INTRODUCTION — Lung cancer is the most common cancer worldwide, with an estimated 1,600,000 new cases and 1,380,000 deaths in 2008 [1]. In the United States, there will be an estimated 226,000 new cases of lung cancer and 160,000 deaths in 2012 [2]. Lung cancer stands out from most other cancers because of our recognition of the major modifiable risk factor leading to the disease — exposure to tobacco smoke. (See "Patterns of tobacco use".)
Not all lung cancer is smoking related, however. Other risk factors include exposure to asbestos, haloethers, polycyclic aromatic hydrocarbons, nickel, and arsenic. Interest has also focused on the potential roles of exposure to environmental tobacco smoke (ie, passive exposure to "second-hand" smoke) and to radon. Potential risk factors include dietary factors, genetic factors, and the presence of underlying benign forms of parenchymal lung disease, including chronic obstructive lung disease and pulmonary fibrosis. (See "Lung cancer in never smokers".)
The major risk factors for lung cancer will be reviewed here. Issues specific to lung cancer risk in women or HIV-infected patients are discussed separately. (See "Women and lung cancer" and "Overview of non-AIDS-defining malignancies in HIV infection", section on 'Lung cancer'.)
SMOKING — Smoking prevalence fell among both men and women from 1975 to 2006 [3]. This was accompanied by both a decline in the death rate for lung cancer among men and a leveling off of the death rate for lung cancer among women. Bronchogenic carcinoma is undoubtedly the most preventable of the common forms of cancer because of the indisputable link between cigarette smoking and risk of lung cancer.
Cigarettes — The possibility that inhalation of cigarette smoke might be a common cause of lung cancer was first suggested by Adler in 1912 [4]. However, it was also noted at the time that a "nearly complete consensus of opinion" existed "that primary malignant neoplasms of the lungs are among the rarest forms of the disease." In 1920, lung cancer comprised only 1 percent of all malignancies in the US.
The first scientific report associating cigarette smoking with an increased risk of premature death appeared in 1938 [5]. It was not until 1950, however, that Doll and Hill clearly demonstrated an epidemiologic association between cigarette smoking and lung cancer mortality [6-8]; this observation was confirmed shortly thereafter by Wynder and Graham [9].
Evidence — The evidence linking cigarette smoking to human lung cancer has included a large volume of both prospective and retrospective epidemiologic research. Well-established criteria, based upon observational evidence, have been described for the attribution of causality to the association between disease and a disease-associated variable. These include [10]:
Based upon application of these criteria to an enormous body of observational data, the Surgeon General of the United States definitively concluded in 1964 "cigarette smoking is the major cause of lung cancer" [11]. This message was again emphasized 40 years later in a 2004 update on the health effects of cigarette smoking [12].
Until recently, the evidence linking cigarette smoking to lung cancer has been primarily indirect. However, a direct link between tobacco and lung cancer was established, based upon the finding that a specific metabolite of benzo(a)pyrene, a chemical constituent of tobacco smoke, damages three specific loci on the p53 tumor-suppressor gene that are known to be abnormal in approximately 60 percent of cases of primary lung cancer [13]. Related polycyclic aromatic hydrocarbons found in smoke appear capable of targeting other lung cancer mutational hotspots [14]. (See "Molecular markers in non-small cell lung cancer".)
Magnitude — Estimates of the relative risk of lung cancer in the long-term smoker compared with the lifetime nonsmoker vary from 10- to 30-fold. The cumulative lung cancer risk among heavy smokers may be as high as 30 percent, compared with a lifetime risk of lung cancer of 1 percent or less in nonsmokers [15,16].
The risk of bronchogenic carcinoma is proportional to the total lifetime consumption of cigarettes. The relative risk increases with both the number of cigarettes smoked per day as well as the lifetime duration of smoking. It has been estimated that a 35 year-old man has a 9 percent likelihood of dying from lung cancer before age 85 if he smokes fewer than 25 cigarettes per day, compared with an 18 percent likelihood if he smokes more than 25 cigarettes per day [17].
Additional factors include [18-20]:
The age at which an increased risk of lung cancer becomes apparent among smokers is the middle to late forties. Beyond that point, the age-specific relative risk for the development of lung cancer rises steadily in smokers until it peaks at an age in the late seventies [21].
Smoking cessation — Smoking cessation clearly decreases the risk of lung cancer among former smokers compared with current smokers [15,22,23]. Large cohort and case-control studies have attempted to quantify the magnitude of the reduction in risk of lung cancer following cessation of smoking [22]:
Smoking cessation may be beneficial even among patients who have been diagnosed with early or limited-stage lung cancer. In a systematic review with meta-analyses, ongoing smoking by patients with early or limited-stage lung cancer was associated with increased likelihood of all-cause mortality, tumor recurrence, and development of a second primary tumor [26].
Smoking reduction — In smokers who are unable to quit, reducing smoking appears to have some affect on reducing lung cancer risk. An observational study from Denmark that included 19,714 adults found that after a mean follow-up of 18 years, heavy smokers (≥15 cigarettes or an equivalent amount of tobacco in another form per day) who continued to smoke but cut back by at least 50 percent reduced their risk of lung cancer by 27 percent (95% CI 2-46%) (table 1) [27].
Thus, encouraging smokers who are unable to quit to decrease their smoking may result in harm reduction, including a decreased risk of lung cancer.
Race — There are ethnic and racial differences in the smoking-related risk of lung cancer. This was illustrated by an observational cohort study that followed 183,813 subjects for eight years [28]. Lung cancer was identified in 1979 subjects (1 percent). African Americans and Native Hawaiians were most susceptible to lung cancer when fewer than 30 cigarettes per day were smoked; there was no difference among the ethnic groups when smoking exceeded 30 cigarettes per day.
Beta-carotene supplementation — Beta-carotene has been studied as a chemopreventive agent, based upon preclinical and epidemiologic data. However, multiple chemoprevention trials have failed to demonstrate any benefit from beta-carotene supplements and have suggested that this approach may be associated with an increased incidence of lung cancer. (See "Chemoprevention of lung cancer", section on 'Primary chemoprevention'.)
A meta-analysis of chemoprevention trials found that high-dose beta-carotene supplementation significantly increased the incidence of lung cancer in smokers (odds ratio [OR] 1.24, 95% CI 1.10-1.39) [29]. Among former smokers, the difference was not statistically significant (OR 1.10, 95% CI 0.84-1.85). The high doses of beta-carotene used in these trials may be also be found in multivitamin formulations used to promote visual health.
Second hand smoke — The intensity of exposure to environmental tobacco smoke (ie, passive or "second-hand" exposure) is far less than that which occurs with active smoking. On the other hand, exposure to environmental tobacco smoke usually begins much earlier in life than it does with active smoking, and the duration of exposure to carcinogens occurs over a longer period of time. (See "Secondhand smoke exposure: Effects in adults".)
Epidemiologic studies have now shown that nonsmokers exposed to high levels of environmental tobacco smoke demonstrate an increased risk of lung cancer compared to individuals with lower cumulative exposures [30-32]. (See "Lung cancer in never smokers".)
There is also a dose-response relationship between intensity of exposure and relative risk:
The risk for the development of lung cancer in response to environmental tobacco smoke may be influenced by genetics. One study found a significant increase in polymorphisms in the gene glutathione S-transferase M1 among 51 nonsmoking women with exposure to environmental tobacco smoke who developed lung cancer compared with 55 nonsmoking women with lung cancer who had no environmental tobacco smoke exposure [35]. Glutathione S-transferase M1 is believed to play a role in detoxifying carcinogens in tobacco smoke; thus, mutations that decrease its activity could serve to promote tumorigenesis.
Cigars — Cigar smoking is associated with an increased risk of lung cancer; however, the risk appears weaker than with cigarettes [36-40]. This is best illustrated by the following studies:
The amount of cigar smoke to which the lungs of cigar smokers are exposed varies widely (according to carboxyhemoglobin levels). This probably reflects differences in the number of cigars smoked, the depth of inhalation, and the degree to which each cigar is smoked to completion [41]. For these reasons, a threshold at which cigar smoking begins to increase the risk of lung cancer has not been defined.
Pipes — Pipe smoking increases the risk of lung cancer [37-39,42]. The increased risk of lung cancer due to pipe smoking is similar to cigar smoking, but less than cigarette smoking [42].
This is best illustrated by an observational cohort study that followed 138,307 men (15,263 pipe-only smokers and 123,044 nonsmokers) for 18 years [42]. Current pipe smoking was associated with an increased risk of death from lung cancer (relative risk 5.0, 95% CI 4.2-6.0). The risk of lung cancer correlated with the number of pipes smoked per day, years of smoking, and depth of inhalation. Conversely, the risk of lung cancer decreased after smoking cessation.
Marijuana — The carcinogenicity of marijuana smoking is less studied than that of tobacco smoking. Several reports have documented histologic and molecular changes in the bronchial epithelium of marijuana smokers that are similar to the metaplastic premalignant alterations that are seen among tobacco smokers [43-45]. However, an association between marijuana smoking and lung cancer has been difficult to prove because studies were limited by selection bias, small sample size, and failure to adjust for tobacco smoking [45,46]. In addition, the duration from the onset of marijuana smoking to outcome (ie, lung cancer) measurement may have been insufficient for lung cancer to develop because young participants were enrolled in most studies. (See "Pulmonary complications of cocaine abuse".)
Users of these drugs are probably at increased risk for lung cancer, although the magnitude of risk has not been well quantified [47,48]. The absolute risk of lung cancer that a given individual accrues likely relates to the magnitude and duration of drug use, the amount of adulterants coingested, and whether exposure to concomitant carcinogens (such as tobacco smoke) is present. In a case-control study, the risk of lung cancer increased 8 percent for each joint-year of marijuana smoking after adjusting for cigarette smoking [49]. In comparison, the risk of lung cancer increased 7 percent for each pack-year of cigarette smoking after adjusting for marijuana smoking.
Cocaine — The carcinogenicity of cocaine smoking is less studied than that of tobacco smoking. There is some evidence that cocaine smokers have histologic and molecular changes in the bronchial epithelium that are similar to the metaplastic premalignant alterations seen among tobacco smokers [43]. However, additional research is required further define any relationship between cocaine smoking and lung cancer.
OCCUPATIONAL AND ENVIRONMENTAL CARCINOGENS — Numerous occupational and environmental carcinogens increase the risk of lung cancer. The best known factors are asbestos and radon; other exposures include arsenic, bis-chloromethyl ether, chromium, formaldehyde, ionizing radiation, nickel, polycyclic aromatic hydrocarbons, hard metal dust, and vinyl chloride [50-59]. Many of these factors act synergistically with tobacco smoke to produce lung cancer, and are also independent risk factors in nonsmokers. (See "Second malignancies after treatment of classical Hodgkin lymphoma", section on 'Lung cancer' and "Complications of breast and chest wall irradiation for early stage breast cancer", section on 'Secondary malignancies'.)
As an example, one study of cancer mortality between 1950 and 1997 in Chile found a risk ratio for lung cancer mortality of between three and four in a region with high concentrations of inorganic arsenic in the drinking water [56]. This finding could not be explained by patterns of tobacco use. Further support for a link between arsenic exposure and lung cancer comes from a Taiwanese study demonstrating a progressive decrease in the mortality rate from lung cancer after elimination of arsenic from a community's water supply [50]. (See "Arsenic exposure and poisoning", section on 'Chronic toxicity'.)
Asbestos — Asbestos exposure is a risk factor for lung cancer to which there can be occupational or nonoccupational exposure.
Occupational — Although some investigators have questioned the causal relationship between occupational asbestos exposure and bronchogenic carcinoma [60], most studies have demonstrated a clear association between the two entities. As an example, a Dutch cohort study of 58,279 men, in which 524 cases of lung cancer developed, found that asbestos exposure was associated with a relative risk of lung cancer of 3.5 (95% CI 1.7-7.2) after adjustment for age, smoking habits, and intake of vitamin C, beta-carotene, and retinol [61]. The risk of lung cancer associated with asbestos exposure is dose-dependent but varies according to the type of asbestos fiber. In particular, for a given level of exposure, the risk appears to be considerably higher for workers exposed to amphibole fibers than for those exposed to chrysotile fibers [62].
The increased risk of lung cancer associated with asbestos is greatly magnified by coexisting exposure to tobacco smoke. In one report, for example, the risk of dying of lung cancer in asbestos workers increased 16-fold if they smoked more than 20 cigarettes per day and 9-fold if they smoked fewer than 20 cigarettes per day, compared to asbestos workers without a regular smoking history [63]. (See "Asbestosis".)
The risk of lung cancer associated with combined exposure to asbestos and cigarette smoke appears to be multiplicative. In the same report noted above [63]:
For any given individual, the relative risk depends upon the magnitude of the exposure both to cigarette smoke and to asbestos. Workers with asbestosis are at greater risk, although it is unclear if this is because asbestosis is a marker for heavier exposure or if the inflammatory process is important per se in triggering or promoting carcinogenesis [64].
Nonoccupational — The degree to which low level, nonoccupational asbestos exposure increases the risk of lung cancer is less well defined. However, the potential risk is of great public health concern because of the large number of individuals who work or attend school in buildings that contain asbestos, and the cost and potential hazards of asbestos removal. The United States Environmental Protection Agency (EPA) standards for low-level asbestos exposure are based upon linear extrapolation of data from occupational settings to nonoccupational airborne concentrations that are approximately 100,000-fold less [65]. (See "Asbestosis".)
One population study of women who resided in chrysotile mining towns in Quebec found that differences in estimated cumulative lifetime environmental asbestos exposure did not produce significant differences in the incidence of lung cancer [65]. The authors speculated that the EPA model may overestimate the dose-response relationship between low level environmental asbestos exposure and lung cancer, although the study's negative findings might also relate to its potential overestimation of asbestos exposure, the fact that the mined asbestos was predominantly chrysotile, or because mined asbestos particles are larger and less respirable than refined asbestos [66]. However, an Italian study also failed to detect an increased risk of lung cancer among persons who resided near an asbestos cement factory in which refined asbestos was used [67].
Radon — There has been considerable public concern in recent years about the possible risk of lung cancer in the general population associated with exposure to radon. Radon is a gaseous decay product of uranium-238 and radium-226, which is capable of damaging respiratory epithelium via the emission of alpha particles. Underground uranium miners who were occupationally exposed to radon and its decay products have an increased risk of lung cancer [68], and there is an interactive effect between radon exposure and cigarette smoking [69,70].
Radon is present in soil, rock, and groundwater, and it can accumulate in homes. However, the risk associated with exposure to radon in the home remains uncertain in the face of conflicting data. A 2005 meta-analysis of 13 European case-control studies reported a linear relationship between the amount of radon detected in the home and the risk of developing lung cancer [71]. The increased risk was small but statistically significant, and the authors estimate that radon exposure could be responsible for up to 2 percent of lung cancer deaths in Europe [71].
Wood smoke exposure — Wood is burned, either for cooking or heating, in many areas around the world. Multiple studies have shown that exposure to smoke derived wood burning is associated with an increased risk of lung cancer [72-75].
A study of 150 consecutive unselected Mexican patients with histologically proven NSCLC analyzed the response to erlotinib [72]. Multivariate analysis found exposure to wood smoke was as important a factor in predicting response as adenocarcinoma histology and female gender, suggesting that the pathogenesis may involve different pathways than those involved in tobacco-induced lung cancer. (See "Small molecule epidermal growth factor receptor inhibitors for advanced non-small cell lung cancer", section on 'Predictors of responsiveness'.)
GENETIC FACTORS — The role of genetic factors as a cause of lung cancer is only poorly understood, but increasing evidence suggests that such factors play a role.
Familial risk — A number of studies suggest that first-degree relatives of individuals with lung cancer have an increased risk of developing lung cancer [76-79]. In most studies, this excess risk of lung cancer in close relatives persists after adjustment for age, gender, and smoking habits. A meta-analysis of 28 case-control studies and 17 observational cohort studies revealed an increased lung cancer risk associated with having an affected relative (relative risk 1.8, 95% CI 1.6-2.0) [76]. The risk was greatest in relatives of patients diagnosed with lung cancer at a young age and in those with multiple affected family members. Other studies have found a lesser, but still significant risk for lung cancer in second-degree and third-degree relatives [78]. The increased risk in relatives of patients with early onset lung cancer appears to extend to non-lung malignancies [80].
Although the molecular basis underlying any familial increase in risk is not well characterized, progress in molecular epidemiology suggests that certain population subsets have a higher risk from certain environmental carcinogens, based upon both genetic and acquired susceptibility factors [81]. However, because no single genetic factor is sufficiently predictive, it is not yet possible to assess a given individual's risk on a molecular level [82].
Specific genes — Advances in molecular biology are beginning to identify specific single nucleotide polymorphisms (SNPs) or mutations that influence the risk of lung cancer.
INFLAMMATION — Chronic inflammation is associated with lung cancer:
DIETARY FACTORS
Antioxidants — An extensive body of literature suggests that low serum concentrations of certain antioxidant compounds, especially derivatives of vitamins A and E, are associated with the development of lung cancer [89,90]. Numerous epidemiologic surveys suggested that high levels of beta-carotene in the diet or in the blood were associated with a lower risk of cancer in general and lung cancer in particular [91]. In addition, an increased consumption of fruit, green and yellow vegetables, and possibly some micronutrients may be associated with a substantially lower risk of lung cancer, both among cigarette smokers and nonsmokers [92-94].
However, large chemoprevention trials using supplementation with retinoids, beta-carotene, and/or alpha tocopherol have not reduced the incidence of lung cancer and some have shown an increase in lung cancer. The results of these trials are discussed elsewhere. (See "Chemoprevention of lung cancer", section on 'Primary chemoprevention'.)
Flavonoids — The flavonoids are plant metabolites that have antioxidant, antiestrogenic, and antiproliferative properties. Sources include citrus fruits, parsley, onions, berries, tea, dark chocolate, and red wine. Observational evidence exists that suggests that flavonoids are protective against the development of lung cancer.
A prospective cohort study followed 2590 middle-aged men for a mean duration of 16 years [95]. Lung cancer was detected in 62 men (2.4 percent), all of whom were current or former smokers. The risk of lung cancer was lower for men in the highest quarter of total flavonoid intake, compared to men in the lowest quarter (adjusted relative risk 0.27, 95% CI 0.11-0.66). Out of five flavonoid subclasses, the flavonols and the flavan-3-ols were most strongly associated with lung cancer risk.
In another prospective cohort study, 34,708 postmenopausal women were followed for 18 years [96]. The risk of lung cancer was smaller for women in the highest quintile of flavanone intake (adjusted hazard ratio 0.68, 95% CI 0.53-0.86) and proanthocyanidin intake (adjusted hazard ratio 0.66, 95% CI 0.49-0.89) than women in the lowest quintile. Flavanones and proanthocyanidins are types of flavonoids. The associations existed only among current and former smokers, not among never smokers.
Cruciferous vegetables — Cruciferous vegetables are rich in isothiocyanates which have preventative properties against lung cancer in animals. Human observational studies suggest that vegetable consumption has a protective effect against lung cancer, with the best evidence for green cruciferous vegetables (eg, broccoli, cabbage). This protective effect is not definite, however, in view of the small size of the studies and potential confounding from other dietary sources [97].
To address these limitations, a multi-national case-control study of 2141 cases and 2168 controls was performed [97]. Participants were stratified according to their GSTM1 and GSTT1 status. (GSTM1 and GSTT1 are genes that encode enzymes responsible for eliminating isothiocyanates, the likely preventative compound). Weekly consumption of cruciferous vegetables protected against lung cancer in subjects that were both GSTM1 and GSTT1 null (odd ratio 0.28, 95% CI 0.11-0.67). Subjects that were null for only one of the alleles were also protected against lung cancer, but to a lesser extent. Subjects that had both GSTM1 and GSTT1 were not protected.
B vitamins — Deficiency of various B vitamins has been investigated as a potential factor in the development of lung cancer. In the European Prospective Investigation into Cancer and Nutrition (EPIC), serum levels of multiple B vitamins, including pyridoxine (vitamin B6), were compared in the 899 individuals who subsequently developed lung cancer and for whom full information was available [98]. Serum levels at baseline were compared with a matched control group of 1770 individuals. In this cohort, lung cancer developed an average of five years after study enrollment.
After accounting for smoking and other known risk factors, increasing levels of serum pyridoxine were associated with a statistically significant, progressive decrease in the risk of lung cancer (odds ratio of fourth versus first quartile 0.44, 95% CI 0.33-0.60). Similar differences were seen in smokers, former smokers, and nonsmokers. However, supplementation with B vitamins has not been shown to decrease the risk of lung cancer in randomized clinical trials, and additional study is required to clarify the role of relative deficiency in pyridoxine and other B vitamins.
Phytoestrogens — A possible role for phytoestrogens was suggested in a study of 1674 lung cancer patients and 1735 matched healthy controls [99]. Increased consumption of phytoestrogens was associated with a decreased incidence of lung cancer in both never smokers and current smokers. These findings are consistent with earlier observations that estrogens may have a protective role [100,101]. However, they require confirmation in prospective, longitudinal studies.
ENDOCRINE FACTORS — The impact of estrogen and progesterone on the risk and natural history of lung cancer is discussed separately. (See "Women and lung cancer", section on 'Endocrine factors'.)
BENIGN LUNG DISEASE — The coexistence of a number of benign lung diseases increases the risk of lung cancer.
Fibrosis — Individuals with diffuse pulmonary fibrosis have an eight to 14-fold increased risk for lung cancer, even when age, gender, and smoking history are taken into consideration [102,103]. Patients with prior asbestos exposure complicated by interstitial fibrosis (ie, asbestosis) are much more likely to develop lung cancer than patients with asbestos exposure alone [64,104].
Obstructive disease — Chronic obstructive pulmonary disease (ie, COPD) has been associated with a two- to six-fold increased frequency of primary lung cancer [105-107]. This appears to be particularly true for men [105,108]. In a retrospective study of 294 patients with newly diagnosed primary lung cancer, more men had coexisting COPD than women (73 versus 52 percent) [108].
Alpha-1 antitrypsin deficiency — In a case control series, carriers of an allele for alpha-1 antitrypsin deficiency (usually the S or Z allele) had an approximately two-fold increased risk of lung cancer [106]. Because of the prevalence of these alleles in this population, an alpha-1 antitrypsin deficiency carrier state was estimated to be a contributory cause in 11 to 12 percent of these lung cancer cases. (See "Clinical manifestations, diagnosis, and natural history of alpha-1 antitrypsin deficiency".)
Tuberculosis — There is observational evidence that pulmonary tuberculosis may be a risk factor for lung cancer [109-114].
The largest study is a population cohort study of over 700,000 individuals from Taiwan, based upon universal health care system claims [114]. Within this cohort, there were 4480 patients with newly diagnosed tuberculosis between 1998 and 2000, and the population was followed through 2007. The hazard ratio for an increased risk of lung cancer in tuberculosis patients after adjusting for sociodemographic factors and chronic obstructive pulmonary disease was 3.3 (95% CI 2.7-4.1).
While it is possible that tuberculosis-related inflammation and scarring contributes to the pathogenesis of lung cancer [113], it is also possible that pulmonary tuberculosis is merely a marker of the harmful effects of smoking. This is supported by studies that found that pulmonary tuberculosis is more common among smokers [115,116] and studies that found that COPD (like lung cancer) is more common in patients with prior pulmonary tuberculosis [117].
ONCOGENIC VIRUSES — A significant role for oncogenic viruses in the etiology of lung cancer has not been proven [118]. A viral etiology for one variety of lung cancer, bronchioloalveolar carcinoma (BAC), has been proposed, based upon similarity to a lesion seen in sheep. However, this has not been definitively linked to BAC in humans. (See "Bronchioloalveolar carcinoma, including adenocarcinoma in situ", section on 'Risk factors'.)
Subsequently, a potential causal role for human papillomavirus (HPV) in squamous cell carcinoma of the lung has been hypothesized because of the presence of HPV DNA within squamous cell carcinomas of the cervix, anorectum, skin, esophagus, and upper airways [119]. Studies analyzing specimens from patients with NSCLC have yielded mixed results [120,121].
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