Etiology of lung cancer: Evidence from epidemiologic studies

Kaiyong Zou; Peiyuan Sun; Huang Huang; Haoran Zhuo; Ranran Qie; Yuting Xie; Jiajun Luo; Ni Li; Jiang Li; Jie He; Briseis Aschebrook-Kilfoy; Yawei Zhang

doi:10.1016/j.jncc.2022.09.004

. 2022 Oct 4;2(4):216–225. doi: 10.1016/j.jncc.2022.09.004

Etiology of lung cancer: Evidence from epidemiologic studies

Kaiyong Zou ^1,^†, Peiyuan Sun ^1,^†, Huang Huang ^1,^†, Haoran Zhuo ², Ranran Qie ¹, Yuting Xie ¹, Jiajun Luo ³, Ni Li ¹, Jiang Li ¹, Jie He ¹, Briseis Aschebrook-Kilfoy ^3,^⁎, Yawei Zhang ^1,^⁎

PMCID: PMC11256564 PMID: 39036545

Abstract

Lung cancer is one of the leading causes of cancer incidence and mortality worldwide. While smoking, radon, air pollution, as well as occupational exposure to asbestos, diesel fumes, arsenic, beryllium, cadmium, chromium, nickel, and silica are well-established risk factors, many lung cancer cases cannot be explained by these known risk factors. Over the last two decades the incidence of adenocarcinoma has risen, and it now surpasses squamous cell carcinoma as the most common histologic subtype. This increase warrants new efforts to identify additional risk factors for specific lung cancer subtypes as well as a comprehensive review of current evidence from epidemiologic studies to inform future studies. Given the myriad exposures individuals experience in real-world settings, it is essential to investigate mixture effects from complex exposures and gene-environment interactions in relation to lung cancer and its subtypes.

Keywords: Lung cancer, Etiology, Epidemiologic study

1. Introduction

Lung cancer remains the leading cause of cancer death and continues to be among the most commonly diagnosed cancers worldwide¹. A recent analysis identified large regional and gender variations in the trends of age-adjusted incidence rates of lung cancer from 1978–2012 with 19 countries showing significantly decreasing trends among men and 26 countries exhibiting significantly increasing trends among women². In China, the age-adjusted rate of lung cancer remained stable among men and increased among women from 2000 to 2010³. In addition to sex and geographical disparities, histologic subtypes of lung cancer also showed apparent difference in incidence trends. In the United States, three major subtypes including squamous cell carcinoma (SCC), large cell carcinoma (LCC), and small cell lung cancer (SCLC) showed initial increasing trends from 1973 to 1980s and then started to decrease; in contrast, adenocarcinoma surpassed SCC in 1985 as the most commonly diagnosed subtype of lung cancer, with rates further increasing from 2003 to 2015⁴. In China, investigators have reported the same shift in histologic subtype incidence, with adenocarcinoma becoming the most commonly-diagnosed lung cancer there as well⁵. A recent study pointed out that an increased use of low-dose computed tomography (LDCT) among non-smoking Asian women was associated with overdiagnosis of lung cancer⁶. LDCT can increase detection of adenocarcinoma⁷, and would be expected to lead to an increase in adenocarcinoma out of proportion to other histologic subtypes.

Over the last decades, epidemiologists have taken significant steps to investigate the etiologic risk factors for lung cancer. While tobacco control programs have effectively reduced lung cancer incidence and mortality overall in many populations¹, the increasing incidence of adenocarcinoma and its spatial and gender variations underscore an urgent need to continue identifying the etiologic risk factors of lung cancer. In this review, we summarize the current evidence of lung cancer etiology from epidemiologic studies and discuss the challenges and opportunities for future epidemiologic studies of novel risk factors.

2. Smoking

Cigarette smoking is a well-documented risk factor for lung cancer⁸. A cigarette contains more than 70 carcinogens that have been evaluated by the International Agency for Research on Cancer (IARC) as human carcinogens, and the evidence of a causal relationship between lung cancer and cigarette smoking from epidemiologic studies has been summarized by IARC monographs⁸^,⁹. The risk of lung cancer generally increases with increasing duration and intensity of cigarette smoking, with a greater risk in current smokers than in former smokers⁹.

While earlier studies suggested a higher risk of lung cancer associated with cigarette smoking among women than men¹⁰^,¹¹, recent evidence supports a comparable risk between men and women12, 13, 14. Evidence of racial and ethnic disparities is mixed⁹, and variations in starting age of smoking, duration of smoking, cigarette filters, ingredients in tobacco products, and other lifestyle and environmental factors could explain some of the racial and ethnic differences in the association between smoking and lung cancer risk in other studies⁹. The Multiethnic Cohort Study in the USA found that while Japanese Americans had the lowest risk followed by Latinos, Whites and African Americans were among those who smoked no more than 20 cigarettes/day, and these racial and ethnic differences were no longer significant among those who smoked more than 30 cigarettes/day¹⁵.

The strength of association between smoking and lung cancer varies by histologic subtypes, demonstrating a stronger association with SCC and SCLC and a weaker association with LCC and adenocarcinoma¹⁶. A meta-analysis of 8 cohort and 14 case-control studies conducted in Japan showed proportionally elevated risks of SCC and adenocarcinoma among active smokers in men (RR = 11.7 and 2.30 respectively) and women (RR = 11.3 and 1.37 respectively)¹⁷.

Evidence linking non-cigarette tobacco products, such as cigars, pipes, and smokeless tobacco, to lung cancer risk has been less overwhelming¹⁸. Generally, studies support a positive association between cigars and pipes and lung cancer risk19, 20, 21, 22. However, the association between lung cancer and smokeless tobacco products has been inconclusive23, 24, 25, 26. One possible explanation for the inconsistent results is that smokeless tobacco consists of many different forms, such as chewing tobacco, Swedish snuff, etc., and the composition of different products varies²⁷. Studies have also shown that smokers who additionally used non-cigarette tobacco had a higher risk of lung cancer than exclusive cigarette smokers²⁵^,²⁶.

Electronic cigarettes (e-cigarettes) have been on the market since 2007¹⁸. Even though e-cigarettes produce lower levels of toxic substances compared to traditional cigarettes, long-term exposure to low levels of carcinogens released by e-cigarettes, including ultrafine particulate matter, polycyclic aromatic hydrocarbons, formaldehyde nitrosamines, and heavy metals might also pose health impact28, 29, 30. In addition, e-cigarettes can lead to nicotine addiction³¹. Although there is a lack of human evidence on long-term exposure to e-cigarettes and lung cancer risk, animal evidence showed that mice exposed to e-cigarette smoke for 12 weeks developed lung adenocarcinoma³², suggesting that future epidemiologic study of long-term exposure to e-cigarettes and lung cancer risk is warranted.

Exposure to secondhand tobacco smoke is associated with an increased risk of lung cancer⁸^,⁹. The most compelling evidence is from studies on exposure to secondhand tobacco smoke from partners⁹. Studies of secondhand tobacco smoke exposure in the workplace generally showed an elevated risk among those with the highest level of exposure⁸^,⁹. Limited evidence shows exposure to secondhand tobacco smoke during childhood associated with lung cancer risk⁹.

In summary, cigarette smoking is strongly associated with an increased risk of lung cancer in an exposure-response manner, and the strength of the association varies by histologic subtypes. Association with secondhand tobacco smoke is challenged by exposure assessment, particularly exposure to secondhand smoke in the workplace and during childhood. Elucidating additional interactions between other lifestyle and environmental factors would provide insights to inform tobacco control prevention strategies.

3. Alcohol consumption

Alcohol has been identified as a Group c by IARC⁹. Although alcohol is causally associated with cancers of the head and neck, esophagus, colon, rectum, female breast, and liver, the relationship between alcohol and lung cancer remains inconclusive⁹. Several meta-³³^,³⁴ and pooled-analyses³⁵^,³⁶ suggested a J-shaped association between overall consumption of alcohol per day and lung cancer. A recent large prospective cohort study conducted in China reported a significant exposure-response relationship between alcohol consumption and lung cancer as well³⁷, which is consistent with two previous prospective studies conducted in China reporting elevated lung cancer mortality among heavy drinkers after adjusting for smoking³⁸^,³⁹. This study also found a significant exposure-response relationship among both smokers and non-smokers³⁷. However, earlier studies generally reported no association among non-smokers⁴⁰.

Several studies investigating alcoholic beverage type and risk of lung cancer found inconsistent results³⁵^,³⁶^,41, 42, 43, 44, 45, 46, 47, 48, 49, 50, 51. Both a meta- and a pooled-analysis suggested an inverse association with wine consumption at low to moderate levels and an increased risk of lung cancer from beer consumption at higher levels³⁴^,³⁵. This meta-analysis also suggested an elevated risk associated with high consumption of liquor in men, but not in women³⁴.

Associations by histologic subtype are also inconclusive, with some studies reporting no association with any histologic subtype52, 53, 54 and others showing significant associations for certain subtypes⁴⁴^,55, 56, 57, 58, 59. An elevated risk was generally reported for SCC⁵⁵, adenocarcinoma⁴⁴^,⁵⁸^,⁵⁹, or both⁵⁶^,⁵⁷.

In summary, the relationship between alcohol consumption and lung cancer is inconclusive, although a weak or moderate association has been reported by some studies. Controlling confounding from smoking is paramount when studying alcohol and lung cancer risk. Investigations by histologic subtype and by beverage type are also warranted in future large studies with sufficient statistical power and detailed information on both active and passive smoking.

4. Occupational exposures

A number of industries and occupations, including mining, construction, metalworking, and driving, have been linked to an increased risk of lung cancer⁶⁰. Established occupational lung carcinogens, including asbestos, diesel fumes, arsenic, beryllium, cadmium, chromium, nickel, and silica, accounted for roughly 10% of lung cancer cases with large regional variations⁶¹. In China, an estimated 9.5% of lung cancer deaths were attributable to occupational exposure in 2005⁶².

Epidemiologic studies using occupation or industry titles to investigate occupational exposure in relation to lung cancer risk were prone to exposure misclassification. Workers who were classified under a specific occupation or industry title could be exposed to multiple agents and vice-versa. Likewise, an occupational/industrial title could entail very different exposure levels of a specific agent. Using a job-exposure matrix to link information from both occupation and industry titles with specific exposure agents would minimize the exposure misclassification and increase statistical power. Recent reports from two large pooled case-control analyses used the job-exposure matrix to investigate the exposure-response relationship between occupational exposure to diesel exhaust or crystalline silica and lung cancer⁶³^,⁶⁴. These studies found that exposure to diesel exhaust or crystalline silica was associated with lung cancer even at the lowest cumulative exposure level. As millions of workers are exposed to diesel exhaust and an increasing number of workers are exposed to crystalline silica while manufacturing stone countertops and sandblasting denim⁶⁵^,⁶⁶, these findings have significant public health implications and highlight the importance of occupational safety regulations and effective control programs to eliminate these exposures.

Night shift work leads to circadian rhythm disruption, which is associated with cancer initiation and progression, and has been classified as Group 2A human carcinogen by IARC⁶⁷. The few studies that investigated shift work in relation to lung cancer risk reached inconsistent results68, 69, 70, 71, 72, 73, 74, 75, 76, which could perhaps be explained by misclassification based on shift work and its co-exposures to other lung carcinogens, as well as incomplete control of confounding factors such as smoking. Sleep duration may modify the association between shift work and lung cancer risk⁷⁰, although the relationship between sleep duration and lung cancer is also inconsistent⁷⁰^,77, 78, 79, 80, 81, 82.

Non-occupational lung cancer risk factors may play a synergistic or antagonistic role with occupational factors. Studies have reported joint effects of smoking and occupational exposures, including diesel exhausts, crystalline silicas, and exposure circumstances as welders, bricklayers, and painters, in lung cancer risk⁶³^,⁶⁴^,83, 84, 85. Future large studies are needed to integrate both occupational and non-occupational risk factors to understand their interactions and mixed effect on lung cancer. Finally, the “healthy worker effect” should be considered when interpreting study results that compare the incidence or mortality of occupational settings to those of the general population, in which the true associations are likely to be underestimated.

5. Radon

Radon has been classified as a Group 1 human carcinogen by IARC based on sufficient evidence from epidemiologic studies reporting a strong exposure-response relationship between occupational exposure to radon and its decay products and risk of lung cancer⁸⁶. It is the leading cause of lung cancer in nonsmokers⁸⁶. Subsequent studies investigating exposure to residential radon and risk of lung cancer have generally supported an adverse association87, 88, 89, 90, although epidemiologic studies have encountered methodologic challenges to exposure assessment of residential radon concentration, which can be affected by the type and age of the house, renovation materials, ventilation capacity of indoor air, temperature, humidity, atmospheric pressure, and season⁹¹.

Studies investigating the association by histologic subtypes have generally supported an adverse association across all histologic subtypes as summarized by a meta-analysis⁹².

6. Air pollution

Outdoor air pollution and particulate matter (PM) in outdoor air pollution were classified as Group 1 human carcinogens by IARC in 2013 based on sufficient evidence from human and experimental animal studies, as well as mechanistic evidence⁹³. Several large-scale cohort studies with data on confounding variables (i.e., cigarette smoking) provided strong evidence of a positive link between ambient air pollution and lung cancer incidence and mortality94, 95, 96. A meta-analysis reported a statistically significant increased risk of lung cancer incidence in each 10 µg/m³ increase in PM_2.5 (RR = 1.09, 95% CI: 1.04, 1.14)⁹⁷. A recently updated meta-analysis including 20 cohort studies reported an even greater risk of lung cancer associated with PM_2.5⁹⁸. Although there was no significant heterogeneity in findings across studies where either fixed site monitoring or model-based approaches for exposure assessment were used, most of these studies were conducted in North America and Europe, where ambient exposure is lower; to date, very few studies have been conducted in Asia and other parts of the world with higher known exposure levels99, 100, 101, 102, 103. Several recent large epidemiologic studies also support an adverse effect of PM_2.5 and PM₁₀ on lung cancer risk104, 105, 106, 107, although two studies showed no clear association with PM due to lack of controlling for cigarette smoking¹⁰⁸ and short follow-up time¹⁰⁹.

In addition to PM, studies on nitrogen dioxide (NO₂), a marker of traffic-related air pollution, suggested an increased risk of lung cancer associated with increasing exposure to NO_2. These studies were summarized in two meta-analyses¹¹⁰^,¹¹¹. Several recent large epidemiologic studies provided inconsistent results, with some studies supporting an increased risk of lung cancer associated with exposure to NO₂¹⁰⁴^,¹¹², and others showing no association¹⁰⁶^,¹⁰⁹^,¹¹³. A recent study among postmenopausal never-smoker women reported an increased risk of lung cancer among those residing <50 m from primary highways, suggesting that other traffic-related indicators including ultrafine particles, particle-bound polycyclic aromatic hydrocarbons (PPAHs) and volatile organic compounds (VOCs) might contribute to an increased risk of lung cancer¹¹³. The few studies that investigated O₃ and lung cancer risk yielded inconsistent results¹⁰⁴^,¹⁰⁶^,¹¹⁴.

Household burning of coal and biomass fuel (primarily wood) has been classified as Group 1 and Group 2A human carcinogens for lung cancer, respectively¹¹⁵. Combustion of solid fuels is also a major contributor to indoor and outdoor air pollution, particularly in “developing countries” including China¹¹⁶. Epidemiologic studies conducted in China¹¹⁷^,¹¹⁸, North America, and Europe¹¹⁵ gave compelling evidence to support the relationship between coal combustion and risk of lung cancer. An updated review of epidemiologic studies reported a summarized OR of 1.17 (95% CI: 1.01, 1.37) for lung cancer associated with biomass for cooking and/or heating, and a higher risk among women in “developing countries” compared with “developed countries”, which was consistent with higher exposure among the former¹¹⁹. Exposure levels of indoor air pollution from combustion of solid fuels for cooking and heating are largely influenced by the type and quality of fuels, the type and condition of stoves, the type of ventilation and housing, the specific tasks and skill of the stove operator, and weather conditions¹¹⁵. Better exposure assessment is warranted to elucidate exposure-response relationship between solid fuels and lung cancer risk.

A limited number of studies have investigated air pollution and risk of lung cancer by histologic subtypes. A meta-analysis reported a stronger association of adenocarcinoma with PM_2.5 (RR = 1.40, 95% CI: 1.07, 1.83 per 10 μg/m³) based on three studies, and with PM₁₀ (RR = 1.29, 95% CI: 1.02, 1.63 per 10 μg/m³) based on two studies⁹⁷. Some - but not all - subsequent studies supported a stronger association between PM_2.5¹²⁰^,¹²¹, PM₁₀¹²², and adenocarcinoma¹²³. Further studies of the relationship between air pollution and lung cancer histologic subtypes are needed.

Evidence of the link between different components of PM and risk of lung cancer is also limited⁹⁷^,¹²⁴. A study using PM_2.5 oxidative burden, the product of PM_2.5 mass, and oxidative potential, which is the ability of regional filter extracts to deplete antioxidants glutathione or ascorbate in a synthetic respiratory tract lining fluid, reported a significantly increased risk of lung cancer mortality associated with glutathione-related, but not ascorbate-related, PM_2.5 oxidative burden¹²⁵. Several other studies reported a similar adverse association between various PM_2.5 components and lung cancer risk126, 127, 128. Several PM components including nickel, chromium, cadmium, and silica dust, as well as diesel engine exhaust have been classified as lung cancer carcinogens by IARC based on sufficient evidence in humans¹²⁹^,¹³⁰.

Very few studies have examined the combined effects of air pollution, cigarette smoking, and other lifestyle factors. The American Cancer Society Cancer Prevention Study II (ACS CPS-II) suggested a greater risk of lung cancer mortality among those with PM_2.5 and cigarette smoking exposures than what was expected from the sum of their individual effects¹³¹. European cohort studies found no interaction between ambient PM_2.5 or PM₁₀ concentrations and fruit consumption in relation to lung cancer risk⁹⁵. Studying the interactions of various lifestyle factors with air pollution in lung cancer risk has important public health implications. Future longitudinal studies with detailed information on confounding factors and modifiable lifestyle factors are needed.

7. Dietary factors

Epidemiologic studies investigating the relationship between dietary intake and lung cancer risk have reported mixed results. The variety of food frequency questionnaires used in these studies makes comparison challenging. Meta-analyses suggested a moderately reduced risk of lung cancer associated with greater intake of fruits and vegetables¹³²^,¹³³, soy-products¹³⁴, and fish¹³⁵, as well as a moderately increased risk associated with high intakes of red and processed meat¹³⁶^,¹³⁷. However, studies of supplementary nutrients including vitamin A, vitamin C, vitamin E, carotenoid, folate, selenium, and multivitamins provided no evidence of their protective effect against lung cancer¹³⁸^,¹³⁹. Two interventional studies indicated that beta-carotene supplements increased the risk of lung cancer among smokers140, 141, 142.

In addition to specific food items and nutrients, recent studies have also investigated dietary patterns in relation to lung cancer risk. Although definitions of dietary patterns differed between studies, healthy dietary patterns, generally defined as a diet rich in fruits, vegetables, fish, white meat, and soy products, have been linked to a reduced risk of lung cancer according to some studies reporting statistically significant results143, 144, 145, 146 and others showing non-significant results147, 148, 149. On the other hand, studies suggested an increased risk associated with a Western diet high in red meat and low in fruits and vegetables¹⁴⁷^,¹⁴⁸^,¹⁵⁰^,¹⁵¹.

In summary, the relationship between dietary intake and risk of lung cancer is inconclusive. The complexity of food items, variety of cooking methods, and variations in eating patterns over time make dietary exposure assessment extremely challenging. Future large prospective studies with longitudinally collected information on dietary intake are needed to elucidate the role of diet and its interactions with other lifestyle and environmental factors in relation to lung cancer risk.

8. Physical activity

Physical activity has proven benefits for prevention of many chronic diseases including certain cancers¹⁵². Epidemiologic studies investigating physical activity and risk of lung cancer, however, have reached inconclusive results. Studies generally supported an inverse association between leisure time physical activity and risk of lung cancer and its histologic subtypes, and found an inverse association mainly among smokers or men153, 154, 155, 156. The few studies that investigated household physical activity and risk of lung cancer reported no association¹⁵⁷^,¹⁵⁸. In contrast, the majority of studies investigating occupational physical activity and lung cancer risk found no significant association¹⁵⁷^,159, 160, 161, 162, 163, 164, except three studies reported a significantly increased risk associated with occupational physical activity165, 166, 167 and that one study showed a reduced risk¹⁶⁸. A recent meta-analysis suggested an elevated risk of lung cancer associated with high-level occupational physical activity compared with low-level occupational physical activity or sedentary occupation among men, but not among women¹⁶⁹.

The observed variations in the association between lung cancer and physical activity by different types of physical activity, by smoking status, and by gender highlight the importance of future research. Residual confounding due to lack of detailed information on smoking intensity and other environmental and lifestyle factors could be a potential concern. Reverse causation should also be considered. For example, a long history of unhealthy lifestyle (i.e., smoking) may cause subclinical cancer or respiratory conditions, which may in turn impede the ability or desire to exercise even years before the lung cancer becomes overt. Therefore, the disease process may be the cause of reduction in physical activity. On the other hand, degrading health might motivate the individuals to change unhealthy lifestyles and become more physically active. It is also essential to understand concurrent co-exposures when assessing occupational physical activity and to elucidate interactions between physical activity and other environmental and lifestyle factors in lung cancer risk.

9. Psychological factors

Few studies have explored psychological factors in relation to lung cancer risk, and the results have been inconclusive. Work stress is not significantly associated with increased risk of lung cancer¹⁷⁰. Early life stress measured as a parental death during childhood is associated with increased risk of lung cancer¹⁷¹. An early meta-analysis reported positive association between stress-related psychological factors and lung cancer risk¹⁷². A recent meta-analysis of cohort studies showed an increased risk of lung cancer associated with anxiety and depression with significant study heterogeneity¹⁷³. Depression has been linked to reduced immune function and increased inflammation, potentially leading to cancer development and progression¹⁷⁴^,¹⁷⁵. Individuals with anxiety or depression are also likely to smoke, drink, and be physically inactive and obese¹⁷⁶. It is essential to control these important lifestyle factors when studying the relationship between depression and anxiety and lung cancer risk.

10. Family history

Family history of lung cancer has been linked to an increased risk of lung cancer in the majority of published studies with an estimated twofold association177, 178, 179, 180. The strength of the association varied by geographic regions and certain sociodemographic factors as reviewed in a recent systematic review and meta-analysis, with a stronger association generally reported among Asians, younger individuals, ever smokers, and individuals with multiple affected relatives (Table 1)¹⁷⁷. Currently no strong evidence indicates significant difference in the association by histologic subtypes¹⁷⁸^,¹⁸¹. Although heritable genetic susceptibility could explain some of the association between family history and lung cancer risk¹⁸²^,¹⁸³, shared environmental and lifestyle risk factors as well as gene-environment interactions are also important contributors to the relationship¹⁷⁷.

Table 1.

Associations between genetic factors, family history and the risk of lung cancer and its subtypes.

	Loci^a	Family history^b HR (95% CI)
Lung cancer
Western	19q13, 15q25, 15q21.1, 10q23.33, 8p21.1, 6q27, 6p21, 5p15, 5q14.2, 4p15.2, 3p26, and 1p31.1	1.73 (1.58–1.89)
Asia	20q13.2, 20q11.21, 17q24.3, 13q12.12, 12q12.2, 10p14, 6p21.33, 6p22.2, 5q32, 5q31.1, 5p15, 3q28, and 1p36.32	2.14 (1.83–2.50)
Squamous cell carcinoma
Western	22q12.1, 13q13.1, 12q13.33, 9p21.3, 6p21, 4p15.2, and 2q32.1	1.55 (1.29–1.85)
Asia	12q23.1	0.65 (0.09–4.68)
Adenocarcinoma
Western	20q13.33, 18q12.1, 11q23.3, 10q24.3, 8p12, 5p15, and 3q28	1.70 (1.49–1.94)
Asia	5p15, 3q28, and 6p21	1.86 (1.34–1.94)
Non-small cell lung cancer
Western	–	1.72 (1.54–1.92)
Asia	3q29	1.76 (1.44–2.16)

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Western refers to European population.

Pooled summary estimates (95% CI) from Ang L et al¹⁷⁷.

11. Genetic factors

A number of genetic susceptibility loci have been identified by genome-wide association studies (GWAS) for lung cancer overall and for specific histologic subtypes over the past decade. Among European populations, 19q13, 15q25, 15q21.1, 10q23.33, 8p21.1, 6q27, 6p21, 5p15, 5q14.2, 4p15.2, 3p26, and 1p31.1 were significantly associated with lung cancer184, 185, 186, 187, 188, 189, 190, 191, 192, 193, 194, 195, whereas 22q12.1, 13q13.1, 12q13.33, 9p21.3, 6p21, 4p15.2, and 2q32.1 were associated with SCC196, 197, 198, 20q13.33, 18q12.1, 11q23.3, 10q24.3, 8p12, 5p15, and 3q28 were associated with adenocarcinoma¹⁸⁵^,¹⁹¹^,196, 197, 198, 199. Among Asian populations, studies have identified 20q13.2, 20q11.21, 17q24.3, 13q12.12, 12q12.2, 10p14, 6p21.33, 6p22.2, 5q32, 5q31.1, 5p15, 3q28, and 1p36.32 for lung cancer200, 201, 202, 203, 204, 3q29 for non-small cell lung cancer ²⁰⁵, 12q23.1 for SCC ²⁰⁶, and 5p15, 3q28, and 6p21 for adenocarcinoma²⁰⁴ (Table 1). Studies, mainly on Asian non-smoking women, have identified 17q24.3, 13q31.3, 12q13.13, 10q25.2, 6q22.2, 6p21, 5p15, 3q28, and 2p16.3 for lung cancer207, 208, 209, 210, and 18p11 for non-small cell lung cancer²¹¹ among non-smokers. These identified loci are mainly located in the regions related to smoking behavior, nicotine addiction, DNA repair, and immune response¹⁸⁶^,¹⁸⁸^,¹⁹³, suggesting potential directions for future etiologic studies. The effect size of most genetic associations reported in the literature was modest with an OR of ∼1.3¹⁸², although higher effect size has been reported in familial lung cancers¹⁸⁷. Considering small effect size of single genetic locus, Shen et al. constructed polygenic risk scores (PRS) and showed that individuals with high PRS (the highest 10%) had 96% higher risk of lung cancer than the lowest 10% (HR = 1.96, 95% CI: 1.53, 2.51), suggesting that PRS could be potentially used to identify high-risk populations for lung cancer²¹².

A growing body of literature has investigated gene-environment interactions and lung cancer risk. Studies using GWAS data to explore gene-environment interactions in lung cancer risk have identified loci on 15q22.32 and 14q22.1 that interact with smoking²¹³, loci on 6p21.32 and 3q28 with household air pollution²¹⁴, and loci on 22q13.31, 11q13, 7q32.1, and 2q34 with asbestos²¹⁵^,²¹⁶. A number of interactions have been reported by a study exploring interactions with occupational exposure to 70 agents²¹⁷. Although gene-environment interactions are likely to play an essential role in individual susceptibility to lung cancer²¹⁸^,²¹⁹, studies investigating gene-environment interactions are still in an exploratory stage due to the limitations of available study populations with sufficient statistical power and data on exposures.

12. Other factors

Several other factors have also been studied in relation to lung cancer risk, but to a lesser extent. Studies linking obesity to lung cancer risk reached inconsistent results. Two meta-analyses of prospective cohort studies showed that waist circumference, a simple yet sensitive indicator of obesity, is positively associated with lung cancer risk regardless of smoking status²²⁰^,²²¹. Compared with the normal category, the highest category of body mass index was inversely associated with lung cancer risk, but the inverse association disappeared for never smokers or SCC after stratifying by smoking status or histological subtype, respectively²²¹. A study covering 42% of the United States population reported an increased risk of lung cancer associated with low social economic status (SES)²²². The observed association is likely to be explained by confounding factors. Smoking is more prevalent among populations with low SES, which is associated with poor access to healthy food, hygiene, health insurance, and professional healthcare²²³. Another study from the United States found a significant negative correlation between lung cancer incidence rates in men and median income at state level, however, the significant correlation disappeared after controlling for smoking, age, and race²²⁴.

A growing body of evidence supports that sex hormones might play a role in the development of lung cancer²²⁵. Epidemiologic studies investigated menstrual and reproductive factors, hormonal contraception, and hormone replacement therapy (HRT) in relation to female lung cancer risk, and the results were inconsistent. A recent meta-analysis employing a combined indicator reported that exposure to higher levels of endogenous and exogenous sex steroid hormones was associated with a reduced risk of lung cancer among non-smoking women²²⁶. The higher levels of endogenous sex steroid hormone exposure were defined as younger ages at menarche, older ages at menopause, longer reproductive windows (only for postmenopausal women), longer menstrual cycle, pregnancy history, first pregnancy at younger ages, and multiple pregnancies. The higher levels of exogenous sex steroid hormone exposure were defined as use of oral contraception, use of HRT, and isoflavone intake from food²²⁶. One population-based prospective study among Caucasian men investigated androgens and found higher testosterone levels associated with increased risk of lung cancer²²⁷.

Infectious agents can activate inflammatory cells and inflammatory signaling pathways that facilitate the development of an inflammatory environment and subsequently promote lung carcinogenesis²²⁸. Mechanistic evidence supports that both bacterial (e.g., Chlamydophila pneumonia, Mycobacterium tuberculosis, Helicobacter pylori) and viral (e.g., human immunodeficiency virus, human papilloma virus, Epstein–Barr virus, cytomegalovirus, and influenza virus) infections may increase the risk of lung cancer, but epidemiologic studies have been limited²²⁸. A recent meta-analysis showed that previous lung diseases, such as asthma, chronic bronchitis, emphysema, pneumonia, tuberculosis, and chronic obstructive pulmonary disease, were associated with increased risk of lung cancer and its subtypes, and the association was stronger among older individuals and Asian populations²²⁹. On the contrary, a history of hay fever was associated with lower risk of lung cancer²²⁹.

13. Risk factors for non-smokers

Lung cancer among non-smokers has been considered as a different disease²³⁰. Approximately 15–25% of lung cancers occur in non-smokers, and the proportion varies significantly among different populations with a much higher proportion for women than men worldwide, particularly in South Asia²³⁰. A majority of lung cancer in non-smokers are adenocarcinomas²³¹. It is essential to evaluate the risk factors for lung cancer among non-smokers. Epidemiologic studies among non-smokers have generally supported an increased risk of lung cancer associated with exposure to second-hand smoke²³²^,²³³, radon²³⁴, PM_2.5⁹⁷, cooking oil fumes²³⁵, and family history¹⁷⁷. Limited studies have investigated occupational hazards and lung cancer risk among non-smokers²³⁶^,²³⁷.

14. Conclusions

As a result of previous studies, smoking, radon, air pollution, and occupational exposure to asbestos, diesel fumes, arsenic, beryllium, cadmium, chromium, nickel, and silica are well-established risk factors for lung cancer. Alcohol consumption, physical activity, obesity, dietary factors, social and psychological considerations, infectious agents, hormones, as well as complex genetic predispositions and interactions have also been suggested as contributing factors for lung cancer, although the roles of these factors are inconclusive.

Residual confounding from smoking and collinearity/multicollinearity due to co-exposures to correlated risk factors has been a major challenge for studying lung cancer risk factors, particularly those with moderate and low associations with lung cancer. Statistical approaches such as adjusting confounding factors to a finer degree, conducting stratified analyses, and performing mixture analyses are available solutions. In addition, given the complex exposure of humans in the real world, it is pivotal to understand the complex exposure patterns among populations and investigate the mixture effects from complex exposures and gene-environment interactions. To achieve this goal, detailed information from large and diverse populations is needed to provide sufficient statistical power to investigate multiple exposures and their mixture effects on lung cancer risk.

An emerging novel approach blending cancer primary prevention service and research through a digital platform may provide a cost-effective solution to the challenges in cancer prevention, including lung cancer. Chinese National Cancer Center recently developed the Smart Health Management Digital Platform for Primary Cancer Prevention (SmartHMDP-PCP), which can provide a tool to build personal exposure profiles for risk assessment, individualized cancer prevention recommendations, and alerts of cutting-edge scientific findings on management of behavioral, environmental, and psychosocial risk factors²³⁸. De-identified exposure profiles of consented individuals will be compiled into the unique epidemiologic databases that are customizable for analytics²³⁸. Implementation studies are needed to understand the effectiveness of SmartHMDP-PCP in lung cancer prevention.

Declaration of competing interest

The authors declare that they have no conflict of interests.

Acknowledgements

This study was supported by the Non-profit Central Research Institute Fund of Chinese Academy of Medical Sciences (grant number: 2021-RC310–009).

Author contributions

All authors contributed to writing and revising the manuscript.

Footnotes

Given their roles as Editor in Chief and Associate Editor, respectively, Jie He and Yawei Zhang had no involvement in the peer-review of this article and have no access to information regarding its peer-review. Full responsibility for the editorial process for this article was delegated to Mei Wang.

Contributor Information

Briseis Aschebrook-Kilfoy, Email: bkilfoy@health.bsd.uchicago.edu.

Yawei Zhang, Email: zhangya69@foxmail.com.

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PERMALINK

Etiology of lung cancer: Evidence from epidemiologic studies

Kaiyong Zou

Peiyuan Sun

Huang Huang

Haoran Zhuo

Ranran Qie

Yuting Xie

Jiajun Luo

Ni Li

Jiang Li

Jie He

Briseis Aschebrook-Kilfoy

Yawei Zhang

Abstract

1. Introduction

2. Smoking

3. Alcohol consumption

4. Occupational exposures

5. Radon

6. Air pollution

7. Dietary factors

8. Physical activity

9. Psychological factors

10. Family history

Table 1.

11. Genetic factors

12. Other factors

13. Risk factors for non-smokers

14. Conclusions

Declaration of competing interest

Acknowledgements

Author contributions

Footnotes

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