pursiainen, 2004). In bacterial systems, the heterocyclic amines and aromatic amines in condensates account for much of the frameshift mutagenicity, whereas the PAHs and nitrosamines may account for some of the base-substitution mutagenicity (DeMarini et al., 1995). G to T is the predominant class of base-substitution mutation induced by condensates in experimental systems and found in oncogenes and tumour-suppressor genes in smoking-associated lung tumours (IARC, 2004a). The genotoxic potencies of a variety of condensates in several genotoxicity assays likely have only qualitative value with regard to health risk assessment (DeMarini et al., 2008). This is consistent with findings that smokers of low- or high-tar cigarettes have similar urinary levels of lung carcinogens (Hecht et al., 2005b; Hatsukami et al., 2006b) and similar risks for lung cancer (Harris et al., 2004).

In rodents, cigarette smoke induces sister chromatid exchange and micronuclei in bone marrow and lung cells. Human newborns of smoking mothers have increased frequencies of HPRT mutations, chromosomal translocations, and DNA strand breaks. Sperm of smokers has increased frequencies of aneuploidy, DNA adducts, strand breaks, and oxidative damage. Cigarette smoke also causes germ-cell mutations in mice (Yauk et al., 2007). Collectively, these data suggest that smoking is likely a germ-cell mutagen in humans. Smoking produces mutagenic urine and somatic-cell mutations in humans, including HPRT mutations, sister chromatid exchange, microsatellite instability and DNA damage in a variety of tissues. Genotoxic effects have been found in eight organ sites at which tobacco smoke causes cancer in humans (DeMarini, 2004; IARC, 2004a).

(b) Mutations in TP53, KRAS and related genes

Gene mutation data from a variety of databases, including the IARC Cancer TP53 Mutation Database (http://www-p53.iarc.fr/), have been collated in the Genetic Alterations in Cancer (GAC) database (http://dir-apps.niehs.nih.gov/gac/) so that mutations in a variety of genes in various cancerous tissues can be compared. An assessment of the Gene Alterations in Cancer database showed that at least three genes were mutated more frequently in lung tumours from smokers than non-smokers (Lea et al., 2007): TP53 (39 versus 26%), K-RAS (20 versus 3%), and loss of heterozygosity at FHIT (57 versus 27%). Thus, genes in the cell cycle (TP53), cell signalling (KRAS) and apoptotic (FHIT) pathways are mutated more frequently in smoking- rather than in nonsmoking-associated lung tumours. Genomic sequencing of lung tumours has identified other mutated genes that are associated with smoking; ten times more genes are mutated in lung tumours from smokers compared to non-smokers (Ding et al., 2008).

GC to TA transversions were the predominant class of base-substitution mutation found in TP53 and KRAS genes in lung tumours from smokers, with the frequency of this mutation in TP53 being 30% in smokers versus 22% in non-smokers. In smoking-associated oral cancers, the percentage of GC to TA mutations in TP53 was 15% versus 2%, respectively. This mutation spectrum is consistent with that produced by a variety of known carcinogens present in tobacco smoke (IARC, 2004a). At the codon level, the most frequently mutated codons in TP53 in lung tumours of smokers were 157, 175, 245, 248, and 273, all of which occur in the DNA-binding domain of the protein; among these codons, only 273 was mutated in lung tumours from non-smokers. Only three of these codons (157, 245 and 273) were mutated in smoking-associated larynx tumours, and only codon 157 was mutated in smoking-associated oral tumours. Thus, the mutational specificity at TP53 is different among smoking- and nonsmoking-associated tumours and among smoking-associated tumours at various organs (Lea et al., 2007). Thus, different pathways are involved in the development of different types of tumours (Le Calvez et al., 2005; Mounawar et al., 2007; Subramanian & Govindan, 2008).

4.1.5 Effects on gene expression profile

As indicated in a review by Sen et al. (2007) involving microarray analysis of 18 studies in human smokers, 7 in smoke-exposed rodents, and 3 in condensate-exposed mammalian cells, smoking generally upregulated a wide variety of genes, especially those involved in the stress response, phase I metabolism, and immune response. Genes that were consistently expressed differentially in smokers (as assessed in alveolar macrophages, lung cells or peripheral lymphocytes) included metallothioneins, heat-shock proteins, superoxide dismutase, glutathione transferase, heme oxygenase, CYP genes (1A2, 1A1 and 1B1), interleukins and chemokines.

Spira et al. (2004) analysed global gene expression in bronchial epithelial cells and found that the expression levels of metabolizing and antioxidant genes had reverted to control levels after two years of smoking cessation. However, expression of potential oncogenes and tumour-suppressor genes never reverted to never-smoker levels even after years of smoking cessation. Consistently, expression of microRNAs is generally downregulated by cigarette smoke (Izzotti et al., 2009). As discussed below, smoking also altered methylation patterns and gene expression in smoking-associated tumours.

4.1.6 Other effects associated with carcinogenesis

(a) Proliferation, differentiation, apoptosis, and inflammation

As noted above, the signal-transduction pathways in lung tumours from smokers are distinctly different from those of non-smokers (Mountzios et al., 2008). Fig 4.5 shows details of signalling pathways that are deregulated by tobacco smoke. The involvement of high frequencies of mutated K-RAS and TP53 genes in smoking-associated lung tumours results in altered regulation of cell proliferation, differentiation, cytoskeletal organization and protein trafficking. Cigarette smoking activates NF-κB, which induces pro-inflammatory cytokine expression and induces growth factors and proliferative signals (Mountzios et al., 2008). This gene also influences the expression of the anti-apoptotic gene BCL2 and pro-apoptotic gene BAX. Smoking produces chronic inflammation, which promotes cancer (Walser et al., 2008). Smoking results in high levels of reactive oxygen species, which damage epithelial and endothelial cells and impair their function. In smoking-associated lung cancer, elevated levels of cyclooxygenase-2 (COX-2) and prostaglandin (PGE₂) indicate apoptosis resistance, proliferation, immunosuppression, angiogenesis, invasion, and epithelial-mesenchymal transition (Walser et al., 2008).

Fig. 4.5

General scheme of some cell-signalling pathways that are deregulated by tobacco smoke in lung carcinogenesis

(b) Endogenous nitrosation

Intragastric formation of N-nitroso compounds, measured using urinary nitrosamino acids excreted in urine, was increased in smokers compared to non-smokers (Hoffmann & Brunnemann, 1983). Two recent studies demonstrated that NNN forms endogenously in some users of nicotine replacement therapy products (Stepanov et al., 2009a, b).

(c) Hormonal changes

These are described in Section 4.3.2a.

5. Evaluation

There is sufficient evidence in humans for the carcinogenicity of tobacco smoking.

Tobacco smoking causes cancers of the lung, oral cavity, naso-, oro- and hypopharynx, nasal cavity and accesory sinuses, larynx, oesophagus, stomach, pancreas, colorectum, liver, kidney (body and pelvis), ureter, urinary bladder, uterine cervix and ovary (mucinous), and myeloid leukaemia. Also, a positive association has been observed between tobacco smoking and cancer of the female breast. For cancers of the endometrium (post-menopausal) and of the thyroid, there is evidence suggesting lack of carcinogenicity.

There is sufficient evidence in humans for the carcinogenicity of parental smoking. Parental smoking causes hepatoblastoma in children. Also, a positive association has been observed between parental smoking and childhood leukaemia (particularly acute lymphocytic leukaemia).

There is sufficient evidence in experimental animals for the carcinogenicity of tobacco smoke and of tobacco smoke condensates.

Tobacco smoking is carcinogenic to humans (Group 1).

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